arrracr females (Wells and Schwartz l9B4)? In Blanchard's cricket frog(Acris ... males to locate one another, (2) that it preserves the species-species temporal information ...... forms of aggression is, arguably, likely to be favoured in a group that typically is long-lived ..... Brenowitz, F.,A,., Wilczynski, W. and Zakon,H. H., lgB4.
CHAPTER
1
Intrasexual Selection and Alternative Mating Behaviour Tim Halliday and Miguel Tejedo
l. ll. lll.
V.
lntroduction Fighting and Weapons Body-size Factors Affecting Male Mating Success and Selection on Male Size B. Factors Affecting Female Mating Success and Selection on Female Size C. Juvenile Growth and Age at Maturuity D. Sexual Size Dimorphism E. Conclusion
Vl.
Alternative Competitive Strategies A. Callers and Satellites in Anurans B. Sexual lnterference and Sexual Defence in Urodeles
Vll.
Sperm Competition
A.
lV. Other Forms of Sexual Dimorphism
S"*uo,
Non-aggressive Competition for Mates Calling in Anurans Threat Displays and Odours in Urodeles
A. B.
Vlll. Sexual Competition lX. Conclusions X. Acknowledgements
Xl.
Among Females
References
that..-o"t;.Ti:i::i::),."
rhar ravours characters giving serection is individuals a competitive advantage in terms of reproductive success over members of the same sex (Halliday 1978). The theory of sexual selection was developed primarily to explain the evolution of sexually dimorphic characters, especially those that are particularly large or elaborate in males (Darwin 1871; Arnold 1983). Intrasexual selection refers to selection that arises when there is variance in the mating success of one sex resulting from fighting and other forms of direct competition (Halliday 1978; Bradbury and Davies 1987). It is most commonly invoked to explain the evolution of larger body-size and specialized weaponry in males (Darwin 1871).
. Evolutionary biologists differ in their views as to whether sexual selection and natural selection are distinct processes (see, for example, Mayr 1972 Moore 1990), or whether sexual selection is a particular form of natural selection (Lack 1968; Halliday 1978, Igg2; Endler 1986). There is also debate about the value of making a dichotomy between intrasexual and intersexual selection (selection arising through variation in attractiveness to mates) (West Eberhard 1983; Halliday 1992; Andersson 1994). In a recent major review of sexual selection, Andersson (1994) argued that all manifestations of sexual selection arise from competition for mates, and identified five categories of mechanism of competition for mates (Table l). This chapter is primarily concerned with all these categories, except for IV (mate choice), which is discussed in Chapter 2 of this book.
AMPHIBIAN BIOLOGY
420 Table
1. Mechanisms of competition for mates, and traits likely to be favoured by selection among the competing sex (based on Andersson 1994).
in the competing
Mechanism
Characters favoured
I.
Early search and swift location of maies; well-developed sensory and locomotor organs. Ability to remain reproductively active during a large part of the season. l. Traits that improve success'in fights, e.g., large size, strength, weaponry, agility, threat signals. 2. Alternative mating tactics in inferior competitors, avoiding contests with superior rivals. l. Behavioural and morphological traits that attract and stimulate mates. 2. Offering of resources (e.g., nutrition, territories, nest sites) needed by the mate for breeding. 3. Alternative mating tactics, e.g., forced copulation. l. Mate-guarding, sequestering, frequent copulation,
Scrambles
IL
Endurance Rivalry
III.
Contests
IV.
Mate Choice
V.
Sperm Competition
sex
production of mating plugs, or other means of preventing rivals from copulating with the mate.
2. Ability to displace rival sperm; production of abundant sperm that outcompetes those of rivals.
Theoretical issues regarding the categorization of different mechanisms of selection are not of direct concern in this chapter. Rather, the focus is on competitive behaviour among amphibians in relation to mating, and on the evolutionary consequences of that behaviour. The chapter follows the approach advocated by Halliday (1992) in arguing that the evolution of sex-related characters cannot be understood purely through the study of sexual interactions, but must also embrace consideration of life-history variables and physiological constraints. In particular, it is emphasized that characters such as body-size are the result of many selective pressures related to life-history phenomena, such as fecundity and age. The chapter begins with a review of fighting behaviour among amphibians and a discussion
of the role of specialized weapons in the context of sexual competition (Section II). Section III presents a detailed discussion of the selection pressures that influence body-size in amphibians. Males and females are discussed separately and data on the way life history factors, such as fecundity and age at sexual maturity, influence body-size are reviewed. Much of the material in this section is concerned with factors that are not directly relevant to sexual competition, but it is our contention that sexual dimorphism cannot be explained solely in terms of sexual selection but can be understood fully only if the role of life history factors are taken into account. Sexual dimorphism is seen, not only in overall body-size, but also in specific morphological characters such as limbs, and these are reviewed in Section IV. Theory suggests that, when social competition occurs, selection will favour patterns of behaviour that minimize the potential costs of aggression. Section V reviews evidence in support of that proposition, notably in relation to calling in anurans. Section VI reviews studies of alternative mating strategies among amphibians, that is, patterns of behaviour that enable potentially less competitive individuals to enhance their mating success. Sexual competition occurs not only prior to mating, but. also subsequently, in the form of sperm competition. The rather few studies of sperm competition in amphibians are reviewed in Section VIL Males generally are regarded as the more competitive sex but there is increasing evidence that intrasexual competition is a feature of the sexual behaviour of females; Section VIII reviews such evidence for amphibians.
A striking feature of amphibians is that, despite there being widespread competitive behaviour in the context of mating, the classic evolutionary outcomes of such competition, large body-size differences and weaponry, are largely absent from the group. Broadly speaking, there are two possible reasons why sexual competition has not led to the evolution of such characters. One is that mating interactions among amphibians may not provide an opportunity for appropriate selection to occur. The second is that such opportunities occur,
HALLIDAYandTEJEDO: INTRASEXUAL SELECTION AND ALTERNATIVE
MATING
421
but they have produced dimorphisms different from those seen in other animal groups. For example, mating competition may not favour characters that confer an advantage within individual conte;ts, so much as favouring stamina, that is, the ability to engage in many such contests over a period of time (Halliday 1987). The class amphibia contains three living orders: Anura, Caudata (Urodela) and Gymnophoniona (Caecilia). Little is known about sexual behaviour of caecilians and they are rrot included in this review. Competitive interactions among anurans (frogs and toads) are often so different from those among urodeles (newts and salamanders), that, where appropriate, the two groups are considered separately.
II. WEAPONS AND FIGHTING Combat is a feature of the reproductive behaviour of many amphibians; typically males fight for females or for a resource that is a prerequisite for attracting females, such as a call siie, a territory, or an oviposition site. Among anurans, males of Acris crepitans blanchardi (Wagner 1989a) and Ranø uirgøtiþes (Given l9BBa) engage in wrestling fights over calling sites; in these bouts larger males have a clear advantage. In Oloþgon rubra, a lekking species, unpaired males attack amplectant males that females have actively chosen and, if they are larger than amplectant males, can displace them (Bourne 1992). In breeding aggregations of thJ European ðommon toad (Bufo bufo) rnales often greatly outnumber females and attempt to dislodge one another from the backs of females. Davies and Halliday (1979) found that nearly +6% of mating males obtained their partners by displacing a rival from amplexrls, in fights that last for añ average of seven hours (Davies and Halliday 1977). In the light of conventional sexual selection theory, it is a paradoxical feature of this and many other anurans that, despite the importance of fights ás a determinant of male mating success, males possess no morphological adaptations for fighting, such as weapons, and that they are smaller than females (Halliday 1992). The selective pressures that determine body-size are discussed in Section III of this chapter.
Theoretical discussions of fighting predict that the duration of bouts will be determined largely by the degree of asymmetry between contestants in characters that affect fighting ability, such as body-size, and also by the value of the resource being contested (Maynard Smith l9B2; Parker 1984). While the first of these predictions has been tested extensively (see Section V), tests of the second are rare. Verrell (1986) showed that, in the red-spotted newt (Notoþhthatmus airidescens.), the duration of wrestling between amplectant males and intruding malei of similar body-size is strongly correlated with the snout-vent length (SVL) of the female being contested; female SVL is correlated with fecundity.
Noble (1954) listed a number of male characters among anurans that may serve as as hypertrophied forelimb musculature, spines on the forelimbs, andtusks protruding from the lower jaw, but noted that the full significance of such sexually_ dimorphiccharacters largely is unexplained. Our knowledge of the functional significance of these èharacters has not advanced much in recent years; there have been few detailed studies of fighting behaviour in amphibians. adaptations for fighting, such
Many male anurans have longer, more muscular forelimbs than females and it has been suggested that it is forelimb length that is the character directly favoured by selection acting during fights over females (Howard and Kluge 1985). Because forelimb size is strongly correlàted with body-size, the positive relationship between male body-size and mating success may be an incidental correlation (Howard and Kluge 1985; Lee 1986). In a recent study of Ototygon rubra, Bourne (1992) suggested that it is the larger arms or certain males, rather than their overall body-size, that enables them to resist the attacks of rivals attempting to displace them from amplexus. The role of arm-length in sexual competition is discussed further in Section IV.
Many male anurans possess nuptial pads on the forelimbs that first appear at sexual maturity (førgensen 1992) and are developed most fully in the breeding season. There is considerable variation among species in the form of these secondary sexual characters; some
L
422
AMPHIBIAN BIOLOGY
of very small species have glandular pads, othery 1 sin_g]g ^thorn-like spine, others hundreds In some-sp9c!9s 1936). Trueb and Duellman ;þi"., (Smith"t95t; Noble t9b4; Tyler-1"976; (Smith 1951; chests on their structures similar have that breed in fast-flowing water, máles
enhance a male's grip on the female during Duellman and Trueb föAO). Nuptial pads ^by mo.re effectively ' In Rana temþoraria' females rivals atìacks resist him to u-pf"""r, enabling following mating (TRH, pers.-obs.). Savage chest tÉe on wounds deep with two are often left (1935) suggesred that r.rupiial pads are analagous to male weapons, þ:..u".t. of their role in àã-påtitiåfi for females, ånd r,rgg.sted that th.y ut" evolved most highly.in those species in^ which male-male compátition is"äost severe. Thomas et at. (1993) identified a category. of in some species, sexually dimorphic skiå glands, present in the nuptial pads of many taïa, and, ability to a male's enhance that seóredons elsewhére o.r th. body, ihat -áy ,..r.t" adhesive hold onto a female. some Structures that are functionally equivalent to nuptial pads also occur in the males of uiridescens Notoþhthalmus 1986); Trueb anã urodele species that have a-ple",rs iDuellman (Verrell t^ggZ) an¿ Taricha sp.ti.r (Davis andTwitty 1964) have keratinized excrescences on their hindlimbs and forelimbs, respèctively, in the breeding season. Pleurodeles wøltlhas similar structures on the upper forelimbs (Arnold 1972)' Among urodeles, male newts of the Asian ge2u2la.ramesotriton are highly aggressive and bite one añother in áquaria, without uppu.etrtly inflicting injury.(Sparreboom I9B4). Males of the newt- Triturus ,ittot , have been observed to bite ãnd inflict injuries on one another (Raxworthy tg3g), as have males of the salamander.Desmognathus ochrophaeus (Yettell and òorrouun íOOt¡, úut the occurrence and significance of such behaviour in a natural setting smaller are unknown. In the laboratory, larger maleã of D¿smognathus-ochrophaetu.sim.ply chase among is wirlespread territory igAA). Biting 11^d^1f.lt"_9f,a -u1., away from a female (Houck and and 19Bl) (faeger cineret'ts in Plethodon Éorestei tOos¡; pt.tfroao.riid salamand.., i1u"g., tail causing tail, the opponent's toward ì,n Euryrro cirrigera (Thomai 19"8g), bites are directed to leading grooves, nasolabial the toward and loss aád .onr.[rr.nt reduction in fat reserves, Aneides plethodo-ntid of the Males location. mate and reduced effectiveness of food intake head and fighting. involves a prolonged, forceful bite flaaipunctatus have a greatly enlarged oi.t.utiittg has been reported_among males fregggncy ñgh u doí"; inui pirs the opponeåt the European salamandrid Euþroctus asper of Males (Staub 1Þ93). field i" th" of thìs species the female by thrusting themselves from male the separate and pairs attack amplectant head-frrst between ih.-; older males may have a competitive advantage because of their proportionately wider heads (Thiesmeier and Hornberg 1990)' Among anurans, males of Hyh rosenbergi possess a prepollical spine on the forelimb with which they"may prr.,.t.rr. the eyes and earõ oi rival máles during fights in defence of a nest the and over f.-ulês (Kluge 198l). Males of several species possess psuedo-teeth, or tusks, in Australian the Iower jaw rhar arg abänt ol. i"r, well-developed in.l.-u.l"t.i -tp_":i:,t include t.rrk.d ¡.og (Ad,el,otus breais) (Tyler 1976), thè Brazilian hylid P@llodytes l!*9!": (Weygoldt lggl), u ,,iuil, monophyleiic ctãde of Rano, species from Asia, including R butli (Emerson and Voris 1992; Emerson 1994), and the South African bullfrog Pyxicepha-lus adsþ_ersus (passmore and Carrurhers l9?9j- Male Phyltod,ytes luteolus bite each other during fights are used to hold large prey iWeygoldr lg3l). The tusks (odontoid pro.eir.sj of Pyxic1phalus (Balinsky and Balinsky du¡rng.figlrts biting of iO,réfi-u" and Trueb t986), but observations suggest that sexual 1992), (Hayes-and.Licht iOf+¡, which is strongly urá.og..r-dependent are probably the result that Inþries evolution. tusk in imp"ortant çã-påtltio.r -uy hurr""úeen 'of of. Rana bþthi t!^.:iT.": field-collected from reported Ëeen haue males fights u-o.rþ (L,merson, pers. comm) and Pyicephølus ad,spersru (Channing et al' 1994). In the latter species Àghting hai bee.r reporred ur-potiibly causing death (Grobler L972). In the Rana clade studied by Emerson, a suite of male characters, comprising fangs, hypertrophied jaw muscles, errlarged head, and body-size grgajer. than the female's' has the ,lflu..d'the nirptial pads, adverti"r"-..rt call, vocal sacs, and body-size smaller than pattern feinale,s rypical of the råst of rhe genus. This appears to be associated with a re-p-roductive and irruolui.rg'purental care and malã defence of^a nest (Emerson and Inger 1992; Emerson Voris 1992; Emerson et al. 1993; Emerson 1994)'
HALLIDAYANdTEJEDO: INTRASEXUAL SELECTION AND AI,TERNATIVE
MATING
423
Weapons such as those described above seem to have evolved only rarely among amphibians. The paucity of observations of fighting probably reflects a number of factors, noábly that contests between individuals generally are resolved by other, non-injurious and less costly mechanisms (see Section V). Where fights do occur, as in Bufo bufo , often they are resolved by differences between contestants, notably in stamina or body-size, rather than by overt fighting or use of weapons. Systematic studies of aggressive behaviour suggest that levels of'aggression vary considerably as a result of a number of factors. In the African treefrog Hyperolius marrnoratu,s, aggressive interactions become more frequent as chorus size increases and nearest-neighbour distance decreases; aggression is also more frequent early in the evening, when males are establishing call sites, than later, when females are arriving at the chorus (Dyson and Passmore 1992). In a laboratory study, Forester et al. (1993) found that male Dendrobates pumilio became more aggressive with time of residence, an effect that reached an asymptote at about one week. In
is directed towards amplectant males, the frequency, may be affected by the duration of amplexus, interactions dìration and outcome of aggressive male to when she spawns. In Bufo bufo, this interval by a i.e., the time from a female's capture in fights over females is more marked when more male advantage is quite variable and a large manipulation (Höglund 1989) result of experimental as a fighting, either time is available for Bufo boreas, amplectant males In (Halliday, data). unpubl. factors climatic or because of in ravens; populations where such of predatory females in the presence release tend to respect to body-size, in contrast to is random with male mating success is intense, predation õther populations where, in the absence of ravens, Iarge males have an advantage (Olson sþècies
I
in which male
aggression
9B9a).
Amplexus in anurans and urodeles is a form of mate-guarding, comparable in function to that observed in many other taxa, notably insects (Thornhill and Alcock 1983). In anurans, effective defence of a female during amplexus insures that a male will fertilize her eggs when she releases them. The effectiveness of amplexus as a form of mate-guarding varies among species. For example, amplectant males are commonly displaced in Bufo bufo (Davies and Halliday 1979), whereas they are displaced very rarely in B. calømita (Tejedo 1988) and B. terrestris (Lamb 1984). In Notoþhtha,lmus airide.scuzs, displacements are also rare and are only successful when intruders are substantially larger than amplectant males (Verrell 1986). tn urodeles, amplexus prior to spermatophore transfer may serve three distinct functions: it enables a male to capture a female before a rival does; it then enables him to resist attempts to displace him from the female; finally, it reduces the risk that a rival will interfere at the stug. òf spermatophore transfer (Halliday 1990a). In both Notophthølrnus airidescens (Verrell t9B2) anlfarichaipp (Smith 1941; Davis and Twitty 1964; Propper 1991) the male stimulates the female by rubbing her with cheek and chin glands, respectively, until she signals that she is sexually receptive, at which point he dismounts and initiates spermatophore transfer. In Notophthaimrrr, t'h. duration of arnplexus is greatly increased if rivai males are present (Verrell' l983a); inTaricha, themaleholdsthefemaleinsuch away thathecancarryherawayfrom any rival males that come near. Taricha. is unique in that after spermatophore transfer, the male re-clasps the female and there is a prolonged post-mating amplexus. This serves as post-copulatory mate-guarding, the male continuing to clasp the female until she has signalled that she is no longer sexually receptive (Propper 1991).
III.
BODY-SIZE
Following the seminal review by Wells (1977a) of anuran mating systems, a plethora of field studies on toudr and frogs have been conducted in both tropical and temperate habitats. These studies arguably have made anurans the best-studied taxonomic group with respect to the mechanisms of sexual selection (See Chapter 2). Several genera from different families have been studied extensively, especially Bufo, Ranø and Hyla. Moreover, different populations of several species have been studied across a geographical gradient, and several populations have been itndi.d over several seasons, making it possible to examine variation in mating pattern within a species. Unfortunately, few populations have been studied in detail over
L-
424
AMPHIBIAN BIOLOGY
more than four seasons (an exception is Olson's (1989b) five-year study of Bufo boreas), and there is thus no direct assessment (as opposed to an estimate) of lifetime reproductive success for any anuran population (Howard 1983). Wells' paper stressed the role of sexual selection as a determinant of mating patterns, and two different approaches have been adopted by subsequent researchers. First, efforts have been made to measure phenotypic traits, such as body-size, that may affect variation in mating success in the context of sexual selection. Second, sexual selection often is assumed to operate only among males, and researchers have tended to neglect variation in female reprodictive success. This latter point is crucial to understanding the selective pressures that act on adult body-size in both sexes and in patterns of sexual dimorphism because body-size often is strongly correlated with fecundity in females. This sex-bias is mosr significant in longitudinal studies (covering at least two seasons) in which selection acting on the female generally is not considered, or if so, a simple relationship between body-size and fecundity is extrapolated. Exceptions include studies of Rana, catesbeiana (Howard 1983, 1988a) and Rana-syluatica (Floward and Kluge l9B5; Howard 1988a). Recognition that selective pressures operare on both sexes is crucial for an understanding of patterns of sexual dimorphism. Body-size often is correlated strongly with fecundity in females.
The focus of most field research thus has been the direct measurement of sexual selection on male traits that arises when some males gain an advantage over others in obtaining mates (Darwin 1871). This somewhat limited approach has been influenced by the view thaisexual selection should be regarded as a separate process from natural selection, as discussed above. Considerations of how life history traits may affect the expression of selection rarely have been tested or examined in depth in amphibians. For instance: Why are females normaily the sex showing delayed sexual maturity? Why do females skip reproduction more frequently than males? Under what circumstances is skipping reproduction ãdaptive? Why are sex ratios at breeding sites most commonly male-biased? Why are females larger in size than males in many species? Why, in some species, do the sexes not differ in size?
A.
Factors Affecting Male Mating Success and Selection on Male Size
The phenotypic trait most frequently -body length (snout-vent or snout-urostyle
measured in studies of anuran mating patterns is length). This readily obtained -easrrré þrovides a good estimate of body-size. Body-size is an important trait in many respects. Because of the inde.terminate pattern of growth exhibited by amphibians, adult body--size may reflecr age, but is generally more strongly influenced by juvenile growth rate (Halliday and Verrell 1g88; Platz and Lothrop 1993). It may be adaptive for females to choose larger males as mates because those males: (l) are older and have shown an ability to survive, (2) ha¿ fasterjuvenile growth, or (3) had a younger age at first reproduction (see Chapter 2). Larger male iize also may involve a direct benefit to females through the outcome of male-male inieractions (Davies and Halliday 1979; Howard and Kluge 1985), or females may enjoy higher reproducrive success because.larger males have better territories (Howard l97Ba, 19786, 1980i. In many lnYlan populations non-random mating with respect to body-size has been reported (see Table 2), and sexual selection may be implicated in the evolution of male body-sizé. However, some studies have shown that other aspects of reproductive effort in males may affect growth rates (Given l9BBa) or that male stamina is correlated with body-size (Tejedo 1992a1. Male þo$y-size therefore may be determined largely by processes associared *ittr tife history. It follows that an approach that takes into account all episodes of selection, all the benefiis in terms of reproductive success and all the costs in terms of survival must be adopted to explain the evolution of sex-related traits. Trade-offs between current and future lêvels of .éproductive expenditure may influence the size that males have attained by a given age. An overview of Table 2 reveals that there have been only 28 studies covering more than one breeding season. Of these, l2 populations exhibited variation in the intensity of selection on male body-qize and l6 showed a consistent trend in the action of selection. Ten populations had a constant_positive association between male size and mating success; in six, mating success was random with respect to size. Considering the data at the species level, and poolinf
HALLIDAY and TEJEDO: INTRASEXUAL SELECTION AND ALTERNATIVE
MATING
Table
SUCCESS
specific References
Mating pattern
Species
Prolonged breeders Alytes obstetricans A. obstetricans A. obstetricans Bornbina uariegata
Bufo calamita B. calamita B- canortn B. hotntonensis B. quercicw B. rangeri B. aerrucosissimus
ReadingandClarke 1988
0 0 0
++
0 0
0
+
B.
0
C entro lene IIa
co
C.feichmanni
Barandun 1990 Arak 1983a, 1988a DentonandBeebee 1993a
+
B. uoodhousü B. uoodhotnü wood,housü
Raxworthy 1990 Márqúez 1993
+
0
Kagarise-Sherman 1980 Hillis et al. 1984; Jacobson 1989
0
Woodward 1982a
+
Sullivan 1987 McDiarmid 1978
þmbipþ la
Greer and Wells 1980 Jacobson 1985 Jacobson 1985
C.f.eichmanni. C. prosobleþon C. ualerioi C hir om antis x e r amþ e lin a
McDiarmid 1978 ef al. 1992 Arak 1988a
Jennions
Rhac oþ honu Le uc omJS to,x E leutherodac ty lus c o qui E þip e d o b at e s e mor alis
E. triuittatus Hyla arborea
Townsend and Stewart 1994
Roithmair 1992 Roithmair 1994 MárquezandTejedo 1990 Gerhatdtet al. lg87 McAlpine 1993
f
H. cinerea H- cinerea H. chrysoscelis H. chrysoscelis H. chrysoscelis H. ebraccata H. faber H. gratiosa H. m.amorata H. rosenbergi H. uersicolor H. aersicolor H- aersicolor H. uersicolor
Wilbur ¿¿ ¿1. 1978 Cherry 1993 Tarkhnishvili 1994 Fairchild l98l
Godwin and Roble 1983
+
0
0
0
Morris l99l Martins 1993
0
0
Murphy 1994
+
Morris 1989 Ritke and Semlitsch 1 991
Lee and Crump
Kluge l98l
+ 0 0
0
l98l
Fellers 1979a Gatz l98la Hausfater¿f ¿1. 1990 Sullivan and Hinshaw 1992
Telford 1983
H1þeroliw mnrmorahs
Passmore and
H. marmorahrc H. marmorahts Physalemu þustuloxu
Telford and Dyson l9B8 Dyson et al. 1992
Pseudacrk crucifer P. crucifer P. regilla Rana catesbeiana R. catesbeiana R. catesbeiana R. clamitans R. úrgatiþes
Triprion
+
Ryan 1985 Gatz l98la Forester and Czarnowsky I 985
Perill 1984 Emlen 1976 Ryan 1980
+
+
0
+
+
þetaßatus
Uþeroleia rrigosa
Howard 1983 Wells 1977b Given 1988b Lee and Crump Robertson 1986
l98l
Explosive breeders Roberts 1994 Márquez 1993
Agalychnis saltator Alytes cisternasü
+
Licht I976
Bufo americanus
B. americc¿nus B. americanus B. americanus B. americanus B. americanus B. boreas B. boreas B. boreas B. bufo B. bufo B. bufo B. bufo B. calmita
L
Will¡r +
+
0
0
et al..
1978
Kruse l98l Gatz l98lb
Howard 1988b Sullivan 1992 1986 1986 Olson¿¿¿1. 1986 Davies and Halliday 1979 Reading and Clarke 1983 Arak 1983b
0+0
Olson
¿l ¿1.
Olson
¿l ¿1.
Höglund and Robertson 1987 Tejedo 1992a, unpubl.
425
AMPHIBIAN BIOLOGY
426 Table 2
-
continued.
Mating pattern
Species
Explosive breeders B. cognahr B. d,ebilis B. exsul B. gutteralis B. þardaLis B. þeriglenes B. terrestris B. terrestrß
B. tyþhonirc B. uoodhotuü
Hfla pseudopuma
Hlla pseudopuma Hflapseudoþuma Pelobates cultrþes Rana at-ualk R. syLaatica R. slLuatica R. syluatiea
R. temþoraria R. temþoraria R. temþoraria Scaphioþtts couchü S. couchü S. couchü S. couchü S. couehü S. couchü S. couchü S. couchü Spea muLtiþlicata S. multiþlicata S. nultiplicata S. multiplicata S. multþlicata S. muLtàþlieata
-
References
continued Sullivan 1983 Suilivan 1984
0 0
+
0
Kagarise-Sherman 1980
0
Telford and van Sickle 1989 Cherry 1992
+ 0
Jacobson and Vandenberg 1991 Wilbur¿r¿1. 1978 Lamb 1984 Wells 1979 Sullivan 1989 Crump and Townsend 1990 Crump and Townsend 1990 Crump and Townsend 1990
0 0 0
+ 0 0 0
0
0
Ltzanaet al. 1994 I. Hedengren, in Arak 1988a
0
+ + + + + + 0 0 0
+ 0 0 0 0 0
+ 0 0 0 0 0
+ 0
+
Howard 1980 Berven l98l Howard and Kluge 1985 Savage l96l Arak 1983b Elmberg 1987 Woodward 1982a Woodward 1982a Woodward 1982a Woodward 1982a
Sullivan and Sullivan 1985 Sullivan and Sullivan 1985 Sullivan and Sullivan 1985
Tinsley 1990 Woodward 1982a Woodward 1982a Woodward 1982a Sullivan and Sullivan 1985 Sullivan and Sullivan 1985 Sullivan and Sullivan 1985
*This table adopts the criterion of Wells (1977a) to distinguish between prolonged and explosive breeders. This is an arbitrary distinction and, wherever possible, the assessment given by the authors cited has been followed. Mating patterns: * : Positive association between male size and mating or hatching success 0 : Random mating effect of body size : Negative association between male size and mating success
-
data from different studies and thus several populations, there are 32 different species for which two or more seasons or populations can be compared. A consistent action of selection has been observed in 13 species but in only six has male mating success been found to be positively size-dependent. These are Abtes cisternøsü, Hylø rosenbergi, Physalaemus pustulosus, Rana catesbeiana, R. sylaa.tica, and R. airgøti'þes.
The factors that may influence the relationship between male body-size and mating success are numerous, and some may be stochastic in their effect.. For example, correlations between male size and operational sex ratio (OSR; defrned as the ratio of fertilizable females to sexually active males at a given time) (Emlen 1976; Emlen and Oring 1977) may generate a non-random mating pattern independently of the action of any mechanism of sexual selection. Another constraint on the action of selection on fhe phenotypic expression of male size would be a low degree of variability for that trait in the population. A direct test of this hypothesis
has nor beén made but presumably the pattern of indeterminate growth exhibited by amphibians, combined with variation in juvenile and adult growth rates, may determine that variation in male body-size is large enough to not constrain a non-random, size-related mating pattern.
Another factor that may affect the correlation between male mating success and body-size is the effect of alternative male mating-tactics which may reduce variance in mating success (see Section VI). If these tactics are size-dependent, any increase in their relative payoff may
HALLIDAY
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427
modulate the response to sexual selection favouring large size of males. One of the more widespread alternãtive mating tactics is satellite behaviour (see Section VI A). Where there is u pr.f"r"n.e by females foi larger males, smaller males may_adopt th^is tactic. Satellite beiraviour has bêen observed in mãny species belonging to several anuran families, including hylids (pierce and Ralin 1972; Fellers i975, 1979b; Perrill et al. 1982; Gerhardt et al. ISBT; úug,1"t 1989b), bufonids (Axtell l95B; Brown and Pierce 1967; Sullivan 1982a; Arak l9BBb; Krtipa t9B9; Tejedo 1992a) and the myobatrachid (lperolcin laeyigata $oþer1qo1 ^199.6) Satellite malËs are often Jmaller in size (Garton and Brandon 1975; Emlen 1976; Wells 1977b; Howard Ig/Ba, 1984; Fellers 19?9b; Forester and Lykens 1986; Tejedo 1992a) but sometimes they do nor differ in size from non-satellites (Perrill 1984; Roble l9B5). The relative paygffs for the alternative tactic are generally low (but see Forester and Czarnowsky 1985). The activities of satellite males, combined with imperfection in the expression of female choice for larger males, may result in a mating pattern that shows little or no consistent relationship with male size. Female choice for specific attributes of the call also may lead to variation in male mating success (see Chapter 2 õf this volume). Certain acoustic traits are related to male size and a preference for sich raits may produce directional selection favouring a shift .in the male acoustic traits does þh"notyp". However, the presente of a female preference^for size-related female p,re.ference for a studies, of In a number by size. mating not impiy non-random but no conditions, experimental under been established has male size related to éues acousti¿ such preference has been observed in a natural situation (Telford et al. l9B9; Dyson et al. 1992). Social or environmental constraints may thwart females' preferences so that males preferred by females under certain conditions have no mating advantage . under others iBo.r..r" 1992; Ryan and Keddy-Hector 1992; Chapter 2 of this volume). An interaction between call parameters may produce a negative correlation between different acoustic traits in terms of thèir attractiveness. This is the case for an intensity-dependent stimulus preference, where the attractiveness of a particular stimulus may be reversed by an increase in the intensity of the alrernative stimulus (S.hratt, 1986; Arak lg88c; Ryan and Rand 1990; Gerhardt 1991). The physical acoustic environment within a frog chorus alsornay impose constraints on the action oî female choice. Experimental manipulation of caller densities can produce an of preference at low dénsities but not at higher ones (Telford et al. 1989). Finally, expression ^many speciès mate acquisition is mediated by males activ€ly searching for females and by in that is not subject to selection through female -ul.r áaopting a silent iearching strategy 1992a). Tejedo l9B8b; (Fairchild Howard l9B4; choice An important factor that frequently has been shown to affect male mating success when it has been measured, is male atiendance at a breeding area (Table 3); indeed, in several studies it has proved to be a more significant correlate of male mating success than body-size or any other phenotypic character (Hattiday l9B7). For example, in Bufo calamita, chorus attenáance explained more of the variation in male mating success than male body-size in one study (Arak lg88c), while in another, the size-advantage observed by Tejedo (1992a) was because of its correlation with chorus attendance. Male stamina affects mating success by the simple addition of nightly probabilities of mating with a female. This factor is related to üfe-Ïistory elements of seieðtio.r and to trade-offs between growth and reproduction, rather than to sáection arising directly from mate competition. To be selected by females, this trait would have to be correlated with an acoustic cue that females can assess in male vocalizations' While it is potentially possible that females could assess male stamina by listening to them over a nr-Èer of nights, as has been suggested for birds (Hutchinson et al. 1993), there is no evidence that any feãture of a male's call that is apparent on a single night correlates with his stamina over several nights. Moreover, in many species females visit a chorus only for a single night and so cannot monitor males over longer periods.
An important consideration is that male endurance may be
correlated_ positively with
body-size. Such a relationship has been reported for Bufo americanus (Gatz 1981b), B. asþer (Hosie, in prep.), B. catamita (Tejedo 1992a), Rana temþoraria (Elmberg 1990) and, in one i.uron out;f four, Hyla chrysoscelii (Morris 19Bg). In a number of other studies, however, this relationship has not been'found: Bufo calamilø (Arak 1988c; Denton and Beebee 1993a),
þ-
AMPHIBIAN BIOLOGY
428 Table
3. Male endurance and mating success in anurans: evidence for a positive relationship between duration ofattendance at a breeding site and rnating success.
with a positive relationship
Species
Buergeria buergeri Bufo americanus Bufo calamita
Fukuyama and Kusano l9B9 Gatz l98lb Arak 1983a, 1988c; Tejedo 1992a;
Bufo gutteralis Bufo rangeri Bufo woodhousü
Telford and van Sickle 1989
DentonandBeebee 1993a
C e ntr
o I en
e
I Ia
f
.
e
ic hm
anni
la þr os o b Ie þ on C hir omantis xer amþ e Lina E leuther o dac $ Ius c o qui E þàþ edob ate s triuittans C entr o len
e
I
Cherry 1993 Woodward 1982b Greer and Wèlls 1980;Jacobson 1985 Jacobson I985 Jennionszfa/. I992 Townsend and Stewart 1994
Roithmair 19947
Hyla cinerea Hyla chrysoscelis
Gerhardtet al. 1987 Godwin and Roble l9B3; Morris l9B9*;
Hylafaber
Martins 1993
Hfla gratiosa
Murphy 1994
Ritke and Semlitsch 1991
HyLa rosenbergi
Hyla uersicolor Hyþerolius marmoratus P hy s alaemus þustulo sus
Rana uirgatiþes Species
with no relationship
Bufo uootlhousü Hyla aersicolor
Hyla
Kluge l98l Sullivan and Hinshaw 1992 Dysonetal. 1992 Ryan l9B3 Given 1988b
chrysoscelis
Sullivan 1987, 1989 Fellers 1979a Morris 1989+*
tPositive relationship is with number of days of calling activity, not with days of *In one out of four years. **[n three out of four years.
residence.
B. gutteralis (Telford and van Sickle 1989), B. woodhousii (Sullivan 1982b), Hfla chrysoscelis (Ritke and Semlitsch l99l), Hyþerolius marrnora.tus (Dyson et al. 1992), and Physølaemus pustulosus (Ryan 1983).
The energetic cost of mating activity has been measured in a number of studies in terms of weight depletion (Table 4). Weight loss per night is more marked in species with short or explosive breeding periods, such as Bufo bufo, B. calamita (in some localities) and Pelodytes punctatus, than it is in species with prolonged breeding periods, such as Bufo rangeri and Ra,na cl¡trnitans. A positive relationship between a male's body-size and his ability to sustain weight loss before having to leave a breeding site may lead to indirect selection for larger body-size in those species in which male attendance signifrcantly affects mating success. Weight changes over the course of the breeding season were monitored in samples of male and female smooth newts (Triturus aulgaris) by Verrell and Halliday (1985). There was marked variation among individuals, with weight changes between entry into and exit from a pond ranging from a loss of 65Vo to a gain of 35%. There was no difference between males and females and, across both sexes, weight change was positively correlated with time spent in the water; individuals spending a short time in the water lost weight, whereas those spend-
ing a long time gained weight. This pattern probably reflects the fact that the two major storage organs of newts, the fat body and the liver, decrease in size in the early part of the season, and increase again later on (Verrell et al. 1986). Some attention has been directed towards specific male morphological traits, notably forelimb size, that may influence male mating success, independently of body-size. Evidence that forelimb length is positively correlated with male mating success has been obtained from explosive breeders in which there is scramble competition for the possession of females (Howard and Kluge 1985; Lee 1986; Höglund and Säterberg 1989; Olson et al. 1986).
The relative size of males and females also has been shown to affect the fertilization rate
of mating pairs. Licht (1976) suggested that positive assortative mating by size should be favoured by selection, because the cloacae of male and female are closer together, leading
HALLIDAY
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TEJEDO: INTRASEXUAL SELECTION AND ALTERNATIVE
Table 4. Weight loss among male anurans
%
Species Bufo bufo B. cûIamitû
(UK)
Weight loss
TaWeight loss per
night
2r
1.07
13
0.32
Mean
number of nights 20
4l
|.7t
4.06 3.74 5.20
Reference
Arak 1983b Arak 1983b .Tejedo 1992a, unpubl. data Tejedo 1992a, unpubl. data
6.95 8.59 4.52
2.30 0.87
B. uoodhousü
ND
ND
Cherry 1993 Sullivan 1982b Cooke 1981 Ryser l9B9*
Rana temporaria (UK) R. temporaria (Swit.) R. clamitans Crinia (= Rani.della) signifera C. signifera
28 25
0.55
l0
0.r75
60
Wells l97Ba MacNally l98l
0.5
40
LemckertandShine 1993
C.
.JO
þarasigniftra
Pelorþtes þunctatus
JJ
20
5.86
429
during reproductive activity
B. calamita (Spain-88) B. rangerà
B. calo,mita (Spain-87)
MATING
1.55
3.85
MacNally l98l Tejedo and Reques, unPubl. data
*Weight depletion was nor only involved in mating activities. This value entails some additional postbreeding mass depletion. ND: no detectable weight loss during the breeding season'
to increased fertilization success. An optimal male-female size ratio that maximizes fertilization rare has been reported by some authórs (Davies and Halliday 1977; Robertson 1990; Bourne tg93) but has nãt been founcl in some species (Kruse 1981; Gibbons and McCarthy 1986; Gerhãrdt et al. 1.987; Höglund and Robertson 1987; Krupa 1988; Tejedo 1992b).
in which males provide parental care, male size may be correlated with reproductive ,'.r...rr, either because larger males provide superior paternal investment or because 1993). published dãta suggest, however., that among such they obtain more marings (Márque:z ^on s,u.ccess is variable. No relationship between male mating spe;ies, the effect of bäy-s¡r. in Eþþedobates femoralis and E. triuittatus (Roithmair found been has ,ir" uná reproductive suc;ess and C. lgg2, lgg¿), Centrolenellaf.ei:chmanni þrosobleporz (Jacobson 1985), or Eleutherodactylus has been reported in Hyla rosenbergz (Kluge advantãge male lu.g. A 1gB4). coqui, (Townsend 1993). (Márquez Alytes species two 1981) and Finally, a number of studies have reported e_vidence for heritable male genetic variation in importJnt larval traits that are likely tó affect fitness, such as duration of larval period and sire ai meramorphosis (Berven t9B7; fravis et at. 1987; Newman 1988). Any variation in male size that is assoìiated with genetic quality and non-random mating may lead to a genetic response in such larval traiis. The ássociation between adult male size and larval traits is varìable, however (Woodward 1986, 1987; Woodward et al. l9B7; Mitchell 1990; Woodward and Travis t99l; Semlitsch 1994). To date, there is no direct evidence for heritability of body-size in any amphibian species.
In
species
Factors Affecting Female Reproductive Success and Selection on Female Size Reproductive success in female amphibians is typically strongly size-dependent, larger females' producing more eggs than smáller ones. Generally, this trend is explained by an
B.
allometric function of the tYPe:
Y:a(x)b where a a¡1d å are constants (Gould 1966). ø gives the intercept and å gives the slope of the regression. The value of å indicates if the relationship is geometrically similar (isometric) or alËmetric. If the growth pattern is isometric, then b : I when x and y are linear measure-
ments, and b : ã when 1, is volumetric. Any deviations from this predicted t¡end would produce an allometric relationship; when the slope is greater than predicted, the response variable (fecundity) increases ut a high"r rate than the independent (any size-related) variable. Values lower than those predicted imply that reproductive output increases with body-size, bur ar a rare that is less than proportional to body-size (Peters 1983; Schmidt-Nielsen 1984). In many species the size-fecùndity relationship is allometric, implying that an increase in
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430
AMPHIBIAN BIOLOGY
female body-size is associated with disproportionately larger clutches. Examples include Rana temþorøria (Cummins 1986; Gibbons and McCarthy lÕ86; Elmberg lggl), R. syluatica (Berven l9BB) and Bufo calamita (Tejedo lgg2c). Another important determinant of female reproductive success is the level of investment made in individual offspring; a major componeni of such invesrmenr is egg size. Egg size is related to larval fitness in some species because it leads ro enhanced growth rãtãs (e.g., ,iåU1*o*o tølpoideum) (Semlitsch and Gibbons 1990) and large size ar metãmorphosis ix.äplan iggf ; Berven and Chadra lgBB; Semlitsch and GibbonJ IOOO¡ but the effeit is nor aþparent in others (Travis 1983; Crump l9B4; Walls and Altig 1986; Perranka et at. lg87; Andrén et al. 198-9; Tejedo and Reques 1992). Variation in egg size often is related to female size, bur the relationshþ is generally weaker than that with-clutch size, suggesting a stronger environmental effect (Cummins l986; Duellman and Trueb 1986; Gibbo.rr utrd MãCarthy lÞ86; Berven l9BB; Tejedo 1992c). Thus, larger females typically not only lay larger clurches tut also larger eggs.
Larger female size may, as in males, be a result either of greater juvenile growth or of greater growth after maturity- Age has been shown to be correlated with reprodu"ctive success in many female amphibians but such a correlation cannot be taken u, .rrid.n.. of a causal relationship because of the t¡pical correlation between age and body-size. It is thus necessary to tease apart size and age effects on reproductive success in order to differentiate the selectivä pressures that determine reproductive performance. Only a few studies have investigated the effect of body-size yhilg c^ontrylling for age (Semlitscn ÍoB5; Gibbons and McCartihy t9B6; Brcrven 1988; Tejedo 1992c). Results from these studies vary considerably, probably ú..urrr. different species respond differently to environmental conditions. Semíitsctr ltOaf) found that older females of Ambys.toma telþoideurn Iay proportionally larger eggs but not larger clutch sizes, whereas.larger females lay bigger clutches.-Gibbons and"McCãithy (1986) fõund that older females lay smaller clutches bui larger egg sizes; larger females of similar ág. u." -o.. fecund.. Similarly,-Berven (1988) found tñat older females-produce smaller clutch"es of larger eggs' Tejedo (1992c) found no correlation between fecundity and female age, but also"no variation in size; larger female¡ were more fecund. In súmmary, fecund"ity is generally -egg proportionalto body-size, but the effect of age on fecundity may be either negatiíe oriandom. Egg size is related most strongly to the availãbility of energy fór vitellogenesls which seems to increase as females become older. Genetic and environm"éntal .o-po"n".rts in reproductive traits in montane and lowland populations of wood frogs (Rana sytiatica) were exämined by Berven (1982a). The montane frogs had lower size-speiific fecuidity, bur produced larger
eggs than did lowland ones. In a reciprocal translòcation experiment bätween the À¡¡o populations,. frogs of montane origin produced larger and smalier eggs, both in their natal and in the alien environment, whereas ihose of lowland origin laid largä clutches and smaller jn both control-a^nd experimental sites. It was concluãed that tñe relationship between 98gs female bgdy-gi1e and fecundity or egg-size, as well as total clurch volume may be genetically fixed within different populations.
The timing of reproduction may yield differential payoffs in fitness for amphibians. For example, in anurans breeding in temporafy ponds, earlier breeders may have àn advantage because of reduced risk of their progeny becoming desiccated (Newman lg8g, lgg2) undu colpetitive advantage for earlier tadpole cohorts (Wilbur and Alford 1985; Morin lg3?; Alford 1989; Warneretal. l99l). If timeof breedingisrelatedtofemalebody-size,suchthat lu..q.I.females spawn earlier than smaller ones, this would increase the fitness of larger individuals. For example, Tejedo (1992c) found that smaller female naterjacks spawned la"rer that larger females. This implies a decrease in metamorphic success over ti"me, due to a higher .i:\ g{ pond desiccation as the season progressed. Nia.ry seasonally reproducing anurans which breed immediately after hibernation oi aestivation -uy rely on stored somatlc reserves to meet the e-nergetic demands of breeding (Rose 1967; Pierantoni et al. tgBB; Long 1982; Jørgensen 1992). Smaller females may postpone breeding within the breeding season È.cu.rr. they are energetically constrained by smallei energetic reserves, having devoteä more available energy to growth than^to reproduction. Alternatively, females may postpone reproduction as an adaptive- size-specifrc tactic that maximizes fecundity. Which'oi rhése stratägies females pursue would need to be investigated by appropriate experiments. In those sp..l.r in which
HALLIDAY and TEJEDO: INTRASEXUAL SELECTION AND ALTERNA:TIVE
MATING
431
reproduction is mediated by rainfall, dry years with early rains may mearr that not all females brèed, especially smaller ones. However, if rains are delayed, bigger and older females might skip breeding and younger ones could attain a reproductive advantage. The duration of the breeding season also may affect female reproductive success inasmuch as longer breeding seasons may allow repeated spawning. In species with prolonged breeding, in which reproductive activity lasts for two to three months or more, females may lay multiple clutches. This has been shown in several anuran families, for example: Hylidae: Hyla chrysoscelis (Godwin and Roble 1983; Ritke et ø1. 1992), Hyla cinerea, H. regilla and H. grøtiosa (Perrill and Daniel 1983), Pachymedusa døcnicol,or (Iela et ø1. 1986), Ranidae: Rana ilo*itont (Wells 1976), Rana catesbeiana (Errrlen 1977; Howard 1978b), Rana esculenlø (Rastogi et at. I9B3). Hyperolidae: Hyþeroli,us ai,ridif.aaus (Richards 1977), Hyþerolius marmoratus (Telford and Dyson 1990), Bufonidae: Bu.fo cøl,a,mita (Banks and Beebee 1986), Discoglossidae: Dßcoglossus þictus (Knoepffler 1962), Bombina aariegata and B. bombina (Obert 1977; Kapfberger 1984); Alytes muletznse's (Bush 1993); Dendrobatidae: Dendrobøtes granuliftrus (Crump 1972). Myobatrachidae: Cri,nia signtfera (Lemckert and Shine 1993). The Majorcan midwife toad (Atytes muletensis) can lay as many as six or seven small clutches in a season (Bush 1993). In urodeles, spawning occurs over an extended period in some members of the family Salamandridae, eggs being laid singly rather than in batches, e.g., Pleurodeles waltl (Gallien 1952), Triturus cristatus (Simms 1968), T. plgmaeus (Diaz-Paniagua 1989) and T. uulgaris (Baker 1992). In some of these species it has been demonstrated that larger females are prone to lay multiple clutches (Howard l97Bb; Telford and.Dyson 1990; Lemckert and Shine 1993) but in H. chrysoscelis, the size of females that lay a single clutch did not differ from those than produced more than one (Ritke et al. 1992). Amphibians are typically iteroparous breeders and although females may reproduce more than once in their lifetime, it cannot be assumed that they breed every year. The phenomenon of females skipping reproduction in a given year is not very well documented but, potentially, is a more important determinant of lifetime reproductive success than has previously been appreciated (Duellman and Trueb l986). In a review of amphibian breeding patterns, Bull and Shine (1979) found at least 24 urodele species and three anurans in which females alternate years of reproduction, or indeed, spend two or three years between successive breeding episodes. The selective forces that control this phenomenon and the implications of it for demographic parameters may be categorized into two different stages: before and after sexual maturation. Before sexual maturation, females may skip reproduction more as a life history tactic than as a response to environmental variability. In numerous amphibian species females delay the age of sexual maturity by one to three years later than males (see below). By delaying maturation, females attain larger body-size at first breeding with a resulting beneflt in reproductive performance. After maturation, all or a proportion of a reproductive population may not breed in a given year, as has been reported in both anurans (Bragg 1940; Blair 1943; Turner 1958; Heusser 1968; Licht 1974; Jørgensen 19BB; Olson 1989b; Jørgensen 1992; Denton and Beebee 1993a; Kagarise-Sherman and Morton 1993; Tejedo, pers. obs.) and urodeles (Vilter and Vilter 1960; Highton 1962; Gasser andJoly I972; Bull and Shine Ig79). This phenomenon seems to be sex-biased because females more frequently skip opportunities for breeding (Bull and Shine 1979; Olson 1989b; Elmberg 1990; Denton and Beebee I993a; Kagarise-Sherman and Morton 1993; Tejedo, pers. obs.). Theoretically, when a female skips breeding there must be a trade-off between losing an
opportunity to breed and any future benefit in fecundity resulting from a consequential
higher growth rate. This will depend on whether the probability of survival is higher or similar for females that skip years, compared to females that breed in successive years. A reduction in the frequency of breeding may be adaptive, especially for younger, smaller females which typically exhibit a higher growth rate. This strategy may be modulated by environmental conditions or by energetic requirements. In amphibians breeding in deserts or very temporary ponds, rainfall may determine pond duration, and this variable may have a direct effect on metamorphic success. It is predicted that, in such populations, skipping opportunities for breeding should be more common in dry years and less common in rainy ones. Finally, energetic constraints may modulate the schedule of female reproduction and determine
L-_
432
AMPHIBIAN BIOLOGY
wherher there is an annual or biannual vitellogenic cycle (Highton 1962; Bull and Shine lgTg). If there is a threshold level in the body resérves necessary to initiate_vitellogenesis, only females whose reserves exceed that threshold will breed in a given year. However, nothing is known about whether this is the case, or whether skipping breeding is either age- or sizedependent. Females also may skip reproduction because of the energetic cost of other activities ,,-,åh u, migration, egg brooáing^or iive-bearing, as has been reported for numerous urodeles (Bull and Shine 1979). In most amphibian populations that have been studied, males outnumber females in breeding aggiegations. Male-skewed sex ratios during breeding may. have important .onr"q.r..rås fä th"e structure of reproductive populations and for the potential for competition (Arnoid and Duvall l9g4). The osit is determinèd largely by the breeding sex ratio (Tejedo, unpubl.), and any shift in the breeding sex ratio may generate variations in the level of mate .oåp.tltion. Variation in sex ratio duiing breeding may þ: the consequence of (a) a sexual bias in survival rates during juvenile or mature stages, (b) variations in age at maturity or Iongevity between the sexesl or (c) the consequence of an asymmetric response of the sexes to ,rr.."rriue breeding events. No difference in survival rates between the sexes from one season ro the next hãs been found in a number of studies (Gibbons and McCarthy 1984; Berven 1990; Elmberg 1990). Within the breeding season, survival has been shown to be lower for males rhan fõr females in Cri,nia si.gnifera (Lemckert and Shine 1993). Breden (1988) provided one of the few available estimates of the sex ratio outside the breeding season, as ivell as in breeding areas, and showed that the sex ratio among adults was not statistically different fro- parìiy. Berven ( I 990) found lor Rana syluatica that the sex ratio at metamorphosis was not differËnt fiom parity. Patón et at. (1991) similarly found that the sex ratio before reproductio n in Røna pirezi was not male-biased. These data suggest that- sex ratios during bräeding are biased significantly compared with those in total adult populations. Variations in age ai maturity are ãnalysed below, but data on relative survival rates of the two sexes are too few for meaningful analYsis. C. Juvenile Growth and Age at
Maturity
Growth in amphibians, as in most ectotherms, is generally indeterminate, individuals continuing to grow throughout their lives. In numerous species, however, the onset of reproductive u.îiuitiãt is accomþanied by a sharp decrease in growth rate (Jørgensen 1992; Stamps lgg3). This reduction in somatic growth aiter sexual maturation has been recognized in both u.r.rrân, (Brown and Alcalá 1970;-Gittins et al. 1982; Hemelaar 1983, l9BB; Ryser t9B8' l98g) and urodeles (Houck 1977;Trlley 1980; Verrell l9B7a; Francillon-Vieillotetal. 1990). Ryser (lgBB) demonitrated that growrh in phalangeal bones (which is highly correlated with current Èody-size¡ decreases signifi"cantly aftêr matuladon. The,process of sexual maturation involves u .ort in terms of reiuced grówth, because energy allocated to gonad growth is diverted from stored resources or fiom resources that þreviously were directed solely towards maintenance metabolism and growth (Bernardo 1993). The correlatedresponse ofmaturation on growth rates may have imþorhnt implications for.fitness, especially for females where a rediction in growth rates may imply no increase in size and thus no increase in fecundity. This effect oñ growth is significani É".u.x. variations in the timing of rnaturity between the sexes may refleãt the differential degree of correlation between size and reproductive success in each Åex and may be responsible for much of the variability in the pattern of sexual dimorphism obserueá in amphbian breeding populations. Theoretical models suggest that ug" ui maturity evolves in ways that maximizè lifutittte reproductive success (Lande 1982; B?rnardo lgg3). Thus, age at maturity, with its associated cost in terms of growth, represents a trade-off between fecu"ndity, develópmental time and survival. Several models based on trade-offs between these traits give accúrate predictions of age at maturity in urodeles (Stearns and Crandall 1981; Kusano lggZ). Kusanô esdmated the optimal age at maturity for the salamander Hynobius nebulosus, as a function of the size-fecundity relationship' growth of immature aná mature animals, and the difference between pre-metamorphic and postmetamorphic survival. The value predicted by the model (5 years) corresponded to that observed in a natural population (Kusano 1982).
HALLIDAY and TEJEDO: INTRASEXUAL SELECTION AND ALTERNATIVE
MATTNG
433
The principal trade-off for females is that between an increase in fecundity resulting from in maturation and an increased chance of dying before maturity. For males the trade-off likewise is between increased mating success and increased risk of mortality. Because survival rate may be similar for both sexes (Gibbons and McCarthy 1984; Berven 1990; Elmberg 1990), the differential benefits in fecundity or mating success as a function of size may determine differences in the age at maturity of the two sexes. Because of the variability observed in the effect of male size on mating success, in contrast to the strong dependence of fecundity on female body-size, one can predict that delayed maturation will be more common in females than in males. A relative delay before first reproduction by females is a common pattern in amphibian populations and sometimes this delay may be as large as two years in comparison with first breeding in males (Table 5). Only in one population (Pelobates cultripes) have females been reported to breed at an earlier age than males. It is important to note that, in those populations where females breed later than males, the degree of sexual dimorphism is greater than it is in the other two groups (femaìes breeding at same age or before males, Í : 1.034 (SD : 0.062), a delay
N: 11;femalesbreedinglaterthanmales,i: 1.166 (SD:0.114),N: 12,U: 13,2:3.262, p : 0.001 I ; data for species with several populations were pooled). This suggests that the sexual
size dimorphism observed in adult populations is a correlated response to the differential age at maturity of the two sexes. In species where there is no difference in age at first breeding, sexual dimorphism in size may be the consequence of (l) an increased risk of mortality with age, (2) selection maximizing the number of breeding attempts made by females, or (3) differential growth rates after maturity (Lykens and Forester 1987). If the larval habitat is very uncertain and risk of desiccation is high, females that increase the number of reproductive episodes during their lifetime should be favoured by selection. A possible example is the natterjack toad (Bufo calamitø). This species breeds in temporary ponds where catastrophic mortalities are a common event
(Banks and Beebee 19BB; Tejedo 1992c). Size and age at maturity are species-specific but, rvithin species, may show considerable variation among populations. A good example of geographical variation in size at time of maturity is the common toad (Bufo bufo) in Europe. At least seven poplrlations have now been studied (Table 5); in most of them growth ceases at the age of first breeding but populations differ in both growth rate and in the age of sexual maturity. The relative contributions of genetic and environmental factors to such inter-population variation has been studicd very little in amphibians. One of the few examples consists of the reciprocal translocations made by Berven (l9B2a, b) of juveniles belonging to two populations of woodfrogs (Rana syh.tatica), one from the mountains and one from the lowlands. Montane individuals attained larger size at first breeding and were older than lowland frogs. This experiment showed that both in montane and lowland environments, frogs of high-altitude origin attained larger size at maturity than did frogs from the lowland population. Bernardo (1994) also evaluated the relative conf.ributions of genetic and environmental factors on populational variability in time of maturation and the body-size attained. He made a reciprocal transplant experiment between two populations of the salamander Desmognathus ochroþhaeus that differed in age and size at maturity (Tilley 1980). By raisingjuveniles in each of the parental habitats, Bernardo found that differences in maturation were independent of growth rate and that genetic variation in the timing of energy mobilization to mature gonads was responsible for the differential age and size at maturity in the two populations. Experimentally, he found that populational differences in age at maturation were not modulated by growth rates.
Hypotheses based on differential growth during the juvenile stage may predict variation in observed adult body-size. However, some evidence shows that larval environments may control both age and size at maturity in amphibians. Smith (1987), working with a hylid frog (Pseudacris triseriata), showed that individuals metamorphosing at smaller sizes and later in the season delayed sexual maturity. Larger metamorphs were also larger at maturity and larger, early metamorphs showed reduced age at maturation. Semlitsch et al. (l9BB) showed in a study of the salamander Ambystoma tolþoideum that larger juveniles were also larger at metamorphosis. Age at maturity was not related to time of metamorphosis in males but, in females, larger, early-metamorphosing individuals reproduced at a younger age than did small early-metamorphosing females. In the woodfrog (Ranø sylaatica), Berven (1990) showed that larger juveniles matured earlier and were also larger as adults. Larger adult body-size is associated with delayed metamorphosis in Desmognathus monticolø (Bruce and Hairston 1990).
434 Tabte
AMPHIBIAN BIOLOGY
5. Minimum age at maturation for different anuran populations.
Species
Female age at maturity
.1
2
2 2 2 2 2 3 3 2
2 2
,NS
2
0.989
2
1.058
2 3
l.033
Females breed before males* P e la b ate s cultr ip e s
Sexual size
Male age at maturity
(Spain)
dimorphismt References
0.996
Talavera l9B9
Females breed at same age as males* Bufo þentoni B. calnmita (UK) B. calamita (Spain) B. uoodhousü Hyla arborea Pelobates cultrþes
P. raraldü Pseudacris crucifer
Rana eascadae R. iberica R. temþorarial R. temþoraria2 R. temþoraria (Eire)
3 2 2
2
I
J
2 3
Francillonetal. l9B4
1.019 1.049 1.097
Denton and Beebee 1993 Tejedo 1989 Breden 1988 Friedl and Klump, in press Talavera l9B9 Talavera 1989 Lykens and Forester 1987
0.886
BriggsandStorm 1970 Esteban 1990
2
1.104 1.037 1.012 1.07
Bush 1993 Acker et al. 1986 Kalb and Zug 1990* Girtins et al. 1982 Hemelaar 1988 Hemelaar 1988 Hemelaar 1988 Hemelaar l9B8 Hemelaar 1988 Höglund and Säterberg 1989
2 2 2
Augert andJoly 1993
AugerrandJoly 1993 Gibbons and McCarthy 1984
Females breed later than males* Alytes muletensis Bufo americanu,s
B. americantu B. bufo (UK) B. bufo (F{olland) B. bufo (Germany) B. bufo (France) A. åtlo (Norway) B. åz/o (Switzerland) B. åzþ (Sweden) B. canoru,s B. þardalis B. tenu.cosissimus Ps¿udacris trkeriata Rana catesbeinn¿ (USA) R. c atesb ¿iøna (Canada)
R. þerezi (Spain 1) R. þerezi (Spain 2)
I
9
1.07
2
3
1.1
2
4
2
J
1.270 1.213
2 2
3
t.225
3
1.206
3
1.265
4
4 6
6
8
1.224 1.183
3
4
1.403
3
4
l.03
I 2
2 5
1.459
I
2
t-2
2-3
3
5
2
3
I
R. þretiosa
4
R. rid.ibunda R. slluatiea (USA) R. rylaatica (Canada)
2
2 5 J
R. temþ orarin (Switzerland) R. temþorøria (Spain)
l3
l.l5
l.l12 1.08
t.075
l 256
Kagarise-Sherman and Morton 1993 Cherry and Francillon-Vieillot 1992 Tarkhnishvili 1994
Smith 1987 Howard l98l Shirose ¿¿ ¿1. 1993 Esteban 1990 Patón et al. l99l
Turner
1960
Aleksandrosvskaya and Kotova 1986
I
2
l.l5
2
J
l.l3l
Berven 1988 Bastien and Leclair 1992
I
3 J
1.08 1.165
Ryser 1988 Esteban 1990
2
*Differences were established by comparing the frequency distributions of age at first reproduction for the two sexes (Kolmogorov-smirnov test, p < 0.05).-In some populations, some females breed one year earlier than stated. Modified from Cherry and Francillon-Vieillot (f 992). tsexual size dimorphism is calculated as female body length/male body length.
By manipulating larval densities in Ambystoma oþaturn, Scott (1994) showed that metamorphf from low-density conditions returned to breed at a younger age and a larger size than did those from high-density conditions. AIso survival to adulthood was higher in the low-density animals. Therèfore, adult body-size may be determined during the larval stage; annual and seasonal variations in aspects of the larval environment, such as temperature, population density and food level, may promote responses in the timing of and size at metamorphosis which will have profound implications for age and size at maturity. More long-term studies of cohorts of márked juveniles are necessary to fully understand this potential determinant of age at maturation and adult size. Age at maturity may be very plastic or may reflect the existence of a canalized phenotype for which there is a threshold in size or age at maturity (Bernardo 1993). Few studies have investigated either of these possibilities in detail. A reproductive size-threshold has been suggesied for the red-spotted îewt (Notoþhthølmn airidescens). A single cohort marked at metamorphosis matured at a variable age of four to nine years, but size at maturity did nor vary over a period of five years (Gill and Mock 1985). In woodfrogs (Rana syluatica),
HALLIDAY and TEJEDO: INTRASEXUAL SELECTION AND ALTERNA.IIVE
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435
Berven (1988) found that females, of the same cohort, but maturing at one or two years old, differed in size at maturity, those females breeding at two years old being larger. This suggests that there is no age- or size-specific breeding threshold in this species.
Amphibian growth rates decline with age (Jørgensen 1992; Hota 1994); consequently, any growth advantage gained by skipping reproduction for a year would affect the lifetime reprõductive success of younger individuals much more than it would that of older ones.
I). Sexual Size Dimorphism 90% of 589 (three mean families), 6I% of 79 species in urodeles, (belonging nine families), and to species in amphibians (Shine Because growth 1979). of males than that is greater body-size fèmale continues after maturation, hypotheses seeking to elucidate proximate determinants of sexual differences in body-size during the adult stage must consider various processes that may operate at different stages during ontogeny. There are two ontogenetic phases that may determine sexual size dimorphism (SSD) in the adult phase:
In amphibians females are generally larger than males. In anurans, about
during the juvenile phase may affect SSD in adults through either differential growth rates or a difference in age at maturity. 2. Proximate determinants resulting in sexual differences in growth rates or survival after
l.
Processes acting
maturity.
Growth during the larval phase typically accounts for a small fraction of total growth, representing only between 0.I% and l\Vo of average adult size (Werner 1986), but this proportion may be higher in some species. For example, nearly 30% of total average adult iize is achieved in the tadpole phase of the Majorcan midwife toad (Alytes maletensis) (Bush 1993). No study has yet been made to investigate to what degree SSD in adult size is explained by differential growth of males and females during the larval phase. The hypothesis that patterns of sexual size dimorphism are determined by mechanisms that act during the adult phase is based on two assumptions: first, that differential energetic demands on the two sexes affect growth rates and, second, that males and females show different mortality rates. Woolbright (1983) sought to explain SSD in amphibians on the basis of energetic constraints associated with reproduction in males. He suggested that differential energetic costs incurred by males during reproduction and a shorter time available to replenish reserves, in comparison with females, explains SSD patterns. An experimental test of this hypothesis which involved males of Eleutherodactylus coquibeing released from parental care duties, produced growth rates no different from those observed in females (Woolbright lg8g). The hypothesis that a difference between males and females in energy allocation during the reproductive season will result in differential growt.h rates between the sexes has been tested only rarely, e.g., in lizards (Nagy 1983). There is also no evidence for sexual differences, either in the physiological effrciency with which food is converted into useable energy for growth, or in intake of energy during the activity period, again based on studies of lizards (Hardwood 1979).
Another potential cause of SSD are differences in survival rates in relation to either body-size or age. Howard (1981) concluded that a higher predation risk among larger male bullfrogs (Rana catesbeiana) is responsible for the SSD observed in a natural population where females are the larger sex, despite the sexes exhibiting similar growth trajectories. This phenomenon may be important in those species where intensity of predation on one sex (e.g., males interacting in breeding aggregations) is high. Predation on males engaged in mating activity has been reported in several anuran species: Bufo americønøs (Schaaf and Garton 1970; Groves 1980), Rana cøtesbeiana (Howard 1978a), Bufo cønorus (Mulder et al. l97B; KagariseSherman 1980), Physalaemus þustulosus (Ryan et al. L98l), Scaþhioþru multiþlicatus and Bufo woodhousä (Woodward and Mitchell 1990), Hflø aersicolor and Pseudacris crucifer (Hinshaw and Sullivan 1990; Woodward and Mitchell 1990), Bufo boreas (Olson 1989a), Crinia signifera (Lemckert and Shine 1993) and Bufo exsul (Kagarise-Sherman l9B0).
436
AMPHIBIAN BIOLOGY
SSD also may arise as a result of intersexual differences in longevity, e.g., Bufo bufo (Hemelaar 1988). One way to test the hypothesis that SSD is determined by factors operating only during the adult stage would be to examine the correlation betweerr the _degree of SSD during the adult phase and observed variation in size dimorphism at the point of maturity (Shine 1990). Low values for this correlation would imply that mechanisms acting after maturation are clearly responsible for SSD, whereas a high correlation would suggest that factors affecting time and sire at maturity are ultimately responsible. There has been no such test for an a.nphibian but, in lizards sexual dimorphism in size at maturity is correlated highly with sexual dimorphism in average adult size (Stamps 1983), suggesting that selection affecting growth rates during the adult phase has no evolutionary consequences in terms of SSD. Previous hypotheses, such as those of Shine, Howard and Woolbright focused primarily on the potential-influence of sexual selection acting on male size. Selection pressures which might áffect female size largely were neglected. It is, however, unlikely that interspecific variation in size differences between the sexes can be attributed to variations in selection operating on one sex only (Harvey 19BB). SSD is not a trait in itself, inasmuch as selection dòes noi act on it directly, but rather is the result of different selective regimens acting separately on males and females. Arak (1988a) developed a model based on a multivariate
stádstical method for measuring selection on correlated traits, calculating the selection gradient (p) (Lande and Arnold 1983). The model assumes that. a trade-off between natural Jelection (survival) and reproductive selection (sexual selection plus selection for female fecundity) produces an optimal body-size. The model predicts that the magnitude of the difference in body-size between the sexes should be proportional to the difference in their reproductive selection gradients. Arak tested this model with data from nine anuran s-pecies and found that observed variation in SSD was explained by differences between male and female selection gradients. Arak's model fails, however, because it is unable to account for differences in the direction of SSD between species. In all species included in his analysis, females were larger than or equal in size to males, but reproductive selection gradients lvere usually larger in males than in females. For example, in Bufo bufo, the male reprocluctive selection giadient was 3.Bl whereas the female value was 3.42. Fernales, however, are 18% larger than males in terms of body length. Values of selection gradients probably vary within populations between seasons and between populations, especially among males. For example, a long-term study of mating patterns in à single Bufo bufo population suggests that larger males have a strong mating äduu.rtug" in some years, a weak advantage in others, and sometimes no advantage at all (Halliday, unpubl. data). For the natterjack (Bufo calamita), estimated selection gradients in the British pópulation studied by Arak (1988a) yielded a male/female ratio of 1.73, whereas an estimate, made over two seasons in a Spanish population, yielded a value of 0.98 (Tejedo 1989). The values of SSD were, however, the same in the two populations. Another caveat to bear in mind with this approach is that the measures of sexual dimorphism used were subject to error, because they wère estimated for populations for which the age distribution was unknown. In most of the species analysed, females delay maturity by one or two years relative to males. The indetermináte nature of growth in anurans makes measurements of selection of adult body-size less relevant than direct estimates of selection on growth parameters and on the timing of first breeding as a function of age or body-size (Arak I98Ba). The hypothesis that SSD is determined prior to sexual maturity implies thatjuvenile-growt! and age at maturity have been subject to differential selection in the two sexes. Halliday and Verreñ (1986, lgBBjsuggested that differences in life-history strategies between male and females, for example in age at first reproduction, may be respoirsible for variation in SSD. Amphibians exhibit indeterminate growth, implying that body-size continues to increase throughout life (Stamps 1993; Hota 1994). Most ofthe amphibian species studied grow after maturation towards attainment of a larger asymptotic size. This growth pattern has considerable implications for rhe expression of SSD in natural populations (for a comprehensive analysis see Stamps 1993). Sexual size dimorphism may arise in one of four ways (Fig. 1):
1. Males and females have the same growth trajectories but initiate reproduction at different ages, e.g., Rana catesbeiøna (Howard 198l) (Fig' la).
HALLIDAY and TEJEDO: INTRASEXUAL SELECTION AND ALTERNATIVE
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437
age of maturation results in the sex with faster reaching a larger asymptotic size, e.g., Bufo maturity growing and sexual delayed bufo (Hemelaar 1988), Ranaternþoraria (Gibbons and McCarthy 1984; Ryser 19BB) (Fig. 1b).
2. A difference between males and females in the
3. Age at maturity does not differ between the sexes but there is dimorphism in maximum asymptotic size with one sex growing more than the other, e.g., Pseudãcris crucifer (Lykens and Forester 1987) and Triturus marrnora.tus (Caetano and Castanet 1993) (Fig. lc).
4. There is no SSD in those species in which both age at maturation and asymptotic size are the same in the two sexes, e.g., Bufo calarnita (Tejedo 1989; Denton and Beebee 1993b) (Fig. ld).
To determine which of these models is applicable in a given instance requires gathering data on growth trajectories and age at maturity, for example by using the technique of skeletochronology (Smirina 1994). Ecological factors may have a profound effect on SSD that arises through sex differences in growth and age at sexual maturity. For example, aîy size- or age-dependent mortality in one sex may enhance or offset any SSD resulting from sexual differences in life history. In some populations of bullfrogs (Røna catesbeiana), growth trajectories do not differ but males mature earlier than females, leading to females being the larger sex. In addition, larger males suffer differential predation by turtles, increasing the degree of SSD (Howard 1981). Ryan (1980) reported a bullfrog population in which males are larger than females, an example of the plasticity shown by many amphibians in terms of life history variables. A factor influencing the estimation of SSD is potential sample bias. In studies of amphibians, samples of adults will be reasonably reliable if all sexually mature individuals congregate at breeding ponds, and ifjuveniles do not. However, distributions of body-size and age often may change temporally within populations (Loman and Madsen 1986; Sullivan 1987; Tejedo 1992c), and any cross-
sectional estimate problem.
of
SSD
in a breeding population must take account of this
f
(b)
(a)
potential
f
m
m q)
N
U)
o
A¡I
-
(c)
f
(d)
m
f m
Age Fig. 1. Growth trajectories in anurans; dots represent sexual maturity. (a) Males and females follow the same growth curve, but females mature later, and at a larger size than males. (b) Males and females mature at different ages, both showing reduced growth after maturity. (c) Males and females rnature at the same age but females continue to grow more than males. (d) Males and females follow the same growth curve and mature at the same age.
AMPHIBIAN BIOLOGY
438
E. Conclusion
Amphibians illustrate well the danger of making uncritical gerreralizations about the evolutionary relationship between body-sir. and sexual selection. Greenwood and Adams (lg8?) drew attention tó two fallacious assumptions commolly -19: in the literature: first, ìnut ií large male size is favoured in sexual competition, males will be larger than females; second, th"at if males are larger than females, thii must be evidence of intrasexual selection among males. The data preúnted and discussed in this Section reveal a number of reasons why, äespite there commonly being intense mating competition among male amphibians, females are more commonly the larger sex: 1. Large body-size confers a consistent mating advantage on males in only a few species. species, large size is advantageous but not consistently so, there being no such advantage in some years and at some localities.
2. In many
3. Attendance at a breeding site, which is not necessarily size-dependent, is often a more
important determinant of male mating success than is body-size' 4. Because of the strong relationship between fecundity and body-size, there is very strong selection favouring large size in females. 5. Females commonly delay breeding by one or two years relative to males, with the result that they achieve larger body-size at sexual maturity. 6. Any competitive advantage accruing to larger males may be obviated or subverted by other p.o..rr.r, such as female-choice foi male ðharacters other than size (see Chapter 2 of this iolume), and effective alternative strategies by smaller males (Section VI). Selection acts on individual phenotypes and any particular trait, such as body-size, is the result of numerous selective pr.rinr.r anã of the historical pathway that that trait has followed during its evolution (Harvey and Pagel 1991). Sexual size dimorphism is not-a trait on which selectón acts directly, but is the result of what are often different sets of selective pressures acring independently on the two sexes. Selection on male body-size is highly variable in direction and in intËnsity, u"¿ it may be constrained by a diversity of ecological and demographic factors, such as duration of the breeding season and the operational sex ratio. In contrast, is typically more uniform in direction and intensity, because of selection on female body-size 'between '6ody-size and measures of reproductive success such as the strong correlation fecundity and offspring size.
direct measures of individual variation in the lifetime More studies are needed that yield .fh" considerable longevity.of many amphibians, together reproductive success of amphibiani. wiih the marked temporal änd spatial variation observed in their mating patterns, means that such studies will need to be long-term.
IV. OTHER FORMS OF SEXUAL DIMORPHISM As noted earlier (Section II), many amphibians possess a number of characters that are prominent in males but absent or less well-developed in females. The role of such characters (Sassoon äs the nuptial pads of male frogs and toads (Blair 1946), the vocal apparatus of frogs and the (Sever 1976) of Eu;rycea cirri and mental qu?dridiglla'úø 19^86), rhe and KellËy lhnds typically are they fact that the in reflected is behaviour in ãexual newts male of crests dorsal strongly androgen-dependent, both at their first appearance in development and, sub,.qrr.îily, o., u"r.urorräl basis (Jørgensen 1992). In thè sexual selection literature, it has long beån the convention to attriËute the evolution of such characters, either to male-male competition or to female choice, but such a dichotomy is often untenable because many dimårphic characrers are involved in both kinds of sexual competition (Halliday.l990b' 1992' 1g93). This is perhaps best illustrated by the current acceptance of the term "advertisement" call, ín favour åf "-áting call", for the vocalizations of frogs, in recognition of its dual function of male secondary sexual characters 1WáUs ß77c). The roleäf female choice in the evolution is discussed in Chapter 2 of this book'
HALLIDAY and TEJEDO: INTRASEXUAL SELECTION AND ALTERNATIVE
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In Andersson's classification of mechanisms of mating competition (Table 1), scramble competition, a feature of many amphibian breeding aggregations, is predicted to favour enhanced sensory and locomotor adaptations in the competing sex. In European newts (Triturus) males use olfaction and, to a lesser extent vision, to find females and Cogalniceanu (1994) suggested that selection may have led to the evolution of an enhancement of these sensory modalities in males. In plethodontid salamanders, the nasolabial grooves that are important in olfactory location and recognition of mates and rivals (faeger and Gergits 1979) are larger in males than in females. In frogs the tympanum is generally the same size in both sexes, or larger in females, but in a few species it is larger in males; the functional significance of this variation is unclear (Duellman and Trueb 1986). Halliday (1975) reiterated the suggestion of Darwin (1871) that the deep tail and webbed feet developed by breeding males of some Triturus species are an adaptation that enable males to pursue and overtake females more effectively prior to courtship. Foot-webbing may serve an alternative or additional role as stabilizers during courtship and other vigorous activities (Beebee 1980; Halliday and Joly 19Bl). There is some evidence that the dorsal crests and deep tails of the larger Triturus species, such as T. cristahu (Hedlund 1990) and T. uittatus (Raxworthy 1989) may serve as threat signals in aggressive interactions among males. In Taricha granulosa males with deeper tail fins have a mating advantage (fanzen and Brodie 1989), although whether this is because they are better able to capture females or, having captured them, better able to guard them, is not clear. Once females have been intercepted by males and, in many species, restrained, they may be subjected to intense stimulation by the male (Houck 1986; Halliday 1990a). Among urodeles, competition for mates has favoured the evolution of a rich diversity of courtship glands and of mechanisms for their delivery to females (Arnold and Houck l9B2; Houck 1986; Halliday 1990a); these are discussed in detail in Chapter 2. Thomas et al. (1993) speculated that the sexually dimorphic skin glands of frogs may fulfil a similar "hedonic" function, as well as possibly enhancing a male's grip during amplexus.
II, the combination of elongated forelimbs, hypertrophied and nuptial pads can be regarded as characters that are favoured in forelimb musculature male-male competition for females. However, the hypothesis of Howard and Kluge (1985) and (Lee 1986) that forelimb length, rather than body-size is the character on which selection primarily acts was rejected by Emerson (1991) on biomechanical grounds. Howard (19BBb) found no relationship between arm-length and mating success among male Bufo antericanus. Sexual competition may not be the only selective pressure favouring these characters, however; Duellman and Trueb (1986) suggested that adaptations enabling males to grip females effectively are most highly evolved in species that mate in running water. As discussed in Section
Sexual dimorphism in relative hindlimb length, with males having longer hindlimbs, has been recordedin Bufo calamita (Tejedo, unpubl. data), and may occur in other anurans. The adaptive significance of this dimorphism is unclear. The shorter hindlegs of females may provide more efficient locomotion when they are gravid; the longer hindlegs of males may have evolved through male-male competition, giving males an advantage in searching for and chasing females. No such dimorphism was found in three Rona species by Esteban (1990).
A bizarre form of sexual dimorphism related to mating competition was studied recently
by Halliday and Hosie (in prep.). Males of the Californian newt Taricha torosø develop a smooth skin in the breeding season, and become greatly inflated with water, physiological changes that are mediated by prolactin (Deviche and Moore 1986; Moore et al. 1978). In breeding ponds studied by Halliday and Hosie, males greatly outnumbered females, and there was marked variation among males in their degree of hydration, measured by dividing their volume by their total length. In an experimental study in which pairs of males of equal length were allowed to compete for a single female, they found that males with greater hydration had no advantage in terms of capturing the female, but were better able to displace less hydrated males from amplexus, and to resist displacement themselves once they had gained amplexus. This form of sexual dimorphism is interesting because, unlike arm-length, it appears to be independent of body-size. The competitive advantage enjoyed by hydrated
AMPHIBIAN BIOLOGY
440
males is probably due to their greater bulk, but it also may be because their smoother, slippery skin is diificult for rivals to grip. e similar phenomenon appears to occur in the Asian salamander Hynobitn nigrescens, in which males compete to monopolize egg sacs rather than females (Éasumi ur,ä l*uru*a 1990; Hasumi 1994). During the breeding season, the head of the male becomes inflated with water. Males with a longer SVL have no advantge in monopolizing egg sacs, but those with larger heads do.
V. NON-AGGRESSIVE COMPETITION FOR MATES Competition between individuals for scarce resources, such as mates, is potentially costly to both *irrrr.r, and losers of contests. Costs may relate to energy expenditure, to time that is not spent on other important activities, to possible injury and, in extreme cases, to death of one ìr both participánts; all such costs may translate into an appreciable reduction in relative individui fitneis. A sophisticated body of theory has developed in recent years around the hypothesis that natural selècdon should favour forms of contest resolution that minimize fitness costs to contestants and maximize the benefits (Maynard-Smith and Price 1973; Huntingford and Turner 1987). In other words, selection should generally favour behavioural mechanisms that resolve contests quickly and by non-violent means. When fights between individuals do occur, for example between males over females, they are commonl"y resolved on the basis of some asymmetry between the contestants. A correlated asymmetry is one which refers to a phenotypic character- that has a direct bearing on the probability rhar an individual will win a contest, such as body-size. AT9"S T:rans larger (Davies and Halliday I9!7,.1979). An -ules .o--only win fights over females, e.g., Bufo bufo of contests but which does not outcome the influences that uncorrelated asymmetry is one residence of a territory is one prior fights; to win individual an reflecr the inheient ability of residents of a territory behaviour, territorial that show amphibians such asymmetry. Among (Given 1988b)' frogs Ranaairgøtþes the include examples intiuders; ouel .o--o.rly win hghts the salamander (Roithmair 1992) and and Epi,pedobates (C-rump 1988) Ateloþus u'ørius femoralis Plethodon cinereus (Jaeger et
al.
1986).
The duration of contests, and the degree to which they escalate toward potentially costly fighting, often is related to the extent to which the contestants are familiar with one another. titherã is some kind of correlated asymmetry between contestants, familiarity will generally lead to quicker contest resolution. Among anurans, the ability to _distinguish familiar neighbouis and unfamiliar animals has been demonstrated in the bullfrog Rana catesbeianø (Da"vis l9B7). Among urodeles recognition of familiar versus unfamiliar individuals has been àemonstraredin Ptelhodon cinereus $ãeger 1981). Individual recognition is only likely to be an important factor in the resolution of mating contests in those specìes in which the breeding ,.uio.r is prorracted suffrciently to allow individuals to establish stable spatial relationships. Together with theory about the evolution of aggression, sig_nalling theory has developed consideiably in the pasr îew years (Krebs and Dawkins 1984). In the context of aggression, conrests typically beþin with ãn exchange of threat displays which, theory predìcts, should convey iniå.-ution ãbo.rt the fighting ability of each contestant. To what extent the information sirould be reliable, as oppósed io "bluff', is a subject of debate (Maynard Smith and Harper lg88). The hypotheiii that the croaks produced by male toads (Bufo buþ) during fighiing reliably indicatè asymmetry in body-size, and thus can be used to resolve fights more qüi.Uyi was tested by Davies and'Halliday (1978). The..frequenry of these calls is strongly årr.út.d with male size and small males are physically incapable of producing the lowfrequency croaks of larger males. By using recorded calls of ,large_ and-small .males, and by size was not broadcast by their calls, Davies -rriing orre of the contãstants so that theii true an¿ fíaUi¿ay showed that male toads are less persiste_nt when attempting to displace an^ apparently lárger rival from the back of a femalé. Call frequency was, however, only one of ñr fights; fighting males are apparently also able to assess one another's relative thË crres "s.d size directly, probàtly Uy"visioñ and by the itrength of the kick they receive from their rival's hind-legs.
HALLIDAY and TEJEDO: INTRASEXUAL SELECTION AND ALTERNATIVE
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A. Calling in Anurans There is considerable variation among anurans in terms of the diversity and complexity of their vocal repertories (Littlejohn 1977). While a large proportion of species have a male advertisement call, a minority have, in addition, distinct aggressive or territorial calls and encounter calls. The advertisement call has two important functions: (1) announcement of occupied territory to other males of the same or different species, and (2) attraction of conspecific females (Bogert 1960; Littlejohn 1977). In the context of (2) anuran calls were widely rèferred to as mating calls but, following Wells (1977c) their dual function is now recognized by the term "advertisement call". The biphasic call of the co-qui lrog (EleutherdacQlus coqui) is highly unusual in that the auditory systems of males and females are specifically tuned to different parts of the call (Capranica I977). Males are tuned to the lower-frequency "co" note, females to the high-frequency "qui". Male anurans typically gather to call at sites suitable for females to lay their eggs; because such sites are commonly very restricted, large numbers of males may assemble and form choruses in which acoustic competition among males can be intense. Competition often is intensified by a male-biased operational sex ratio, caused by the fact that, whereas males typically spend several days or weeks at a chorus, individual females visit only briefly to mate and lay their eggs. Over the last 20 years, there have been numerous studies of acoustic interactions in anuran choruses, focussing on two related questions: How do acoustic interactions among males affect the ability of females to recognize, locate and choose among conspecific males? How do such interactions influence the ability of males to attract females?
The ability of females to locate males whose calls they prefer might be expected to be impaired in larger choruses. Evidence that this is so is provided by studies of the South African reed frog, Hyþerolius mørmorøtus; in the laboratory, females show a clear preference for the Iow frequency calls characteristic of larger males (Dyson and Passmore I988a) but, in the field, mating is random with respect to male size (Dyson et al. 1992). An experimental study by Dyson (1989) suggested that female preference in this species is expressed only when male chorus size is less than eight individuals. Gerhardt (1982) showed that, in Hyla cinerea, female preference for particular call frequencies is less marked in laboratory phonotaxis experiments in which females can choose among four speakers than in those in which they are required to choose between only two. Acoustic complexity may not be the only factor making it more difficult for females to express mating preferences in natural choruses. In many species, choruses contain a variable number of non-calling satellite males that seek to intercept females before they reach calling males (see Section VI A).
The size of a chorus also affects male behaviour in some species. For example, in small breeding aggregations of the natterjack toad (Bufo calarnitø), males call and attract females, although there is also a variable number of non-calling satellite males (Arak 1988b). In larger aggregations, however, males abandon calling and engage instead in scramble competition (Tejedo 1988). A similar shift from calling to scramble competition as breeding po¡rulalon srze rncreases occurs in the common toad (Bufo bufo) (Davies and Halliday 1979; Verrell 1983a; Höglund and Robertson 1988). Calling is an energetically expensive activity for males (Pough et al. 1992); consequently, many anurans adjust the amount of effort that they put into calling in relation to the number of competitors in a chorus. There are a number of ways in which males can alter their calls in response to competition from rivals, such as: increasing call intensity, increasing call duration, increasing note repetition rate, adding extra notes to the call, and adding new notes to the call (Wells 1977c Wells 1988). Numerous studies, using phonotaxis experiments, have shown that such alterations make male calls more attractive to females. For example: louder calls are preferred by female Hyla aersicolor (Fellers I979a) and Bufo cølamita (Arak 1983a); longer calls are preferred by female Hyla regilla (Whitney and Krebs 1975) and H. aersicolor (Sullivan and Hinshaw I992); higher call rates are preferred by female Bufo uoodhoruei (Sullivan 1983) and B. rangeri (Cherry 1993); and calls with added notes are preferred by female
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AMPHIBIAN BIOLOGY
(Ryan 1985). In all of these examples, female preference is such as to favour thosé males that invest higher levels of energy in calling (Halliday 1987). Male-male competition takes the form of competing to be attractive to females, rather than direct aggression, the more successful males being those that invest most in calling.
Physal.aemtn þustulosus
Male calls also are involved in maintaining spatial separation between individual males. Such separation will reduce acoustic interference, making it more likely that an individual male's cãil can be detected and located by females above the general noise of the chorus' Backwell and Passmore (1990) suggested that, in Aþixalus delicatus, males space themselves in a chorus such that minimum nearest-neighbour distance is 30-35 cm thereby insuring reduced acoustic interference and a clear pathway for females. Brenowitz et ø1. (1984) suggested that, in the spring peeper (Pseudacris crucifer) males space themselvg in a chorus rolhut the calls of their neighbours are just barely audible. Gerhardt et ø1. (1989), however, tested this hypothesis and found that, over a wide range of chorus densities, male spring peepers are spaced such that the amplitude of their nearest neighbour's call is well above their ãuditory thréshold. Male cricket frogs (Acris crepitans blanchardi) occupy calling sites and modify'their calls in response to recorded conspecific calls played close to them; such call modification appears to be a mechanism by which males space themselves (Perrill and Shepherd 1989). }y'rale Eleutherodactylus coqu'i also use calls to space themselves and fight only in dlefense of nests or retreats. In playback experiments, Iouder stimuli elicit an increasing number of aggressive calls in response, up to a threshold of B9-94d8, at which males become silent and move away from the sound source (Stewart and Bishop 1994).
In frog choruses, an increase in the number and density of calling males often leads to an increase in individual calling effort, as males compete to attract females, but it may also lead to an increase in the rate at which males interact aggressively. If males use their calls in aggressive interactions, they face an interesting dilemma: Can they alter their calls to make tñem more effective in aggressive interactions and, at the same time, maintain their ability to arrracr females (Wells and Schwartz l9B4)? In Blanchard's cricket frog(Acris crEinn^s blnnchn'rdi), males produce calls in distinct groups, with the duration and complexity of individual calls increasìng from the beginning to the end of a group (Wagner l989b). As chorus denslty increases, and nearest-neighbour distance decreases, so the sound pressure level perceived by
a male increases. Males respond to increased sound level by increasing call duration and
number of pulses per call, but this effect is more marked in the later calls in a call group than in the earlier ones. Wagner suggested that these changes represent graded aggressive signals; that is, such variations signal a male's preparedness to escalate an aggressive int.eraction. Furthermore, by selectively altering the calls produced later in call groups, males preserve the species-specific characteristics of the earlier calls. Wagner suggested that the early calls serve primarily to attract females, the later ones as aggressive signals between males. The role of call complexity in relation to the dual functions of aggression and mate arrraction has been studied in the reed frog Hyþerolirc tuberilinguis by Pallett and Passmore (l9BB). The advertisement call of this species consists of one to six click notes; the number of clicks increases with chorus size, but males rarely produce calls containing more than three clicks. In experiments in which males were played calls of varying complexity, subjects tended to match thè complexity of a stimulus call, but not to exceed it. Playback experiments with females showed that females prefer two- and three-note calls to simpler or more complex ones. It thus appears that males moderate their aggressive response to rival males, expressed as an increaselñ call complexity, in ways that minimize any decrease in the attractiveness of their calls to females. Increases in calling effort as a result of social competition not only incur an added expenditure of energy, but also may incur other costs, such as increased predation. In Physalaemus þustulosus, the addition of extra notes ("chucks") to their calls by males in larger choruses, not only makes those males more attractive to females, but also makes them more susceptible to attack by predatory bats (Ryan 1985). In many frog species, males in denser choruses adjust their calling behaviour in ways that avoid acoustic overlap between their calls and those of their rivals, with neighbouring males tending to alternate calls. Examples include the fire-bellied toads (Bombinø), in which the
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neurobiological basis of call alternation has been investigated (Walkowiak 1992) and Bufo wood.howäfowleri (Given 1993a). Schwartz (1987) tested three hypothesis for the function of call alternation: (1) that it facilitates inter-male spacing, making it easier for neighbouring males to locate one another, (2) that it preserves the species-species temporal information coded in the call that attracts conspecific females, and (3) that it makes it easier for females to locate individual males. Schwartz used data from three species, Pseudacrk cruciftr, Hyla uersicolor and 11. microceþhøla, to test these hypotheses. Males of all three species produce more aggressive calls in response to high-intensity advertisement calls that alternate with their own calls than they do to similar calls that overlap their own, supporting hypothesis (l). Choice experiments involving four speakers using alternating and overlapping calls provided evidence that preservation of signal integrity is importan t in H . aersicolor and 1{. microceþhalø, supporting hypothesis (2). In playback experiments, females did not discriminate between alternating and overlapping male calls, rejecting hypothesis (3). Likewise, call alternation does not enhance location of males by females in Hyþerolius marmorøh.ts (Passmore and Telford lg8l), Pseudacris uuciþr (Forester and Harrison 1987), Afrixølus delicatus (Backwell and Passmore 1991) and Bufo woodhousi.i.fowleri (Given 1993a).
In Hyla microceþhala. chorusing males tend to call in unison, with distinct bouts of calling separated by periods of silence (Schwartz 1991). Indirect data suggest that males to conserve energy by periodically ceasing to call. During calling bouts, males adjust the timing of their multi-note calls in ways that avoid acoustic overlap with their nearest neighbours. When the calls of neighbouring males do overlap, females may prefer either the leader or the follower in the association, thus promoting male competition to be the first or the last to call, respectively. Female preference for leader males has been demonstrated in Hyþerolius marmorctttts (Dyson and Passmore l9BBb) and Hyla cinerea (Klump and Gerhardt 1992); preference for follower males has been found ín H1lø ebraccatø (Wells and Schwartz 1984).
In some frog species, aggressive interactions among males involve the use of aggressive calls that are distinct from advertisement calls. In Hyla rnicrocephølø, aggressive calls are more variable than advertisement calls (Schwartz and Wells 1985). In playback experiments, males increased the duration of the introductory note of their aggressive calls in response to increasing intensity of conspecifrc advertisement and aggressive calls. The use of graded aggressive calls that signal variation in a male's aggressive motivation has been studied in detail in
Acris
crepitans blanchardi (Wagner 1989a, 1989b, 1992). In this species, males defend call sites by fighting, during which aggressive calls are produced. The dominant frequency of male calls
is correlated negatively with body-size, but individual males also are able to vary dominant frequency over a certain range. AsinBufo bufo (Davies and Halliday 1978), males can assess the size of their rivals on the basis of the frequency of their calls, but unlike B. bufo, they reduce the frequency of their own calls in response to the deeper sound of larger opponents. By means of experiments using synthetic calls, Wagner (1992) showed that the initial frequency of a male's call at the start of a flght signals his body-size to his opponent, and that the degree to which the frequency is lowered during the fight signals a male's readiness to fight, a variable largely independent of body-size. Male carpenter frogs (Rana airgøtiþes) have a complex vocal repertoire that includes a one- to ten-note advertisement call, a single-note and a multi-note aggressive call, and a growl given during wrestling (Given 1987). Both the dominant frequency and intensity of these calls are correlated with body-size, larger males producing deeper and louder sounds, but these correlations decrease at larger body-sizes. In playback experiments, male aggressive responses increase as stimulus intensity increases and males respond more strongly to the sounds of small males than to those of larger ones. Small males generally retreat in response to auditory signals.
In addition to advertisement calls and territorial and aggressive calls, an additional kind of call, produced in male-male interactions, has been identified in some species (Littlejohn 1977; Wells 1977c). These "encounter calls" occur in territorial interactions in which two males are close together, and they may be elicited by visual or vibrational, as well as acoustic Territorial and encounter functions may, however, be combined in the same call in some
cues.
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(Littlejohn 1977). Encounter calls have been described for Pseudacrk (Hyla) regilla by Allan (1973) and have been studied by Brenowitz and Rose (1994). Males are spaced such species
that the sound of an individual's nearest neighbour is at a threshold level, defined as the lowest amplitude that will elicit encounter calls. This "aggressivel? threshold is not frxed, but varies accòrding to the social context. If the nearest neigbour is.removed, the threshold falls, so that males would then become responsive to more distant males. If the nearest neighbour is replaced by a super-loud stimulus, the threshold rises. This effect is not due to sensory adãptation but appears to be a mechanism that enables males to respond selectively only to near neighbours at different chorus densities.
The examples discussed so far primarily have been of species in which males form choruses in which their attendance usually lasts only a few nights and in which they do not defend resources of reproductive value to females. In some anurans, males defend territories over long periods and these provide sites where the eggs develop, in some species (e.g., dendrobatids) cared for by one or both parents. In such systems, territories are defended by persistent calling which may also signal male quality to females; examples include Dendrohates granul,iftrus (van Wijngaarden and van Gool 1994), Eþipedobøtes femoralis (Roithmair 1992) and E. triaittatus (Roithmair 1994). Studies of acoustic interactions in anurans have proliferated exponentially in recent years, largely as a result of the development of experimental paradigms using natural and synthetic calls in playback experiments. From this exterìsive literature, only briefly reviewed here, it is clear that many anurans possess rich and sophisticated communication systems in which acoustic signals are used to resolve contests for territories, call sites or females, and thus to reduce the incidence of fighting. Because advertisement calls also attract females, variation in their acoustic
properties often represents a trade-off between maximizing their attractive properties for females and maximizing their effectiveness in resolving contests. Because calling is energetically very expensive, variation also reflects trade-offs between maximizing the effectiveness of communication and minimizing energetic costs. B. Threat Displays and Odours in Urodeles
Social communication in urodeles is affected primarily through olfactory, rather than auditory cues (Halliday 1990a; Houck and Verrell 1993; Jaeger and Forester 1993). Superficially, urodeles do not appear to engage in social interactions as complex as those of anurans, but this probably does not reflect biological reality so much as the fact that salamanders have been studied less often, olfactory signals being less amenable to experimentation than are auditory ones. Jaeger and Forester (1993) suggested that the social life of plethoclontid salamanders is just as rich and complex as that of other vertebrate taxa.
In a study of aggressive interactions in Aneides f,aaipunctatus, Stawb (1993) identified no less than l2 distinct attack or threat behavioural pattelns, and three submissive ones. The extent to which aggressive behaviour in this and other plethodontid salamanders determines mating patterns is unclear; territoriality in plethodontids seems to be related primarily to the defense of an adequate food supply. Graded threat signals were describedfor Plethodon cinereus
by Jaeger and Schwartz (1991), and Wise (1991) showed that relative body-size is a major determinant of the outcome of contests in this species. Losers of fights in P. c'inerew often lose their tails by autotomy; as the tail is an energy store, this may represent a substantial cost
of fighting. There is some evidence that the mating patterns of the larger European newts resemble leks, and that males use visual displays to defend ephemeral mating territories. This has been suggested for Triturus cristøtus (Hedlund 1990) and T. uittatus (Raxworthy l98g). Zuiderwijk and Sparreboom (1986) reported that in aggressive interactions among male T. cristatus and T. rna.rmoratu the initial resident of a temporarily occupied (one evening or less) mating territory usually wins over intruders. No systematic studies of aggressive behaviour in Triturus have yet been made, however, so these conclusions are somewhat speculative.
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In aggressive interactions, plethodontids use odours secreted by skin glands to communicate the relative size and dominance-status of contestants (Jaeger and Forester 1993). In Plethodon c'inereus there is also an unusual form of communication involving faecal pellets (Jaeger et ø1. 1986). Faeces are used as territorial markers and olfactory cues contained in them signal residence of a territory; intruders encountering them avoid and display submissively towards burrows marked by conspecific males. Faecal pellets also are used as territorial markers in P. dunni (Ovaska and Davis 1992). Female P. cinereus inspect male faecal pellets closely and may use them to assess the quality of males' territories (Jaeger and Wise 1991). Males may use them to assess the competitive ability of rival males (Jaeger and Forester 1993). On the basis of field and laboratory studies, Mathis (1991a, 199lb) suggested that, in addition to insuring a secure food supply for residents, territories in this species also may provide, for both sexes, an area in which mating will not be interrupted by rivals. Male and female territories overlap and, because they are occupied for long periods, prospective mates have ample opportunity to evaluate one another and their territories.
VI. ALTERNATIVE MATING
STRATEGIES
An important effect of an increased tendency among researchers to study the behaviour has been to show that different individuals may use very different behaviour patterns during competition for a limited resource such as mates. These different patterns are called alternative mating strategies (Rubenstein 1980; Dunbar 1982; Arak 1984). The existence of a mixture of behävioural strategies in a single population raises
of individually marked animals
interesting questions (Partridge and Halliday 1984). Does the mixture represent frxed individual differences or does each individual produce the same mixture? If there are individual differences, do they have a genetic basis? If so, what maintains the polymorphism? If not, what is the causation and ontogeny of the alternative phenotypes? What are the relative adaptive values of the alternative phenotypes? Amphibians have proved to be a rich source of alternative mating strategies, and provide some of the best-studied examples.
In anurans one can flnd alternative non-calling behavioural mating tactics, such
as males
actively moving around the breeding area seeking females, e.g., Bufo bufo (Davies and Halliday 1979), Rana syluaticø (Howard 1980; Woolbright et al. 1990) and Bufo cøl,a,mita (Arak l9BBb; Tejedo 1992a). Occasionally males fight for the posession of females already in amplexus, and engage in protracted struggles, e.g.,Bufo bufo (Davíes and Halliday 1979),8. arnericannu (Howard 1988b), B. gutteralis (Telford and van Sickle l9B9) and Rana syluøticø (Howard and Kluge 1985). Both these tactics are typical of explosive breeders and their occurrence is densitydependent (Woolbright" et al. 1990). In some anurans, especially in those with prolonged breeding seasons, alternative strategies take the form of caller-satellite associations. In many urodeles they are expressed as sexual interference; these very different kinds of behaviour are treated separately.
A. Callers and Satellites in Anurans
In
several frogs and toads, male-male competition takes the form of caller-satellite in which a male calling from a call site or breeding territory is attended closely by one or more non-calling males that seek to intercept and mate with females as they approach the calling male. From studies of caller-satellite associations in anurans and other taxa, a number of different hypotheses for how these associations arise have been proposed. Wells (I97?a) put forward two hypotheses for the occurrence of caller-satellite associãtions: (1) that satellites are waiting for limited call-sites and (2) that satellites are sexual parasites of calling males. Behavioural observations suggest that the first of these hypotheses applies to Hyla uersicolor (Fellers 1979b), and the second to H. chrysoscølis (Roble 1985), H. cinerea (Perrill et al. 1978) and ,F1. ebrøccatø (Miyamoto and Cane 1980). In the light of several recent studies, Wells' two hypotheses can be extended and refined and grouped into three categories, competitive, parasitic and energetic, although it is important to emphasize that these categorizations are essentially heuristic and are not mutually exclusive in natural situations. associations,
AMPHIBIAN BIOLOGY
446
1. Mating competition. Call
for which males to other means, such as fighting. Callers are
sites or breeding territories are a scarce resource
compe"te by^calling, sometimes in additiõn more competitive than satellites.
(a) Callers have superior frghting ability, and this information is coded in their calls. A
correlated asymmetry beiween callers and satellites, e.g., in body-size, is to be expected. (b) Callers have superior ability to attract females, by virtue of specifrc properties of their calls. A correlated asymmelry between callers and satellites, €.g., in body-size, is to be expected.
2. Sexual parasitism. Satellite behaviour is adopted opportunistically as an alternative strategy to calling. There are two ways in which alternative strategies may be maintained in a breeding population (Arak 1984, l9BBb): (a) The relative frequencies of callers and satellites is such that an evolutionarily stable srraregy (ESS) is ãchieved, in which both strategies yield roughly equal mating success; this is called a mixed ESS. (b) Callers and satellites have unequal payoffs but selection favours the two strategies in individuals of differing competitivè ability or in different social or environmental contexts. This is called a pure conditional strategy.
3. Energetic constraints. By virtue of superior energy reserves,
callers are able to call more
effectively than can satellites.
(a) The difference between callers and non-callers reflects some permanent (in the context of a given breeding season) asymmetry, such as body-size or size of fat reserves. (b) The difference between callers and non-callers reflects some temporary asymmetry, such as reduced energetic substrates or a build up of the by-products of anaerobic respiration. Hypothesis l(a) is exemplified by the bullfrog Rana catesbeiøna (Howard 1978a). This species irus, u..rorrrce-based mating pattern, in which males defend ov1p9s!t19n sites that vary in quality in rerms of the their suitability for egg development (Howard 1978b)' Larger, older younger males behave -u1,., défend the better sites that are preferred by females. Smaller, as satellites of larger males but may occasionally occupy a territory vacate_d by a larger male; such occupancy iJ usually only temporary, however, as small males usually are displaced by larger neighbouring males. Hypothesis l(b) is applicable to the natterjackBufo cala:rnita (Arak 1988b, 19-88c), in which females^are attracted by^lõuder calls of large males. Smaller males, incapable of matching the call intensity of larger animals, behave as satellites. lt Bufo cognatus, satellite males associate with larger males t-hat produce longer calls (Krupa 1989)._ In Pseudacris c,rucifer, -there is no relations"hip between male body-sizé and mating success, but calling- males are larger than satellites (Êorester and Lykens 1986). The lower-frequency calls of larger males are more attractive to females (Forêster and Czarnowsky 1985); such males compete for optimal call sites. Smaller males, by adopting a satellite strategy, save energy. Forester and Lykens reported that small males ur. trror. ãleri and agile than are larger ones, qualities that suit the smaller individuals for a satellite role. Hypothesis 2 has been supported by observation and experimentation in the green treet fiit" cinerea. In choruses^óf thit species, some males are consistent callers over several "g others are equally consistent satellites wheteas still others switch between roles "igËtri fräquently, even within a single night. Calling -4.t and satellites e1g91ie1c^e^approximately .qrràl -uiing success (Perrilfet ø1.- 1978), as predìcted by Arak's (1988b) ESS model. In an experimentai study (Perrill et at. 1982), a totãl of 19 tests were conducted in which calling groups; in 11, one of the satellites began to call, in -å1., were removed from caller-satelliteorie.tted toward another caller. Whg_" synthetic calls eight the satellites remained silent and wäre played to calling males, most of them sto-pped calling and became satellites. In none of these experiments diã body-size explain any of the variation in behaviour; larger males were just as likely to be satellites as smaller males.
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In no species studied so far has hypothesis 3, in either of its forms, been found to be a sufficient explanation for caller/satellite patterns, but a number of authors have suggested that energetic constraints may cause males to become satellites (Robertson 1986; Krupa lg8g; Ovaska and Hunte 1992). Lance and Wells (1993) tested the hypothesis that satellite males are physiologically inferior in the spring peeper (Pseudacris cruc'ifer), but found no evidence that physiological constraints are any more severe or limiting for satellites than they are for callers; nor were satellites smaller than callers
A number of studies have provided support for more than one of the above hypotheses. In Hfla minuta, calling males are, on average, larger than satellites (Haddad 1991). In ten tests in which a calling male was removed, his place was taken by a satellite in eight, supporting hypothesis 1; in two, satellites moved to another calling male, supporting hypothesis 2. In EleutherodacQlus johnstonei, the frequency of caller-satellite associations increases with chorus density (Ovaska and Hunte 1992). Calling sites are defended by displays and flghting and are held by larger males, supporting hypothesis 1(a). For small males, satellite behaviour is a conditional strategy (Dunbar 1982). Larger males also may be satellites; for them, satellite behaviour appears to be a response to a lack of call sites at high chorus densities and rnay be a response to energetic constraints (Ovaska and Hunte 1992).
In some anurans, predators pose a potential risk during breeding. In some species, predators are attracted by the advertisement calls of males; the best-known example is Physalaemus.þustulosus, which is preyed upon by bats (Ryan et al. 198I,1982). Reduced risk of predation among non-calling satellites is an additional factor determining the relative payoffs of caller and satellite strategies; when predation on calling males is severe, the relative frequency of satellites would be expected to increase, although satellite behaviour is not favoured by predation in Physal.ctemas prutulostzs (Ryan 1985). From the female's perspective, caller-satellite associations pose a potential threat to her fitness. Because satellites are typically silent, they do not provide females with the information by which they can be recognized as conspecifics. ln Bufo calamita, females vigorously oppose attempts by silent males to amplex them; in many localities, breeding sites are shared with B. bufo, a species in which males typically do not call. Arak (1983b) suggested that females' rejection of silent males helps to prevent heterospecific amplexus. If male advertisement calls contain information by which females can assess the quality of potential mates, then satellites involve the risk that females may mate with low-quality males whose quality they have not had an opportunity to assess. Active avoidance of satellites by females has been reported in Bufo cognøtus (Sullivan 1982b; Krupa 1989).
ln Rana airgøtiþes, females give calls as they approach calling territorial males, who respond by producing aggressive calls. It has been suggested that this may enable a female to differentiate between a territorial male and a satellite (Given 1993b). B. Sexual Interference and Sexual l)efense in Urodeles Many urodeles gather to mate at confined breeding sites, such as ponds, and the resultant high population density provides frequent opportunities for mating competition to occur. In all but the most primitive families of urodeles, sperm transfer is achieved by means of spermatophores, a mechanism that is both intrinsically unreliable and open to a particular form of male-male competition called sexual interference (Arnold 1972, 1976, 1977; }ìalliday 1977, 1990a). The most important opportunity for interference arises in the interval between a male depositing a spermatophore on the substrate and a female picking it up a few seconds later. Successful transfer depends on the female behaving in a very precise and accurate way and she can be disrupted very readily by intrusion by another male. Male urodeles interfere in the courtship of other males in a variety of ways, the most simple being attempting to display to a female that already is being courted. Other forms of sexual interference are summarized in Table 6. In descriptions of sexual interference, the male that already is engaged in sexual behaviour is called the courting male; the male that then intrudes is called the interfering male. The most sophisticated forms of interference are female mimicry and spermatophore covering. In female mimicry the interfering male causes the courting male to deposit a
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AMPHIBIAN BIOLOGY
Table 6. sexual interference and sexual defense
in salamanders and newts
Nature of interference shown by interfering male (lM) towards courting male (CM)
IM mimics female behaviour
Ambystoma
maculatum
to elicit spermatophore
Nature ofdefense shown by courting male (CM)
References
CM covers IM's spermatoPhore with one of his own
Arnold 1976
CM covers IM's spermatoPhore with one of his own. Increased
McWilliams 1992
deposition by CM, then deposits his spermatophore on top of that of CM Amblstoma texanum
IM deposits his spermatoPhore on top of that of CM
Ambystoma tigrinum
spermatophore production
IM mimics female behaviour
CM carries female away from
IM
Arnold 1976
to elicit spermatophore
deposition by CM, then
Cynops ensicaud,a
deposits his spermatoPhore on top of that of CM IM pushes female away from rival male IM mimics female behaviour to elicit spermatoPhore deposition by CM
CM forcibly removes female from the vicinity of rivals
Desmognathus ochroþhaeus
Eurycea cirrigera
IM mimics female behaviour
NotophthaLmu,s û.ridescens
to elicit spermatophore deposition by CM and leads female away IM mimics female behaviour to elicit spermatophore deposition by CM and leads female away IM mimics female behaviour to elicit spermatoPhore
Plethod.on
jorclani
Sparreboom 1994
Houck 1988 Thomas 1989
CM prevents interference by clasping female in amPlexus
Verrell 1982, 1983a
CM chases potential IM awaY from female
Arnold 1976
CM carries female away from potential rivals
Arnold 1977;
deposition by CM, then deposits his spermatophore on top of that of CM Taricha torosa
IM nudges female to one side just before spermatoPhore transfer
Triturus
boscai
IM attempts to court female and pushes against tail
of
CM pushes IM away, avoids spermatophore dePosition
Halliday and Hosie, in prep. Faria, in press
CM Triturus cruta'ttts andmarmoratus
Triturus italicus
Triturus tulgaris
IM mimics female behaviour to elicit spermatoPhore deposition by CM and leads female away IM pushes CM out of the way during display and disPlaYs to the female himself IM mimics female behaviour to elicit spermatophore deposition by CM and leads female away
Males defend display sites, chase rivals away
Zuiderwijk and Sparreboom l986
CM chases and pushes IM awaY
Giacoma and Crusco l9B7
CM increases his display rate'
Verrell 1984
CM attempts to lead female away
from IM by performing
retreat display
spermarophore by mimicking female behaviour, usually by a_ nudge w^ith his snout against the 'male's t;il. This sp"ermatophore is not transferred to the female for one of three c'ourting reason; depending on the ipecies: ihe interfering male pushes the female out of the way, or he leads hei away ão initiate spermatophore transfur himself, or he deposits a spermatophore of his own on top of it. In sþermato¡hore covering, only the sperm of the second male is accessible to the female's cloaca (Arnold 1976). In many species in which interference occurs, male behavioural patterns can be identified that function .ittr.r in countering the adverse effects of sexual interference' or in preventing it happening ar all; rhese are calleã sexual defense (Arnold 1972,1976). Like sexual interference, sexual defense occurs in a diversity of forms (Table 6). They include simply pushing the rival
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away from the female, increasing the rate of display directed at the female, and retaliatory covering. The latter can lead to a situation in which several spermatophores, S alternately by two males, are stacked on top of one another Because of the complexity of the behaviour involved, sexual interference and defense mostly have been described in the laboratory, making it difficult to assess the significance of such behaviour in the field. An exception is a field study by Faria (in press) of sexual interference in Triturus boscøi. Such field data as are available suggest that, in nature, sexually active males often greatly outnumber receptive females and sexual interference is very common; in T. boscai, sexual interference occurs in 52Vo of courtships, Sexual interference leads to low rates of successful spermatophore transfer, as reported in field studies of Triturus uulgaris (Verrell
and McCabe 1988), T. italicus (Giacoma and Crusco 1987) and Notoþhthalrnus
airid,escens
(Massey 19BB). Sexual interference has been described so far in three urodele families, the plethodontids, the ambystomatids and the salamandrids; it is not known whether it occurs in other families. The taxonomic distribution of interference suggests that it is an extremely ancient form of behaviour, and that it pre-dates the evolution of many of the diverse forms of courtship behaviour observed among living urodeles (Halliday 1990a). Thus, many aspects of courtship behaviour, such as elaborate displays and leading the female prior to spermatophore deposition, may be forms of sexual defense, as well as serving other courtship functions, such as stimulation of the female and insuring spermatophore transfer. For example, the "retreat display" phase of courtship in Triturus uulgaris was interpreted by Halliday (1974) as a mechanism by which the male 'tests' the responsiveness of the female; later studies by Verrell (1984) suggested that it also may serve to lead the female away from a potentially interfering male. Sexual interference entails a number of costs for courting males. Interference generally increases the duration of courtship, and sexual defense involves an increase in expenditure of energy. Such costs are probably trivial, but spermatophores that are not picked up by the female, or that are covered by a rival's spermatophores, represent a cost in terms of wasted reproductive effort. It is not known whether sperm per se are costly for males to produce, but there is good evidence that costs involved in the production of spermatophores impose quite severe physiological constraints (Halliday l9B7). In Triturus uulgaris, as in many temperate ectotherms, males have a dissociated reproductive cycle (sensu Crews l9B7); as a result males start the breeding season with a finite supply of sperm which they cannot augment during the season (Verrell et al. 1986). During the coursè of the season, the num6er of spermatophores that a male produces during a mating encounter declines steadily (Halliday 1976), and, following an encounter, males require between one and two days to recover full spermatophore production capacity (Verrell 1987b). In some species, females become less responsive sexually when interference occurs (Verrell 1984; Sparreboom 1994). This represents another cost of sexual interference. A consequence of this effect is that interference not only reduces the mating success of the courting male, but also yields a very low pay-off to an interfering male, because females rarely pick up their spermatophores (Verrell 1984).
Mechanisms of sexual defense can be divided into two categories, pre-emptive and retaliatory. Pre-emptive mechanisms include carrying, pushing or leading a female away from rivals prior to spermatophore deposition. In the great majority of urodeles, there is some form of amplexus prior to spermatophore transfer; as discussed in Section II, amplexus in Notoþhthalmru and Taricha can be regarded as a form of mate-guarding that reduces the risk of interference. Halliday (1990a) suggested that the enormous diversity of forms of amplexus observed among urodeles is the result of a number of independent evolutionary evénts in which taxa have evolved means of female-capture in response to a number of selective pressures, one of which is the risk of sexual interference. A number of urodeles are territorial, notably terrestrially breeding plethodontids (see Chapter 6 of this volume); effective territoriality must reduce the possibility that intruders will interfere with a male's courtship attempts. It has been suggested that males of some of the aquatic European newts (Triturzr) defend ephemeral territories during the breeding period and that these reduce the incidence of interference (Zuiderwijk and Sparreboom 1986; Raxworthy 1989; Hedlund 1990).
AMPHIBIAN BIOLOGY
450
Arnold (1977) drew attention to the marked variation that exists among urodeles in the
number of spermatophores that males produce during courtship encounters (also see Halliday1990a). At one extrème, ambystomatids are capable of producing very large numbers of spermatophores in a single night; at the other, plethodontids produce only one_every f9w dãys. Salamandrids, suchãs the European newts, fall between these two extremes. This variation is related to the length of the breeding season. Ambystomatids are explosive breeders, their mating activity beir¡g limited to a few days, and so their spermatophore production is concentrateã into a short period. Plethodontids, in contrast, have a prolonged season lasting months, over which they have to spread their spermatophore production. The breeding period of most Triturus species is intermediate. Across the three genera.Am.bystomø, Triturtn ànd, Ptethod,on, there is a trend for the amount of male courtship activity invested in each spermatophore to increase, with a parallel increase in the rate at which spermatophores are successfully transferred to females. The longer courtship lasts, however, the more opportunities there are for rivals to interfere. The limited data available suggest that it is in species that have very lengthy courtship, llke Ptethodon jordani and Desm.ognathus ochrophaeus (Houck 1980), that sexual defense is pre-èmptive, males seeking to repel rivals before courtship begins. It is in the more explosive breedeis, like Ambystomø møculatum, that sexual defense generally takes the form of retaliation. The most detailed and complete study of alternative mating strategies in urodeles is that of Notophthalmus airidescens by Vèrrell (1982, 1983a) (see also Halliday 19-90a). Males seek to obtain matings in one of four ways, depending both on the receptivity of the female and on whether rival males are present (Fig. 2): 1. "Hula" display: a brief display preceding spermatophore transfer, performed only if the female is receptive and if no rival is present.
2. Amplexus: a lengthy activity, performed if the female is unreceptive and/or if a rival is pr.retrt. Amplexus serves both to stimulate the female and to guard her against rivals. 3. Sexual interference: adopted if the female is already engaged in courtship with another male. There are two forms of interference:
(a) If the pair are engaged in spermatophore transfer, the interfering male shows female mimicry and attempts to inseminate the female himself.
(b) If the pair are in amplexus, the interfering male attempts to displace the courting
male
from the female's back, but is seldom successful. These alternative strategies, and those shown by Triturus species, can be categorized as conditional strategies (Dunbar I9B2); which strategy a male adopts on a particular occasion depends on the conditions prevailing at the time, not on any inherent property of the male, trlðh ur body-size. This is wèll illustrated by Ambystoma species, in which two males take it in turns to be courter and interferer, covering each other's spermatophores. In the pre-emptive type of sexual defense shown by plethodontids, body-size does ap_pear to be_ an important faitor. [n the laboratory, Houck (1988) reported that larger males of Døsmognøthu ochrophaeus consisrenrly drive smaller males away from females and, in the field, Mathis (1991b) found that males of Plethodon cinereus that are close to females are significantly larger than those found alone. This effect may, however, reflect female choice, as Mathis also found that, in the laboratory, females prefer to associate with larger males.
VII.
SPERM COMPETITION
Sperm competition arises when ejaculates from two or more males compete for access to
a femäle's eggs (Þarker 19?0; Smith 1984). Its occurrence and significance among amphibians was revie*eã-by Halliday and Verrell (1984), who were able to draw only speculative conclusions
from the u..y ipurc. data available at that time. Ten years ago, there was no demonstration of sperm compêtition in any amphibian species, a situation that has slightly improved since' tn this secrioi, rhe dara gathered by Halliday and Verrell are not reviewed again. Rather, some recent studies of sperm competition among amphibians are discussed.
HALLIDAY and TE.IEDO: INTRASEXUAL SELECTION AND ALTERNATIVE MATING
451
Approoch $
ls she qlrcqdy being courted? SEXUAL INTERFERENCE
ls shc recept¡ve?
AMPLEXUS
Are other
dd prescnt?
.HULA'
Fig. 2. Courtship in the red-spotted r'ewt Notoþhthalrnus uiridescens. Top: the male in amplexus with the female , rubbing his cheek glands (inset) against her nostrils. Below: alternative male courtship strategies in relation to the receptivity of the female and the presence or absence of other males (From Halliday 1990a).
452
AMPHIBIAN BIOLOGY
Among anurans, most of which have external fertilization, there is potential for sperm competition, and for more than one male to fertilize a female's eggs, when single males are very close to amplectant pairs. This occurs in several species (e.g., Bufo bufo and Rana temþoraria, Halliday, pers. obs.), but no study has demonstrated multiple paternity of anuran egg masses. The greatest potential for sperm competition arises in those species in which mating pairs spawn in a nest and are closely attended by satellite or peripheral males. Just such a situation has been studied in the African foam-nesting rhacophorid Chiromantis xerømþelinø. Foam nests are constructed over water by amplectant pairs, 90/a of which are attended by one to seven peripheral males (fennions et al. 1992). Those peripheral males that are closest to the pair compete to position their cloacae against the female's cloaca during oviposition; male participation in these groups, as amplectant or peripheral male is not related to male size and individual males may participate in mating, on different occasions, in both amplectant and peripheral roles. To test the hypothesis that peripheral males obtain fertilizations, Jennions and Passmore (1993) performed a "sterile male" experiment, in which the amplectant male was enclosed in a condom-like sheath, and found that the eggs were fertilized. Among males, sperm competition is predicted to select for greater sperm production, and thus large testis size, a relationship that has been found in a number of taxa, e.g., birds (Birkhead and Møller 1992) and primates (Harcourt et al. l98I). Jennions and Passmore (1993) compared the testis size of three foam-nesting rhacophorids, Chiromantis xeramþelina, Rhacoþhorus erboreus, and iR. schlegelli, and found that relative testis mass (correcting for body mass) is 3.8 to 14.6 times greater in these species than in 31 non-foam-nesting species. Among urodeles, the combination of internal fertilization and spermathecae in which sperm are stored (in some species over a very long time) provides abundant potential for sperm competition [o occur (Halliday and Verrell l9B4). The other condition necessary for sperm competition, that females mate with more than one male, has been demonstrated in only a few species, but may be quite widespread. Tilley and Hausman (1976), using genetic techniques, estimated that at least 7% of egg clutches of Desmognathus ochroþhaeus have more than one father; Rafinski (1981) reported high levels of multiple paternity inTriturus o,lþestris. In both Triturus aulgaris and Notoþhthalmus airidescens, Verrell found that already-inseminated females will pick up spermatophores from males (Halliday and Verrell l9B4) and Verrell (1984) showed that, in T. uulgaris, sexual interference can lead to females picking up sperm from both the courting and the interfering male (see Section VI.B). Data gathered by Hosie (1992) suggests that female T. uulgaris typically mate with several males over the course of a season, and, in an experimental study, she showed that, when tested twice over a two-day interval, females are more likely to pick up the spermatophore of a novel male in the second test, rather than that of the male whose sperm they picked up two days previously (Hosie, submitted). Possible functional explanations for this behaviour are (1) that females are guarding against the risk that their first mate is sterile, (2) that females actively seek multiple paternity of their broods, and (3) that females actively promote sperm competition (Halliday and Arnold 1987). Sperm competition has been investigated extensively in Triturus by J. Rafinski and A. Pecio. In a paternity study of different populations of T. alþestris, males were used whose origins could be identified by electrophoretic markers. There was considerable variation, with second-donor males fathering 15-95% of a female's progeny but, overall, a slight secondmale advantage (Rafinski, pers. comm.). Pecio (pers. comm.) investigated paternity by mating females sequentially with males of different species, T. uulgaris and Z. rnontandoni. There was a tendency for the second male to have a mating advantage, although this was tempered by a tendency for conspecific sperm to more effectively fertilize a female's eggs. Overall, these data suggest that there is a last-male advantage in Triturus.
The prevailing view is that sperm competition is a manifestation of male-male competition. However, given that sperm competition can only occur if females provide appropriate conditions, both by mating multiply and by storing sperm, more attention should be paid to possible adaptive consequences for females of sperm competition (Eberhard 1990). Halliday (1983) suggested that females might use multiple mating, combined with sperm competition
HALLIDAYandTEJEDO: INTRASEXUAL SELECTION AND AT.TERNATIVE
MATING
453
in which there is a last-male advantage, to insure that they mate with high quality males. If a female mates with the frrst male she meets, she guarantees that her eggs will be fertilized. Thereafter, she can sample further males and, by mating only with those of higher quality than previous partners, she can maximize the quality of her progeny. This hypothesis has been iested by Gabor and Halliday (submitted) in the smooth newt (Triturus u. aulgøris); in this species, females show a preference for picking up the spermatophores of males with relatively larger crests (Hosie 1992). Females were presented with single males, varying in cresr height, in two tests, separated by a period of 20 days during which females could lay eggs. In the second test, a significant majority of females mated only if the male had a higher ciest height than the male with whom they mated in the first test. This result supports the hypothesis that females may combine multiple mating and sperm competition in an adaptive máting strategy, although multiple mating may serve other, additional functions (Halliday and Arnold 1987). These recent studies provide a tantalizing glimpse of what are probably very complex reproductive strategies among female urodeles, involving multiple mating, mate choice and spèrm competition. Further studies of female mating patterns and of sperm storage and use are urgently need to build up a more complete picture.
VIII. SEXUAL COMPETITION AMONG
FEMALES
A recent increase in interest in the sexual.behaviour of females
has followed repeated a bias towards considering suggestions that the literature on animal mating patterns exhibits The amount of data (e.g., 1993). scant Ahnesjö et al. oniy male behaviour and male interests female sexual competition is that is the case but it also on the subject may reflect such a bias, There are is males. than it among more subtle, is often it does occur, much rareî and, where "sex reversal" role said to show which are of taxa, a variety among a number of species, (Trivers 1972; Williams 1975) a term of dubious heuristic value (Vincent et ø1. 1992). A common feature of such species is that females compete with one another and that males are
the more choosy sex (Petrie 1983). These uncommon patterns of behaviour are associated strongly with male parental care (Clutton-Brock 1991), which is a rare phenomenon among amphibians (Wells 1981).
Many of the dendrobatid frogs care for their young and there is variation among species in whether it is the male, the female, or both that is responsible for that care (Duellman and Trueb 1986; Heselhaus 1992). In Colostethus trinitatis, the male carries the tadpoles from terrestrial oviposition sites to water and the female defends those sites by displays and fighting (Wells 1980a). ln C. inguinøli,s,by contrast, the female carries the tadpoles but does not defend the territory (Wells 1980b). Summers carried out detailed studies of a number of species, seeking to test alternative hypotheses for the function of female competition. ln Dendrobates eltrrahts, females are larger than males, they compete for males and are the more active partner in courtship. Wells (1978b) suggested that this is because the small clutch size and large time investment by males in parental care causes receptive males to be rarer in the population than are receptive females. Summers (1989) compared this "sex role reversal" hypothesis with an alternative one, namely that females compete to monopolize the parental care of particular males. He concluded that a number of features of the behaviour of this species support the latter hypothesis. Among these are that (1) females compete for males, but are more selective than males about mating, (2) females take up position close to particular males and keep other females away from them, and (3) females appear to use courtship to prevent males from mating with other females. Apart from fighting with one another, female D. auratus compete by destroying the eggs of other females when they locate them. Summers ( 1992) also tested the same two hypotheses in a comparative study of Dendrobates in which the male cares for the young, and D. histrionicus, in which the female cares. His observations again support the parental care hypothesis; females of both species are selective when mating and female D. leucomelas associate with and compete for particular males, whereas female D. histrionicøs do not.
leucomelas,
454
AMPHIBIAN BIOLOGY
The theoretical framework for analyses of sex roles, like those of Summers, has been the concept of parental investment (sensu Trivers 1972). Clutton-Brock and Vincent (1991) suggested an alternative approach based on the concept of potential reproductive rate, defined as the maximum number of independent offspring that parents can produce per unit time (see also Clutton-Brock and Parker 1992). Differences in the reproductive rates of the two sexes commonly are caused by physiological constraints on the rate at which gametes can be produced (Halliday 1987), or they may arise from sexual differences in time allocated to searching for mates (Sutherland 1987). The operational sex ratio in any population will be biased toward whichever sex can reproduce faster. The surplus of mates available to the more slowly breeding sex results in competition between individuals of the faster breeding sex for access to mates. Considering species with male parental care, Clutton-Brock and Vincent gathered data from the literature to show that the sex with the faster potential rate of reproduction is usually the sex that competes for mates. The explanations offered by Trivers and Clutton-Brock and Vincent may not be mutually exclusive, because in most cases the sex with the higher parental investment will also be the sex with the slower potential rate of reproduction. Clutton-Brock and Vincent argue, however, that reproductive rates may be much easier to measure than is parental investment, and that more rigorous tests of hypotheses can therefore be made.
In Bush's (1993) study of the Majorcan midwife toad (Aþtes muletensis), a species in which males brood the eggs, two explanations for the evolution of female competition were suggested. The first is based on Summers' studies of dendrobatids and argues that females will compete for males if there is large variation among males in the quality of care that they provide for the eggs. The second argued that females will compete for males when their reproductive rate is higher than that of males; that is, when females can produce new clutches of eggs faster than males can brood and release them. Bush found no support for the first hypothesis; there is, for example, no obvious male correlate, such as body-size, of variation in hatching success. A. muletensis offers an excellent opportunity to test the reproductive rate hypothesis, because both male and female rates vary over the course of the long breeding season, depending on (l) food supply, which affects how fast females can produce a new clutch of eggs, and (2) temperature, which affects how fast males can brood and release eggs (Bush and Halliday, work in progress). Competition among female A. muletensis takes a variety of forms (Bush 1993). A single female may attempt to separate an amplectant pair by grappling with the female, climbing on top of the male, or pushing herself between them; as she does so, she calls continuously. Females also show a form of sexual interference, in which they clasp amplectant males around the waist, thus preventing them from performing a "pedalling" leg movement that is an essential component of successful courtship. In the absence of this behaviour, an amplexed female will remove the amplectant. male. Similar displacement behaviour by females has been described in A. obstetricans by Verrell and Brown (1993).
A possibly unique example of sex role reversal is shown by the Bornean frog Ranø bþthi (Emerson 1992). In this species, only the female calls. This apparently coordinates mating activities with the male, who initiates the construction of a nest in which mating takes place. Among urodeles, parental care is provided only by females (Duellman and Trueb 1986) and has been most intensively studied in plethodontids (Jaeger and Forester 1993). The only reported observation of female competition is that by Waights (submitted) of sexual interference between female smooth newts (Triturus a. uulgaris), in which, during courtship, an interfering female picks up the spermatophore just before the courting female, who has just solicited it from the male, is able to do so. This behaviour apparently occurs only at the very beginning of the breeding season and is explicable in terms of the relative reproductive rates of males and females. Early in the season, females are highly receptive to males and mate frequently (Hosie 1992). The one- to two-day refractory period in male spermatophore production (Verrell 1987b) appears to mean that receptive females outnumber sexually competent males at this stage of the season, so that females have to compete for the available sperm. An interesting frnding in Waights'study is that the rate at which females pick up spermatophores
É
HALLIDAY
ANd
TEJEDO: INTRASEXUAL SELECTION AND ALTERNATIVE
MATING
455
during female-female interference is relatively high (78%), compared with that in courtship involvìng pairs (43%) (Halliday 1990a), and that in courtships in which male interference occurs (22%) (Verrell 1984). Female competition
for mates also may be involved in the territorial behaviour observed
among female Plethodon cinereus, as well as among males (Mathis 1991b). Males and females have õverlapping territories and, while the primary function of territoriality in this and other plethodontidi is ass,rrance of an adequate food supply (see Chapter 6 of this. volume) it may älso insure, for both sexes, exclusive access to mates and reduced risk of sexual interference.
IX.
CONCLUSIONS
As suggested in the introduction to this chapter, amphibians pose something of a puzzle in the context of sexual selection theory. Despite intense competition among males being a common phenomenon, males are rarely larger than females, and are often smaller, and in only a few species do they possess weapons. This is all the more remarkable in view of the fact that, with a few exceptions, the male's contribution to reproduction consists only of the production of sperm. As discussed in Section III, two major factors contribute to selection on Èody-size in amphibians. First, large body-size confers a reproductive advantage on males only in a few species, whereas selection on females, because of the positive relationship between body-size ând fecundity, consistently favours larger body-size. Second, in many species in which a positive advantage for males being larger has been demonstrated, it is not consistent between years or between populations. Many of the studies reviewed here suggest that variation in male reproductive success is attributable, not to body-size, but to factors such as stamina and the adoption of alternative mating strategies (Section VI).
The rarity of weapons among amphibians can be attributed to two factors. First, amphibians have not evolved weapons functioning in other contexts, such as feeding and defense, so that there are no appropriate characters on which selection arising through mating competition could act. Second, amphibians have evolved effective and less-costly means of resolving conrests, such as through calling and threat displays (Section V). The evolution of low-cost forms of aggression is, arguably, likely to be favoured in a group that typically is long-lived and that shows indeterminate growth. Younger, smaller animals that engage in costly fights are likely to pay a heavy cost in terms of reduced survival or of slower growth. The classiflcation of sexual selection mechanisms proposed by Andersson ( 1994) (Table I) provides a convenient way to summarize the role of intrasexual selection in amphibians. Scramble competition is quite common, especially among those species, such as many bufonids, for which ecological and climatic factors favour explosive breeding. There is little evidence among amphibians that scramble competition has favoured enhanced sensory or Iocomotor capabilities among males; rather, the ability to sustain vigorous activity over time seems to be the most important determinant of reproductive success. Examples of endurance rivalry are quite numerous among amphibians, both in terms of being able to sustain sexual activity over the course of a season (e.g., calling frogs), and in being able to engage in lengthy fights (e.g., attempts to displace amplectant males in toads and newts). Direct contests between males are quite common but, as discussed above, body-size and weapons have not been as strongly selected as low-cost forms of fighting (Section V) and alternative tactics (Section VI). The potential for sperm competition has favoured mate-guarding in many amphibians but there is a need for more research on this phenomenon, especially among urodeles (Section VII). The dynamics of mating competition in breeding populations are influenced very strongly by the OSR. The more OSR is biased towards an excess of males, the more intense will be male-male competition. In the majority of amphibian breeding assemblages studied to date, OSR is male-biased, though this is by no means always the case. For example, Denton and Beebee (1993a) have reported a population of natterjacks (Bufo cal.a,mita) that shows a pronounced female-bias, probably because males suffer higher predation by snakes. In species
fÌ1--=
AMPHIBIAN BIOLOGY
456
with extended breeding seasons, the OSR may vary considerably over the course of a season of time at breeding sites.
because individuals of both sexes typically spend varying amounts Biased sex ratios may arise in a number of ways:
l. There may be a bias in the actual sex ratio,
i.e., more individuals of one sex are produced during reproduction. Biased actual sex ratios have been reported in a number of taxa, but no amphibian examples are known.
2. One
sex, usually females, may breed at an older age than the other. Unless age-related mortality is different in the two sexes, the later-breeding sex will be outnumbered in
breeding populations.
3. One sex, usually females, may skip breeding seasons more often than the other. 4. One sex, usually females, may spend less time at the breeding site than the other. 5. One sex, usually males, may be capable of mating more often in the course of a mating season than the other.
6. One sex, usually females, may have a slower reproductive rate than the other. 7. OSR may be influenced by the degree of breeding synchrony shown by each
sex. For example, in the smooth newt (Triturus aulgaris), females ovulate within one or two days of one another, leading to a short-term reduction in the value of the OSR (Verrell and Halliday l9B5).
There have been no studies of how variations in OSR might affect mating dynamics in amphibian breeding populations; in particular, the prediction that the degree of male-bias will influence the intensity of selection on males has not been tested. It should be noted that all of the factors listed above that influence the OSR are related to life history phenomena. This reinforces the point, made by Halliday (1992), that a full understanding of the selective pressures that affect males and females in the context of mating, cannot be gained by analysis at the behavioural level only, but must take into account many aspects of life history.
X. ACKNOWLEDGEMENTS We thank Sarah Bush, Mandy Dyson, Michael Jennions and Verina Waights for reading all or part of the manuscript, and Thomas Friedl, Jan Rafinski and Verina Waights for allowin[ us to quote their unpublished work.
XI. Acker, P. M., Kruse, K. C. and Krehbiel,
E.8.,
REFERENCES
1986.
Aging Bufo americanus by skeletochronology.
HerþetoL
2ù
..¡1.
570-574.
Ahnesjö, I., Vincent, 4., Alatalo, R., Halliday, T. and Sutherland, W. J., 1993. The role of females in influencing mating patterns. Behau. Ecol.4: I 87-l 89. Aleksandrosvskaya, T. D. and Kotova, E. L., 1986. Données préliminaires sur les caractéristiques d'age des grenouilles lacustres (Rana ridibunda Pallas) de 3 régions d'Arménie. Proc. Zool. Inst. Acad. S¿i. USSA 157: 177-18O.
Alford, R. 4., 1989. Competition between larval Rana þaLustris and Bufo americanus is not affected by
variation in reproductive phenology. Copeia 19892 993-l 000.
Allan, D. M., 1973. Some relationships of vocalization
to behavior in the Pacifrc treefrog, Hlla
Herþetologica 29: 366-37
Andersson,
regilLa.
l.
M., 1994. "Sexual Selection".
University Press, Princeton, New Jersey.
Andrén, C. M. Mardén, M. and Nilson, G.,
1989.
Tolerance to low pH in a population of moor frogs, Rana at-ualis, from an acid and a neutral environment: a possible case of rapid evolutionary response to acidification. Oihos 56t 215-223.
Arak, P. 4., 1983a. Sexual selection by
male-male
competition in natterjack toad choruses. Nature 306-
26r-262.
Arak, P. 4., 1983b. Male-male competition and mare choice in anuran amphibians. Pp. l8t-210 in"Mate Choice", ed by P. P. G. Bateson. Cambridge University Press, Cambridge.
Arak, 4., 1984. Sneaky breeders. Pp. 154-194 in "Producers and Scroungers", ed by C. J. Barnard. Croom Helm, Beckenham.
Arak, P. .4., 1988a. Sexual dimorphism in body size:
a
model and a test. Euolution 422 820-825. Arak, P. 4., 1988b. Callers and satellites in the natterjack
Princeton
toad: evolutionarily stable decision rules.
Behaa. 362
416432.
Anim.
HALLIDAY
ANd
TEJEDO: INTRASEXUAI, SELECTION AND AI.TERNATIVE
Arak, p. 4., 19BBc. Female mate selection in the ¡ucl toáa: active choice or passive alraction? "EcoL
sociobiol: 22:
natterBehaa.
317-327.
S. J., 1972. The evolution of courtship behavtor in salamanders, Ph.D. dissertation, Univ. of Michigan, Ann Arbor.
Arnold,
Arnold, J., 1976. Sexual behavior, sexual interference and sexual defense in the salamanders Amblstoma maculatum, Ambystoma tigrinum and Plethodon jordani. S.
Z. Tierþs1chol. 422 247-300.
salamanders. Pp. l4l-l83 in "'fhe Reproductive Biology of Amphibians", ecl by D. HTaylor and S. I. Guttman. Plenum Press, New York.
Old World
Arnold, S. J., 1983. Sexual selection: the interface of theory and empiricism. Pp. 67-107 in "Mare Choice", ed by P. P. G. Bateson. Cambridge University Press, Cambridge.
Arnold, S. J. and Duvall, D., 1994. Animal mating systems: a synthesis based on selection theoty. Amer.
Natur. 143: 317-348.
Arnold, S. .f. and Houck, L. D., 1982. Courtship pheromones: evolution by natural and sexual
ielection. Pp. 173-2ll in "Biochemical Aspects of Evolutionary Biology", ed by M. H. Nitecki. University of Chicago Press.
Augert, D. andJoly, P., 1993. Plasti':ity of age at ma-turity
benveen trvo neighbouring populations of the common lrog (Rana temþoratia L.). Can..l. Zool. 7lt 26-33.
Axtell, R. W., 1958. Female reaction to the male call in trvo anurans (Amphibia). SW Natur. 3t 70-76 Backwell, P. R. Y. and Passmore, N. I., 1990. Aggressive interactions and intermale spacing in choruses of the
leaf-folding frog, Aft'ixalus delicatus. S A. J. Zool.25:
r33-t37.
I., 1991. Sonic complexity and mate localization in the leaf-foldìng frog', Afrixalus delicatus. Hërþetologica 4lz 226-229.
Backwell, P. R. Y. and Passmore, N.
Balinsky, B. L and Balinsky,J. 8., l954 On the breeding
habits of the South African bullfi-og, adspersus. South
Baker,
AfricanJ.
PlxiceþhaLus
51: 55-58.
J. M. R., 1992. Egg production in the
Banks, B. and Beebee, T.J. C., 1986. A comparison of the fecundities of two species of øad (Bufo bufo and Bufo caLamita) from different habitat types in Britain. J . ZooL, ktnd. 208: 325-337 .
Banks, B. and Beebee, T.J. C., 1988. Reproductive success of natterjack toaðs Bufo calamìta in two contrasting habitats.;ir. Anim. Ecol. 572 475492.
Barandun, J., 1990. Reproduction of yellow-bellied toads Bombina uariegata in a man-made habitat. AnphibiaReþtilia llz 277-284.
Bastien, H. and Leclair, R., 1992. Aging wood frogs (Rana sllaatica) by skeletochronology.../. Herpetol. 262 ooo qqK
f'. J. C., 1980. Belly colour and foot-webbing in
newts of the genus Trilznrs. Brit. J. Herþetol.6: 59-61.
Bernardo,
B., 1993. Determinants of maturation in
animals. Trends Ecol. EwL Sz 166-173.
L-
8., 1994. Experimental analysis of allocation in two divergent, natural salamander populations.
Bernardo,
Amer' Natur' 143: 14-38'
Berven, K. 4., 1981. Mate choice in the woodfroS, Rana syluatica. Eaolution 3* 707-722.
Berven, K. 4., 1982a. The genetic basis of altitudinal variation in the wood lrog Rana sylaatica. l. An experimental analysis of life history traits. Euolulion 36: 962=983.
4., 1982b. The genetic basis of altitudinal variation in the woodfrog Rana slhatica. II. An experimental analysis of larval development Oerologia
52: 360-369.
Berven, K. 4., 1987. The heritable basis of variation in larval developmental patterns within populations of the rvood frog (Rana slluatica). Euolution 4l: l 088-1 097.
Berven, K. ,A.., 1988. Factors affecting variation in repro-
ductive traits rvithin a population
of wood
frogs
(Rana slluatica). Coþeia 1988¡ 605-615.
Berven, K. .A., 1990. Factors affecting population fluctuations in larval and adult stages of the lvood ftog (Rana slhtatica). Ecology 7lz 1599-1608. Berven, K. A. and Chadra, B. G., 1988. The relationship among egg size, density and food level on larval
development
in the wood frog (Rana slluatica).
Oecologia (BerL) 752
67-72'
Birkhead, T. R. and Møller, A. P., 1992. "Spenn Competition in Birds: Evolutionary Causes and Consequences". Academic Press, London.
Blair, A. P., 1943. Population structure in toads.
,42¿¿¡.
Natur. 772 563-568.
Blair, A. P., 1946. ^fhe effects of various hormones on primary and secondary sex characters in juvenile Bufo
fouleri. J. Exþ. Zool. 103: 365-400.
Bogert, C. M., 1960. The influence of sound on the behavior of amphibians and leptiles' Pp' 137*320 in "Animal Sounds and Communication", ed by W. E. Lanyon and W. N. Tavolga. Amer. Inst. lliol. Sci. Publ. 7, Washington D.(ì. Bourne, G. R., 1992. Lekking behavior in the neotropical frog Olo\gon rubra. Belt'au. Ecol. SociobioL. 3l: I
smoôth
newr (Tt'iturus aulgaris). Herþetol../. 2: 90-93.
Beebee,
457
Berven, K.
Arnold, S. J., 1977. The evolution of courtship behavior in New World salamanders with some comments on
Sc¿.
MATING
73-l 80.
Bourne, G. R., 1993. Proximate costs and benefits of mate acquisition at leks of the frog Olol¡gon rubra. Anim. Ilehau. 45:
l05l-1059.
Bradbury, J. W. and Davies, N. 8., 1987. Relatives roles' of intra- and inter-sexual selection' Pp. 143-163 ln "sexual Selection: Testing the Altelnatives", ed byJ. W. Bradbury and M. B. Anclersson. John Wiley and Sons, Chichester.
Bragg, A. N., 1940. Observatiolrs on the ecology and natural history of Anura: 1. Habits, habitat, and breeding of Bufo clgnatus Say. Amer. Natur. 74:
424438. Breden, F., l9BB. Natural history and ecology of Fowler's toarJ, B ufo zu o o tlh ouse i fo toleri (Am phibia : B ufonidae), in the Indiana Dunes national lakeshore. Field. Zool.
49¡ l-16. Brenowitz, E. A. and Rose, G. J., 1994. Behavioural plasticity mediates aggression in choruses of the Pacific treefrog. Anim. Behau. 47: 633-641.
458
AMPHIBIAN BIOLOGY
Brenowitz, F.,A,., Wilczynski, W. and Zakon,H. H., lgB4. Acoust ic communication in spring peepers. Environ_ mental and behavioral aspécts. j ,o*p. ph.ysiot. A 155: 585-592.
J. L. and Storm, R. M., 1970. Growth and population structure of the Cascade lrog, Rana casrudae Slater. Herþetologica 26: 2BZ_300. "
Briggs,
Brown, L. E. and pierce, J. R., 1962. Male_male inter_ actions and chorusing intensities of the great plains toad, Bulo clgnatus. Coþeia
lg67:
I4g-1b"4.
Crump, M. L., 1984. Intraclutch egg size variability in Hyla crucfer (Anura: Hylidae) . Cóþeia t9B4:302_á08.
Crump, M. I ., lg88, Aggression in harlequin frogs: male-male competirion and a possible conflict of interest between the sexes. -Anim. Behaa. 36: 1064_t077.
Crump, M. L. and Townsend, D. S., lgg0. Random maring by size in_ a neotropical treefrog, Hyla þseudoþuma. Herþetologtra
46: 3g3_3g6.
Brown, W. C. and Alcalá, A. C., lg?0. population ecology erythraea in southern Negros, gl ..1h.. îrog -Rana tg70z 6t t-622. Philippines. Coþeia
Cummins, C. P., 1986. Temporal and spatial variarion in egg size and fecundity in Ranø temporaria. J. Anim. Eeol.5* 303-316.
Bruce, R. C. and Hairston, N. G., lgg0. Life_history correlates of body-size differences between two
Darwin, C., l87l. "The Descent of Man, and Selection in Relation to Sex',. John Murray, London. 6gg pp. Davies, N. B. and Halliday, T. R., 1977. Optimal mate_ selecrion in rhe toad Brfo bqfo. Nature i6g; b6_5g.
populations of the salamander
monticola.
Desmosnathlß
J. Herþetol. 24: 124-134.
Bull, J. J. and Shine, R., lg7g. Ireroparous animals that skip opportunities for reproduciion. Amer. Nat. ll4z 296-303. Bush, S. L., 1993. Courtship and male parental care in the Mallorcan midwife-toad, Aþtes^mutetensis. phD. Thesis, University of East Angliâ. Caetano, M. H. and Casraner,
I., lggg. Variabilirv and microevolutionary patterns in Triturus matm'oratus from.Portugal: age. size, longevity and individual
growrh. Amþhibia Reþtilia 14. ft7_i29. Capranica, R. R., 1977. Auditory processing of vocal signals in anurans. pp. 327-ZBb j¿ ,,TËe Reoro_ ductive-Biology of Amþhibians", ed by D. H. Taylor and S. I. Guttman. plenum press, New york. Channing, 4., du Preez, L. and passmore, N., 19g4. Status, vocalization and breeding biology of two species of African bullfrogs (Ranidãe : pyxicephalus).
Davies, N. B. and Halliday, T. R., lg7B. Deep croaks and ¡t¡titS assessmenr in toads Bufo bufo. Nature 274t 683_685.
N. B. and Halliday, T. R., 1g79. Comperirive mate sea_rching in male common toads, Bifo bufo. Anìm. Behau. 27t I2bZ:-1267
Davies,
Davis, M. S., 1987. Acoustically mediated neighbor recognition in the North American bullfros,'Rana catcsbciana. Bchau. Ecol. Sociobiol.
2l:
l35_19õ.
Davis, W. C. and Twirry, V. C., 1964. Courtship behavior
and reproductive isolation in the speciesïf Taricha (Amphibia, Caudata). Copeia 1964i601_609.
Denton, J. S. and Beebee. T..1. C., lgg3a. Reproducrive strategies in a female-biased population of natterjack toads, Bufo calamita. Anim. Bihau.46:
I169_ll7b.
Cherry, M. L, 1992. Sexual selecrion in the leopard toacl,
Denton,J. S. and Beebee, T.J.C., lgg3b. Density_related fearures o[ natrerjack toad ¡Bufo calamita) pooula_ tions in Brirain.r/. Zool., Lond. ZÞS: IOS_l lSl
Cherry, M. I., 1993. Sexual selection in the raucous toad, Bu,fo rangeri. Anim. Behaa. 452 Zbg-373.
Deviche, P. and Moore, F. L., l9g6. prolactin regulation of morphological characteristics in the male"rough_ skinned newt (Taricha granulosa). Abstract, Western
J.
Zool..
Lond.234: 14l-148.
Bu[o þardalis. Bchauiour
120: 164-176.
Cherry, M. and Francillon-Vieillor, H., 1992. Body size, age.lld reproduction_in the leopard road, nufo þardalzs. J. Zool. Lond. 22Bz 4l-50. Clutton-Brock, T. H., lggl. ..lfhe Evolution parental
of
Care". Princeton Univ. press, princeton, NewJersey.
Clutton-Brock, T. H. and parker, G. A., lgg2. potential
reproductive rates and the operation
selection. Quart. Reu. Biot. 67:
4274b6.
of
sexual
Clutton-Brock, T. H. and Vincenr, A. C.J., lg9l. Sexual selection ,and the potential reprod"uctive rates of males and females. Nature 35lt 5g_60. Cogalniceanu; D., lgg4. The relative importance of vision and olfaction in mate recognition in male newts (genus Triturus). Herþetotogicã 50 244_249. Cooke, A. S.,
l98l . Amphibian growth
6:179-180.
rates. Brit. J. Herp.
Englewood Cliffs, New Jersey.
Crump, M. L., 1572. Terriroriality and marins behavior De ndro batcs,
Herþetologira
granu
t ile
rus ( An
28: 195-198.
u
ra
: Dendiobatidae).
Conference on Comparative Endocrinology.
Univ. California, Davis.
Diaz-Paniagua, C., lg8g. Oviposition behavior in Triturus memoratus Nrygmaeus. J. Herpetol. 23: lb9_163.
Duellman, W. E. and Trueb,
L., lgg6. ,,Bioloev of
Amphibians". Maccraw Hill, New york. Dunbar, R. I. M., 1982. Intraspecific variations in mating in ..perspectives in Ethology, :lr?r.-ql. Pp_ 38b-431 p. G. Bateson and p. H. Klopféi. 5", by-p Y."1. 19 Plenum, New York.
Dyson, M.
L.,
1989. Aspects
of
social behaviour
in
a
popu.lation ofpainted reed frogs. phD Thesis, Univ. of Wirwarersrand, Johannesbuig.
:3ged
Dyson, M. L. and Passmore, N. I., lggga. The combined effecr o[ intensity and the remporal relationship ol strmulr_ on the phonotactic responses ol female painted^
Crews, D., 1987. Diversity and evolution of behavioral controlling mechanisms. pp. gg_t lg in .,psycho_ biology of Reproductive Behavior: an Evolutiánary Perspective", by D. Crews. prenrice HalÍ, _ 9d
in
l¡gro"rl
reed frogs
(Hyþerotius rnarmoratus). Anim,
Behaa. 362 I 555- I 556.
Dyson, M. L. and passmore, N.
I., lg8gb.
Two_choice
phonotaxis in Hyþerolius marmora¿us (Anura:
Hyperolidae): the effect of temporal variaijon on
presented stimuli. Anim. Behart.36: 64g_652.
L. and Passmore, N. L, lgg2. Inter-male spacing, and..aggression in African painted reed ftogs, Hyþerolùn mannlratus. Ethology Si: 227_2a?.
Dyson, M.
HALLIDAY and TEJEDO: INTRASEXUAL SELECTION AND ALTERNATIVE Dyson, M. L., Passmore, N. L, Bishop, P. J. and Henzi, S. P., 1992. Male behavior and correlates of mating success in a natural population of African painted reed frogs (Hyperolius marmoratus). Herþetologicø 48t 236-246. Eberhard, W. G., 1990. Inadvertent macltisrno? Trends EcoI. Eaol.
6:263.
Elmberg, J., 1987. Random mating in a boreal population of European common frogs Rana temþoraria. Holnrctic Eeol. l0z 193-195. Elmberg, J., 1990. Long-term survival, length of breeding season, and operational sex ratio in a boreal population of common frogs, Rana temþoraria. Can. J. Zool. 68t l2l-127.
MATING
459
Fellers, G. M., 1979a. Mate selection in the gray treefrog,
Hyln uersicolor. Copeia 19792 286-290.
M., 1979b. Aggression, territoriality, and mating behaviour in North American treefrogs.
Fellers, G.
Anitn. Behat. 272 L07-119.
Forester, D. C., Cover, J. and Wisnieski, 4., 1993. The influence of time of residency on the tenacity of the territorial defense bv the dart-poison frog Dend,robates þwniko. II erþetologica 49: 9tl-99. Forester, D. C. and Czarnowsky, R., 1985. Sexual selection
in the spring peeper, Hyla cruciftr (Amphibia, Anura): role of the advertisement call. Behaaiour 922 I 13-128.
Elmberg,
J., 1991. Ovarian cyclicity and fecundity in boreal common frogs Rana temþoraria L. along a climatic gradient. Funct. Ecol. 5: 340-350.
Forester, D. C. and Harrison, W. K., 1987. The signifrcance of antiphonal vocalization by the spring peeper, Pseudacris crucifer (Amphibia, Anura). Behauiour 103: 1-15.
Emerson, S. B., 1991. A biomechanical perspective on the use of forelimb length as a measure of sexual selection in frogs..¡L eaol. Biol. 4z 671478.
Forester, D. C. and Lykens, D. V., 1986. Signifrcance of satellite males in a population of spring peepers (H1la crucifer). Coþeia 1986t 719-724.
Emerson, S. 8., 1992. Courtship and nest-building behavior of A Bornean frog, Rana blythi, Coþeia
Francillon-Vieillot, H., Arntzen, J. W. and Géraudie, J.,
Il23-rr27.
19922
Emerson, S.
8.,
1994. Testing pattern predictions of
sexual selection:
a frog example. Am. Nat. 1432
848-869. Emerson, S. B. and Inger, R. F., 1992. The comparative ethology of voiced and voiceless Bornean frogs.;ir. Herþetol.26: 482490.
1990. Age, growth and longevity of sympatric Triturus cristahs, T. marmoratus and their hybrids (Amphibia,
Urodela): a skeletochronological comparison. 'Herþetol.24t 13-22.
3L
Francillon-Vieillot, H., Barbault, R., Castanet, J. and de Ricqlés, 4., 1984. Etude complémentaire sur la biologie de I'amphibien déserticole Bufo þentoni: données de squelettochronologie et d'écodémographie. Rea. Ecol. (Terre Vie) 892 209-224.
Emerson, S. B., Rowsemitt, C. N. and Hess, D. L., 1993. Androgen levels in a Bornean voiceless frog, Rana bþthi. Can. J. Zool. 7ll. 196-203.
Friedl, T. W. P. and Klump, G. M., in press. Some aspects of population biology in the European rreefrog, Hyla arborea, as revealed by skeletochronology.
Emerson, S. B. and Voris, H., 1992. Competing explanations for sexual dimorphism in a voiceless Bornean frog. Functional Ecol. 6z 654-660.
Fukuyama, K. and Kusano, T., 1989. Sexu4l size dimorphism in a Japanese stream-breeding frog, Buergeria buergeri (Rhacophoridae, Amphibia).
Emlen, S. T., 1976. Lek organization and mating strategies in the bullfrog. Behaa. Ecol, Sociobiol. lz 283-3 I 3. Emlen, S.
^f
., ß77. "Double clutching" and its possible the bullfrog. Coþeia 19772
signifrcance in 7 49-75t.
Emlen, S. T. and Oring, L. W., 1977. Ecology, sexual selection and the evolution of mating systems. Science l97z 215-223.
4., 1986. "Natural Selection in the Wild." Princeton Univ. Press, Princeton, NewJersey.
Endler, J.
Cunent Herþetology in East Asia 306-3L3.
Gabor, C. R. and Halliday, T. R., submitted. Sequential mate choice: mating tactics used by female smooth newts (Triturus tt. aulgaris).
Gallien, L., 1952. Éleuage et comportement du pleurodele au laboratoire. BulI.
Soc. Zool. France
77:
45646t. Garton, J. S. and Brandon, R.
4.,
1975. Reproductive
ecology of the green treefrog, Hyla cinnea, in southern Illinois (Anura: Hylidae). HerþetoLogica 3l: 150-161.
J. M.J., 1972. Existence d'un cycle sexual biennal chez la femelle de Salamandra
Gasser, F. and Joly,
Esteban, M. L., 1990. Evolución del género Rana en la Península Ibérica: Estudio de la variabilidad morfológica y genética del complejo Rana temþoraria L. PhD. Thesis, Universidad Complutense, Madrid.
sahrnandra fastuos¿ Schreiber (Urodèle, Salamandridae)
Fairchild, L., 1981. Mate selection and behavioral thermoregulation in Fowler's toads. Science 2l2t 95O-952.
Gatz, A. J., l98la. Size-selective mating in Hylaursicolor and Hfla cructfer. J. Herþetol. l5: I l4-116.
Fairchild, L., 1984. Male reproductive tactics in an
Garz, A. J., l98lb. Non-random mating by size in American toads, Bufo americanus. Anim. Behau. 29t
explosive breeding toad population. Amer. ZooL. 242
407418. Faria, M. M., in press, A field study of reproductive interactions in Bosca's newt, Triturus åoscøi (Amphibia: Salamandridae). Etholog.
Fellers, G. M., 1975. Behavioral interactions in North American treefrogs (Hylidae). Chesaþeahe Science 16: 2 I 8-2 19.
a différentes altitudes dans les Pyrénées centrales: Influence des facteurs génétiques et climatiques. Ann. Sci. Nat. Zool. (Paris) 14:427444.
1004-1012.
Gerhardt, H. C., 1982. Sound pattern recognition in some North American treefrogs (Anura: Hylidae): implications for mate selection. Amer. Zool. 222 58
l-595.
Gerhardt, H. C., 1991. Female mate choice in treefrogs: static and dynamic acoustic criteria. Anim. Behaa, 42: 615-635.
'tAMPHIBIAN BIOLOGY
460
Gerhardt, H. C., Daniel, R. E., Perril, S. A. and Schram, S., 1987. Mating behavior and male mating success in the green treefrog. Anàm. Behaa.35: 1490-1503.
Gerhardt, H. C., Diekamp, B. and Ptacek, M., 1989. Inter-male spacing in choruses of the spring peeper, Pseudttcris (H1ln) crucifer. Anim. Behau.382 1012-1024.
Giacoma, C. and Crusco, N., 1987. Courtship and male interference in the Italian newt: a ñeld study. Monit, zool. Ital. (N.s.) 2r: 190-191. Gibbons, M. M. and McCarthy, T. K., 1984. Growth, maturation and survival of frogs Rana temþoraria L. Holarctic EcoL 7¿
419427.
Gibbons, M. M. and McCarthy, T. K., 1986. The reproductive output of frogs Rana temþoraria (L.) with particular reference to body size and age. J. Zool., Lond.2092 579-593.
Gill, D. E. and Mock, B. 4., 1985. Ecological and evolutionary dynamics
of
parasites: the case of
Tryþanosoma d.iemycQLi in the red spotted newt Notoþhthalmus tirid.escens. Pp. 157-183 in "Ecology and Genetics of Host-parasite Interactions", ed by
D. Rollinson and R. M. Anderson. Academic Press, New York.
Gittins, S. P., Kennedy, R. L and Williams, R,, 1985. Aspects of the population age-structure of the common toad (Bufo bufo) at Llandrindod Wells lake, mid-Wales. Brit. J. Herþetol. & 441449. Gittins, S. P., Steeds, J. E. and Wiliams, R., 1982.
Population age-structure of the common toad (Bufo ata lake in mid-Wales determined from annual growth rings in the phalanges. Brit. J. Herþetol. 6z 249-252,
bufo)
Given, M. F., 1987. Vocalizations and acoustic inter-
actions of the carpenter frog, Rana
xirgatiþes.
H erþetologica 432 467 481.
Given, M. F., 1988a. Growth rate and the cost of calling
activity in male carpenter frogs, Rana
Behaa. EcoL. Sociobiol,
xirgatiþes.
22: 153-160.
Given, M. F., 1988b. Territoriality and aggressive inter-
actions
of male carpenter frogs, Rana airgatþes. 4ll42l.
Coþeia 1988:.
Given, M. F., 1993a. Vocal interactionsin Bufouoodhousü fowleri. J. Herþetol. 27:
447452.
Haddad, C. F. 8., 1991. Satellite behavior in the neotropical treefro
g Hyla minuta.
J. H erþetol.
25
z
226-229.
Halliday, T, R., 1974. Sexual behavior of the smooth newt, Triturus aulgarß (Urodela: Salamandridae). * 277-292,
r1.
Herþetol.
Halliday, T. R., 1975. On the biological signifrcance of certain morphological characters in males of the smooth newt Triturus aulgaris and of the palmate ll.ewt Tritunls helueticus (Urodela: Salamandridae). Zool. J. Linn, Soc.56¡ 291-300. Halliday, T. R., 1976, The libidinous newt. An analysis of variations in the sexual behaviour of the male smooth newt, Triturus uulgaris. Anim, Behaa, 24t
398414. Halliday, T. R., 1977. The courtship of European newts: an evolutionary perspective. Pp. t85-232 in "'[he Reproductive Biology of Amphibians", ed by D. H. Taylor and S. I. Guttman. Plenum Press, New York. Halliday, T. R., 1978. Sexual selection and mate choice. Pp. 1 80-2 1 3 in "Behavioural Ecology. An Evolutionary
Approach", ed by J. R. Krebs and N. B. Davies. Blackwell Scientifi c Publications, Oxford.
Halliday, T. R., 1983. The study of mate choice. Pp. 3-32 in "Mate Choice", ed by P. Bateson. Cambridge
Univ. Press, Cambridge. Halliday, T. R., 1987. Physiological constraints on sexual selection. Pp.247-264 in "Sexual Selection: Testing the Alternatives", ed byJ. W. Bradbury and M. B. Andersson. John Wiley and Sons, Chichester.
Halliday, T. R., 1990a. The evolution of courtship behavior in newts and salamanders. Adaances in the Studl of Behauior
l9:
137-169.
Halliday, T. R., 1990b. Morphology and sexual selection. Mu. reg. Sci. nat. Torino 1990:9-21. Halliday, T. R., 1992. Sexual selection in amphibians and reptiles: theoretical issues and new directions. Pp.
8l-95 in "Herpetology: Current
Research
on the
Biology of Amphibians and Reptiles", ed by K. Adler. Society for the Study of Amphibians and Reptiles, Oxford, Ohio.
Halliday, T. R., 1993. Sexual selection and mating Pp.264-306in "Evolution. A Biological and Palaeontological Approach", ed by P. Skelton.
systems.
Addison Wesley, Wokingham.
Given, M. F., 1993b. Male response to female vocalizations in the carpenter ftog, Rana airgatiþes. Anim. Behav,46z ll39-1149.
Halliday, T. and Arnold, S. J., 1987. Multiple mating by females: a perspective from quantitative genetics. Anim. Behao. 35: 939-941.
Godwin, G. J. and Roble, S. M., 1983. Mating success in male treefrogs, Hyla chrysoscelis (Anura: Hylidae).
Halliday, T. R. and Hosie, C. A., in prep. Competitive mating in the Californian newt Taricha torosa torosa.
Herþetologica
39: l4l-146.
Gould, S. J., 1966. Allometry and size in ontogeny and phylogeny. Biol. Reu.4l¡ 587-640.
Greenwood, P. J. and Adams, J., 1987. Sexual selection, sexual dimorphism and a fallacy. Oihos 48:. I 06-1 08. Greer, B.J. and Wells, K. D., 1980. Territorial and repro-
ductive behaviour
of the tropical American frog
Centrolenella feischmanni. Herþetologica
36:
3
l8-326.
Grobler, J. H., 1972. Observations on the amphibian P2xiceþhahs adsþersus Tschudi in Rhodesia. Arnoldia (Rhod.) Groves,
6: 14.
J. D., 1980.
the American
Mass
predation on a population of
toad, Bufo arnericanus, Aner, MidL
Natur. l03t 202-203.
Halliday, T. R. andJoly, P., 1981. The functional significance of foot-webbing in European newts (Triturus). Brit. J. Herþetol.
6: l3l-132.
Halliday, T. R. and Verrell, P. 4., 1984. Sperm competition in amphibians. Pp. 487-508 en "Sperm Competition and the Evolution of Animal Mating Systems", ed by
R. L. Smith. Academic Press, New York. Halliday, T. R. and Verrell, P. 4., 1986. Sexual selection and body size in amphibians. Herþetol. /. f : 86-92.
Halliday, T. R. and Verrell, P. A., 1988. Body size and age in amphibians and reptiles. J. Herþetol. 22t 253-265. Harcourt, A. H., Harvey, P. H., Larson, S. G. and Short, R. V., 1981. Testis weight, body weight and breeding system in primates. Nature 293: 55-57.
7 HALLIDAY and f'EJEDO: IN"I-RASEXUAL SELECTION AND ALTERNATIVE Hardrvood, R. H., 1979. The effect of temperature on the digestive efficiency of three species of lizards, Cnemidoþhorus tigris, Gerrhonotus multicarinatrs, and Sceloþorus occidentalis. Comþ. Bioch. Physiol. 63Az
417433. Harvey, A. W., 1988. Sexual size dimorphism and fecundity in satyrid butterflies: a comment. ,At¿¿t. Natur. l32t 750-752.
461
Hosie, C. .A., in prep. Spacing and calìing behaviour of BtLfo asþer in peninsular Malaysia.
Hota, A. K., 1994. Grorvth in amphibians. Gerontolog¡ 40: 147-16, Houck, L., 1977. Reproductive biology of a neotropical salamander,
Bo litoglossa
rostrata. Coþeia 197
7
t
7
0-83
,
Houck, L. D., 1980. Courtship behavior in the pletho-
Harvey, P. H. and Pagel, M. D., 1991. "The Comparative Method in Evolutionary Biology". Oxford Univ. Press, Oxford.
dontid salamander
Desmognathus ochroþhaetts. Amer.
Zool. 20: 825.
salamander Hynobius nigrescens: monopoly of egg sacs during scramble con-ìpetition. J. HerþetoL. 28: 264-267.
Houck, L. D., 1986. The evolution of salamander courtship pheromones. Pp. 173-190 in "Chemical Signals in Vertebrates, Vol. 4: Ecology, Evolution, and Comparative Biology", ed by D. Duvall, D. Muller-Schrvarze and R. NI. Silverstein. Plenum,
Hasumi, M. and In'asarva, H., 1990. Seasonal changes in body shape and mass in the salamander, Hlnobius
Houck, L. D., 1988. The effect of body size on nale
Hasumi, M., 1994. Reproductive behavior of
the
J. Herþetol. 24r I l3-l 18. Hausfater, G., Gerhardt, H. C. and Klump, G. M., 1990. Parasites and mate choice in gray treefrogs, Hlla nigrescens.
uersicolor. Anrcr. Zool. 30: 299-31
Hayes,
T. and Licht, P., 1992.
1.
Gonadal involvement itr
sexual size dimorphisrn in the African bullfrog (Plxiceþhalus adsþerms). J. Exþ. Zool. 264: 130-135. Hedlund, L., 1990. Courtship display in a natural population of crested newts, TrittLrus cristatus. Ethologt 85: 279-288.
Hemelaar, 4., 1983. Age of Bu.t'o åaþ in amplexlrs over the sparvning period. OlÅos 40: l-5. Hemelaar, 4., 1988. Age, grorvth and other population characteristics of Bufo bufo from different latitudes and altitudes..il. Herþetol. 22: 369-388. Heselhaus, R., 1992. "Poison-arrorv Frogs. Their Natural History and Care in Captivity". Blandford, London.
Heusser, H., 1968. Die Lebensrveise der Erdkröte Bzr/o bufo (L.).: Wanderungen und Sommerquatiere. Reuue Suisse de Zoologie 7* 927-982.
Highton, R., 1962. Geographic variation in the life history of the slirny salamander. Coþeia 1962t 597-6 l 3.
Hillis, D. M., Hillis, A. M. and Martin, R. F., 1984. Reproductive ecology and hybridization of the endangered Houston toad (Bufo houstonensis). J. Hu'þetol. l8z 56-72. Hinsharv, S. H. and Sullivan, B. K., 1990. Preclation of Hlla aersicolor and Pesudau'is crucifer during reproduction. rl. Herpetol. 24: 196-197.
Nerv York.
courtship success in a plethodontid salamander. Anint. Belmu. 36: 837-842.
Houck, L. D. and Verrell, P. 4., 1993. Studies of courtship behavior in plethodontid salamanders: review. Herþetologica 492
17
a
5-184.
Horvard, R. D., 1978a. The evolution of mating strategies in bullfrogs, Àana catesbeiana. Erolution. 32: 850-87 1. Horvard, R. D., l97Bb. The influence of male-defended ovipositior-r sites on early embryo mortality in bullfrogs. Ecologl 59t 789-798.
Ho*'arcl, R. D., 1980. Mating behaviour at-rd mating success
in'woodfrogs, Rana slluatica. Anim. Behau.28z
705-7 16.
Horvard, R. D., 1981. Sexual dimorphisrn in bullfrogs. Ecolog¡ 621 303-310. Horvard, R. D., 1983. Sexual selection and variation in reproductive success in a long-lived organism. ,4ner. Natur. l22t 301-325.
Hou'ard, R. D., 1984. Altet-native mating behaviors of young male bullfiogs. Ante¡'. Zool. 24t 397406. 1988a. Reproductive success itr nvo "Reproductive Success", ed by ^f. H. Clutton-Brock. Univ. Chicago
Ho'çvard,
R. D.,
species
of anulans. Pp. 99-l13 in
Press, Chicago.
Horvard, R. D., lg88b. Sexual selection on male body size and mating behavioul in American toads, Bt(o americanus. Anim. Belmu. 36: 1796-1808.
Horvard, R.
D. and I(luge, A. G., 1985. Pt-oximate in rvood frogs.
mechanisrns of sexual selection Erolution 392 26tJ-277.
Höglund, J., I989. Pairing and spawning patterns in the common toad, Bufo bufo: the effects of sex ratio and the time available for male-male competition. ,Anir¿. Behat. 38t, 423429.
Huntir-rgford, F. and Turt-rer,
Höglund, J. and Robertson, G. M., 1987. Random mating by size in a population of common toads
Hutchinson, J. M. C., McNamat-a, J. Nf . and Cuthill, L C., 1993. Song, sexual selection, start'ation and strategic handicaps. Ani¡¡t. Behatt: 45t 1153-1171.
(Bufo bufo). Amþh. Reþt.8: 321-330.
Höglund, J. and Robertson, G. M., 1988. Chorusing behaviour, a density-dependeut alternative rnating strategy in male common toads (Bufo bufo). Ethology 792 324-332. Hôglund, J. and Säterberg, L., 1989. Sexual selection in the common toads: correlates with age and body size. J. euol. BioL. 2z 367-372, Hosie, C. ,{., 1992. Female choice in newts. PhD Thesis, The Open University.
l--
N'ÍATING
4., Ì987. "Animal Conflict". Chapman and Hall, London.
Iela, L., Rastogi, R. K., Deh'io, G. and Bagnara, J. T., 1986. Reproduction in the Mexican leaf frog, Pachyntedttsa dacnicolot:3. The female. Gen. ConQ. Endocrinol. 63: 38 l-392. Jacobson, N. L., 1989. Breeding clynalnics of the Houstou toad. SW Natu'. 342 374-380.
Jacobson, S. K., 1985. Reproductive behavior and male mating success in trvo species of glass fi'ogs (Centrolenidae). Herþetologica
4lt 396404.
AMPHIBIAN BIOLOGY
462
Jacobson, S. K. and Vandenberg, J. J., 1991. Reproductive ecology of the endangered golden toad (Bufo þeriglenes).
J. Herþetol. 252 32I-327.
Jaeger, R. G., 1981. Dear enemy recognition and the costs of aggression between salamanders. Am' Nat. ll7z 962-974. Jaeger, R. G. and Forester, D. C., 1993. Social behavior of plethodontid salamanders. Herþetologica 492
163-t75. Jaeger, R. G. and Gergits, W. F., 1989. Intra- and interspecific communication in salamanders through chemñal signals on the substrate. Anim. Behaa. 27t 150-156.
Jaeger, R. G., Goy, J. M., Tarver, M. and Marquez, C. E., 1986. Salamander territoriality: pheromonal markers as advertisement by males. Anim. Behau.34t 860-864.
Jaeger, R. G. and Schwarz, J. K., 1991. Gradational threat postures by the red-backed salamander. .il. Herþetol. 252
ll2-114.
Jaeger, R. G. and Wise, S. E., 1991. A reexamination of the male salamander "sexy faeces hypothesis"' ,I. Herþetol. 252 370-373.
F.J. and Brodie, E. D., 1989. Tall tails and sexy males: sexual behavior of rough-skinned newts (Taricha granulosa) in a natural breeding pond
Janzen,
Kluge, A. G., l98l. The life history, social organization, and parental behavior of Hykt rosenbergl Boulenger, a ne st-building gladiator frog. Mìsc. Publs. Mus. Zool., IJnia. Michigan 160, vi: l-170.
Klump, G. M. and Gerhardt, H. C., 1992. Mechanisms and function of call-timing in male-male interactions in frogs. Pp. 153-174 in "Playback and Studies of Animal Communication", ed by P. K. McGregor. Plenum, New York.
Knoepfher, L.-P., 1962. Contribution a l'etude de genre Discoglossus (Amphibiens, Anoures). Vie et Milieu l3z r-94.
J. R. and Dawkins, R., 1984. Animal signals: mind-reading and manipulation. Pp. 380402 in "Behavioural Ecology. An Evolutionary Approach", 2nd. Edn., ed by J. R. Krebs and N. B. Davies.
Krebs,
Blackwell Scientific Publications, Oxford.
Krupa, J. J., 1988. Fertilization efficiency in the great plains toad (Bufo cognatus). Copeia 1988: 800-802.
Krupa,.f ..f ., 1989. Alternative mating tactics in the Great Plains toad. Anim. Behau.37: 1035-1043. Kruse, K. C., 1981. Mating success, fertilization potential,
.and male body size in the American toad
Kusano,
'f.,
1982. Postmetamorphic growth, survival,
and age at frrst reproduction of the salamander, Hynobius nebulosus toþoensis Tago in relation to a consideration on the optimâl timing of first repro-
Coþeàa 19891 1068-1071.
Jennions, M. D., Backwell, P. R. Y. and Passmore, N. I., 1992. Breeding behaviour of the African frog, Chiromantis xera.mpelina: multiple spawning and polyandry. Anim. Behatt. 44: l09l-1 100.
(Bufo
americanus). Herþetologica 37 z 228-233.
duction.
Res. Poþ.
Ecol.24t 329-344.
Lack, D., 1968. "Ecological Adaptations for Breeding in Birds". Methuen, London.409 pp. Lamb, T., 1984. Amplexus displacement in the southern toacJ.,
Bufo terrestris. Coþeia 19842 1023-1025.
N. t., 1993. Sperm competition in frogs: testis size and a sterile male experiment on Chiromantis xeramþelina (Rhacophoridae). BioL. J. Linn. So¿. 50: 2ll-220.
Lance, S. L. and Wells, K. D., 1993. Are spring peeper satellite males physiologically inferior to calling males? Copeia 1993¡ I 162-1 166.
Jørgensen, C. 8., 1988. The role of endogenous factors
Lande, R., 1982. A quantitative genetic theory of life
Jennions, M. D. and
Passmore,
seasonal maturation in temperate zone female toads, Bufo bufo. J. Herpetol. 22t 295-300.
history evolution . Ecology 63: 607-615.
in
Lande, R. and Arnold,
selection
Jørgensen, C. 8., 1992. Growth and reproduction. Pp. 439466 i¿ "Environmental Physiology of the Amphibians", ed by M. E. Feder and W. W. Burggren. Chicago Univ. Press, Chicago.
S.
J., 1983. The measurement of
on correlated
characters. Eaolution 372
r2t0-1226. Lee,
J. C., 1986. Is the large-male mating advantage in anurans an epiphenom enon? Oecologta 6* 207-212.
J. C. and Crump, M. L., 1981.
Kagarise-Sherman, C., 1980. A comparison of the natural history and mating system of two anurans: Yosemite toads (Bufo canortu) and black foads (Bufo exsul). Ph.D. Diss., Univ. Michigan, Ann Arbor.
Lee,
Kagarise-Sherman, C. and Morton, M. L., 1993. Population declines of Yosemite toads in the eastern Sierra Nevada of California.rl. Herþetol. 27: 186-198.
Lemckert, F. L. and Shine, R., 1993. Costs of reproduction in a population of the frog Crinia signifersa (Anura: Myobatrachidae) from south-eastern Australia. J. Herþetol. 21: 420425. Licht, L. 8., 1974. Survival of embryos, tadpoles, and adults of the frogs Rana aurora aurore and Rana' þetiosa pretiosa sympatric in south-western British Columbia. Can. J. ZooI. 52: 613427. Licht, L. E., 1976. Sexual selection in toads (Bz/o americanus). Can. J. Zool. 542 1277-1284.
Kalb, H. J. and Zug, G. R., 1990. Age estimates for a population of American toads, Bufo americanus (Salientia: Bufonidae), in northern Yirginia. Brimleyana 16z 79-86. Kapfberger, D., 1984. Untersuchungen zu Populationsaufbau, Wachstum, und Ortsbeziehungen der Gelbauchunke, B ombirn a arie gata u arie gata (Linnaeus, 1758). ZooI. Ant 212: 105-1 16.
Kaplan, R. H., 1985. Maternal influences on offspring development in the California newt, Taricha torosa' Coþeia 19852 1028-1035.
Morphological
correlates of male mating success in Triþrion þetasatus and, Hfla marmoratrß (Anura: Hylidae). Oecologia (BerI.) 5Or 153-157.
Littlejohn, M. J., 1977. Long-range acoustic communication in anurans: an integrated and evolutionary approach. Pp. 263-294 in "The Reproductive Biology of Amphibians", ed by D. H. Taylor and S. I. Guttman. Plenum Press, New York.
HALLIDAYandTEJEDO: INTRASEXUAL SELECTION AND ALTERNATIVE Lizana, M., Márquez, R. and Martin-Sanchez, R. 1994. Reproductive biology of Pelobates cultrþes (Anura: Pelôbatidae) in central Spain.J. Herþetol.28t 19-21. Loman, J. and Madsen, T., 1986. Reproductive tactics of
farge and small male toads Bzlo hufo. Oikos 462 57-41.
Long, D. R., 1987. A comparison of energy substrates and reproductive patterns of two anurans, .Acrrs crepitans and Bufo uoodhousi. Cornp. Biochm. Phlsiol.
874: 8l-91. Lykens, D. V. and Forester, D. C., 1987. Age structure in the spring peeper: do males advertise longevity? H erþe tolo gic a 43 z 2 16-223.
MATING
463
Moore, A. J., 1990. The evolution of sexual dimorphism by sexual selection: the separate effects of intra-
sexual and intersexual selection. Eaolution
'44¿
315-331. Moore, F. L., Seide, R. L., Specker, J. L. and Swanson, L., 1978. Effects of prolactin and methallibure on second metamorphosis and plasma androgens in male newts, Tarichø granulosa. Comþ. Biochem. Physiol.
6lÀz 419422. P. J., 1987: Predation, breeding asynchrony, and the outcome of competition among treefrog tadpoles. Eeologl 682 675-683.
Morin,
MacNally, R. C., 1981. On the reproductive energetics of chorusing males: energy depletion profiles, restoration and growth in two sympatric species of Ranü'ella (Anura). Oecologia 5l: l8l-188.
Morris, M. R., 1989. Female choice of large males in the tteefrog Hyla chrysoscelis: the importance of identify-
Márquez, R., 1993. Male reproductive success in two midwife toads, A\tes obstetricar¿s and A. cütemasü.
Morris, M. R., 1991. Female choice of large males in the treefrog Hyla ebraceata. J. Zool. Lond.223:371-378.
Behaa. Ecol. Sociobiol. 322 283-291.
Márquez, R. and Tejedo, M., 1990. Size-based mating pattern in the treefrog Hyla arborea. Hnþetologica 46:
172-r78.
scale
of
choice. Behau. Ecol. Sociobiol. 252
275-28r.
Mulder, B. S., Schultz, B. B. and Sherman, P. W., 1978. Predation on vertebrates by Clark's nutcrackers. Cond.or 8Oz
449451.
Murphy, C. G., 1994. Chorus tenure of male barking
Martins, M., 1993. Observations on the reproductive behaviour of the Smith frog, Hylnfaber. Herþetol. J. 3z 3l-34. 4., 1988. Sexual interactions in red-spotted newt populations. Anim. Behaa. 36: 205-2 10.
Massey,
Mathis, 4., l99la. Large male advantage for access to females: evidence of male-male competition and female discrimination in a territorial salamander. Behau. EcoI. Sociobiol. 29: 133-138.
Mathis, 4., l99lb. Territories of male and female terrestrial salamanders: costs, benefi ts, and intersexual spatial associations. Oecologin 862 433440.
Maynard Smith, J., 1982. "Evolution and the Theory of Games". Cambridge Univ. Press, Cambridge.
Maynard Smith, J. and Harper, D. G. C., 1988. The evolution of aggression: can selection generate variability? Phil. Trans. R. Soc. Ser. B 3l9z 557-570. Maynard Smith, J. and Price, C., 1973. The logic of animal conflict. Nature 246: 15-18. -Mayr, 8., 1972. Sexual selection and natural selection. Pp. 87-104 ¿n "Sexual Selection and the Descent of Man" ed by B. Campbell. Heinemann, London.
McAlpine, S., 1993. Genetic heterozygosity and reproductive success in the green treefrog, Hyla cinerea. Hneditl 70: 553-558. McDiarmid, R. W., 1978. Evolution of parental care in frogs. Pp. 127-147 in "The Development of Behavior: Comparative and Evolutionary Aspects", ed by G. M. Burghardt and M. Bekoff. Garland STPM Press, NewYork. McWilliams, S. R., 1992. Courtship behavior of the smallmouthed salamander (Amblstoma texanutn): the effects of conspecific males on male mating tactics. Behauiour
ing the
l2l: l-19.
Mitchell, S. L., 1990. The mating system genetically affects offspring performance in Woodhouse's toad (Bufo woodhau.sei). Euoluti.on
M:
502-5 19.
Miyamoto, M. M. and Cane, J. H., 1980. Behavioral observations of non-calling males in Costa Rican Hyln ebraccata. Biotropica l2t 225-227.
frogs, Hyla gratiosa. Anim. Behaa. 482 763-777.
Nagy, K. ,4.., 1983. Ecological energetics. Pp. 24-54 in "Lizard Ecology: Studies of a Model Organism", ed by R. B. Huey, E. R. Pianka and T. W. Schoener. Harvard Univ. Press, Cambridge, Mass. Newman, R.4., 1988. Adaptive plasticity in devçlopment of Scaþhioptts couchü tadpoles in desert ponds. Eztolution 42: 7 7 4-7 83.
Newman, R. 4., 1989. Developmental plasticity of Scaphiolrus couchü tadpoles
in an
unpredictable
environment. Ecology 7O': 1775-1787. Newman, R. 4., 1992. Adaptive plasticity in amphibian metamorphosis. BioScience 422 67 147 8.
Noble, G. K., 1954. "The Biology of the Amphibia". Dover Publications, New York.
Obert, H.-J., 1977. Hormonal influences on calling and reproductive behavior in anurans. Pp. 357-366 in "The Reproductive Biology of Amphibians", ed by D. H. Taylor and S. I. Guttman. Plenum Press, New York.
Olson, D. H., 1989a. Predation on breeding western toaðs (Bufo bmeas). Copeia 1989: 391-397.
H., 1989b. The Ecological and Behavioral Dynamics of Breeding in Three Sympatric Anuran Amphibians. PhD. thesis, Oregon State University,
Olson, D.
Corvallis.
Olson, D. H., Blaustein, A. R. and O'Hara, R. K., 1986. Mating pattern variability among western toad (Bufo boreas) populations. Oecologiø 70: 351-356. Ovaska,
K. and Davis, T. M.,
1992. Faecal pellets as
burrow markers: intra- and interspecifrc odour recognition by western plethodontid salamanders.
Anim. Behau. 43: 931-939. Ovaska, K. and Hunte, W., 1992. Male mating behavior
of the frog Eleutherodacllus johrctonei (Leptodactylidae) in Barbados, West Indies. Herþetologica 48:40-49.
Pallett, J, R. and Passmore, N.
I.,
1988. The signiñcance
advertisement calls in a reed frog, Hyþerolûrs tubnilinguis. Bioacoustics I : I 3-23.
of multi-note
AMPHIBIAN BIOLOGY
464
Parker, G. 4., 1970. Sperm competition and its evolutionary consequences in the insects. Biol. Rea. 45:525-568. of
Partridge, L. and Halliday, T., 1984. Mating patterns and mate choice. Pp. 222-250 i¿ "Behavioural Ecology. An Evolutionary Approach", Znd. Edn., ed byJ. R. Krebs and N. B. Davies. Blackwell Scientific Publications, Oxford.
N. L and Carruthers, V. C., 1979. "South African Frogs". Witwarersrand Univ. Press,
Passmore,
Johannesburg. N. I. and Telford, S. R., t981. The effect of
Passmore,
chorus organization on mate localization in the painted reed frog (Hyþerotius mar"morahu). Behau. Eeol. Sociobìol, 9: 291-293. Telford, S. R., 1983. Random mating by size and age of males in the painted reed frog,
Passmore, N. I. and
Hyþerolhu m(umorah$. S. á...¡f. Sci. 79: 353-355. Patón, D., Juarranz,
4., Sequeros, E., Pérez-Campos,
R.,
López-Torres, M. and Barja de Quiroga, G., 1991. Seasonal age and sex structure of Rana þerezi asæ.ssed by skeletochronology...¡1. H erþetol. 25: 389-394.
Perrill, S, 4., 1984. Male mating behavior in Hlla regilla. Coþeia 1984:727-732.
Perrill, S. A. and Daniel, R. 8., 1983. Multiple egg clutches in Hgla regilla, H. cinerea and H. gratiosa. Coþeia 19831 513-516.
Perrill, S. 4., Gerhardt, H, G. and Daniel, R.,
1978.
Sexual parasitism in the green treefrog, HyLa cinerea. Science 2002 I
179-I 180.
Perrill, S. 4., Gerhardt, H. G. and Daniel, R.,
1982.
Mating strategies shifts in male green treefrogs (H1la cinerea): an experimental study. Anim. Behau. 302
4348. S.
and male-male communication in the
H.,
1993. "The Ecological lmplications of Body Size". Cambridge University Press, Cambridge.
Peters, R. Petranka,
J. N., 198I. Multiple paternity in a natural population of the alpine newt, Triturus alþestru (Laur.). Amþhibàa-Reþtilia 2z 282.
Rastogi, R. K., Iela, L., Di Meglio, M., Di Matteo, L., Minucci, S. and lzzo-Vitiello, I., 1983. Initiation and kinetic profiles of spermatogenesis in the frog, Rana . escul¿nkt (Amphibia)./. Zool. Lontl^ 201: 515-525. Raxworthy, C. J., 1989. Courtship, frghting and sexual
dimorphism
of the banded l:ewt, Tritunß 8l: 148-170.
aittatl¿s
oþhryticus. Ethology
Raxworthy, C. J., 1990. Non-random mating by size in
the midwife toad
Alytes obstetricans:
cârry more eggs. Amþhibia-Reþtilia
llz
bigger
males
247-252,
Reading, C. J. and Clarke, R. T., 1983. Male breeding behaviour and mate acquisition in the common toad, Bufo bufo. J. Zool. Lond. 20l: 237-246. Reading, C. J. and Clarke, R. T., 1988. Multiple clutches, egg mortality and mate choice in the mid-wife toad, Alltes obstetricans. Amþhibia-Reþtilia. 9z 357 -364.
Richards, C.
M.,
1977. Reproductive potential under
laboratory conditions of Hyþerolius úridifauus (Amphibia, Anura, Hyperolidae). J. Herþ. ll:
42M28.
Ritke, M. E., Babb, J. G. and Ritke, M. K., 1992. Temporal patterns ol reproductive activity in the Gray treefrog (H1la chrysoscelis). J. Herþetol. 262 107-1
il.
Ritke, M. E. and Semlitsch, R. D., 1991. Mating behavior and dete rminants of male mating succe ss in the gray treefrog, Hyla chrysoscelis. Can. J. Zool. 69t 246-250. Roberts, W. E., 1994. Explosive breeding aggregations
and parachuting in a neotropical frog,
Agalychnis
saltator (Hylidae). J. Herþetol. 28: 193-199.
A. and Shepherd, W.J., 1989. Spatial distribution northerrr cricket frog, Acris ereþitans blanchardi. J. HerþetoL.23z 237-243.
Perrill,
îewrTo,r¿chú granulosa. Anim. Behau. 4lz 541-554.
Rafinski,
4.,
1984. Assessment strategy and the evolutron fighting behaviour..¡1. theor. Biol. 472 223-243.
Parker, G.
Propper, C. R., 1991. Courtship in the rough-skinned
J. W., Sih, ,{., Kats, L. B. and Holomuzki, J.
R., 1987. Stream drift, size-specific predation, and the evolution of ovum size in an amphibian. Oecologi.a (Berl.)
7L
624-630.
Petrie, M., 1983. Mate choice in role-reversed species. Pp. 167-119 in "Mate Choice", ed by P. Bateson Cam bridge Univ. Press, Cambridge. Pierantoni, R., Varriale, 8., Simeoli, C., De Matteo, L., Milone, M., Rastogi, R. and Chieffi, G., 1983. Fat bodies and autumn recrudescence of the ovary in Rana esculenta. Comþ. Biochem. Pþsiol. 76A:.
3l-35.
Pierce,J. R. and Ralin, D. 8., 1972. Vocalization behavior of the males of three species in the Hfla uersicolor complex. Herþetologica 282 329-337 .
l. E. and Lothrop, 4., 1993. Body size and age assessment among advertising male chorus frogs.../. Herpetol. 27: 109-l I l.
Plarz,
Pough, F. H., Magnusson, W. E., Ryan, M.J., Wells, K. D. and Taigen, T. L.; 1992. Behavioral energetics. Pp. 395436 in "Environmental Physiology of the Amphibians", ed by M. E. Feder and W. W. Burggren Chicago Univ. Press, Chicago.
J. G. M., 1986. Female choice, male strategies, and the role of vocalizations in the Australian frog Uþeroleia rugosa. Anim. Behatt. 34t 773-784.
Robertson,
J. G. M., 1990. Female choice increases fertilization success in the Australian lrog, Uþeroleia
Robertson,
laerigata. Anim. Behaa. 39: 639-645.
Roble, S. M., 1985. Observations on satellite males in Hyla chrysoscelis, Hyla þicta and Pseudacris triseriata. J. Herþetol. l9z 432436.
Roithmair, M. 8., 1992. Territoriality and male mating success in the dart-poison frog, Eþiped,obates femoralis (Dendrobatidae, Anura). Ethology 922 33 l-343.
Roithmair, M. E., 1994. Male territoriality and female mate selection in the dart-poison frog Eþiþed,obates triuittatus (Dendrobatidae , Anura). Coþeia 1994t 107-l 15. Rose, F. L., 1967. Seasonal changes in lipid levels of the salamander Arnþhiuma means. Coþeia 1967 z 662-666.
Rubenstein, D. I., 1980. On the evolution of alternative mating strategies. Pp. 65-100 i¿ "Limits to Action: the Allocation of Individual Behavior", ed by J. E. R. Staddon. Academic Press, New York.
Ryan, M. J., 1980. The reproductive behavior of the bullfrog (Rana catesbeiana). Coþeia 1980: 108-l 14. Ryan, M. .J., 1983. Sexual selection and communication in a neotropical frog, Pþsakemus þtstulosus, Eaolutiut
31:261-272.
AND ALTERNATIVE MATING HALLIDAYANdTEJEDO: INTRASEXUAL SELECTION
Semlitsch, R. D', Scott, D. E. and Pechmann, J' H',K ' and size at metamorphosis related to ISSS. fi*.
in Sexual Ryan, M.J., 1985' "The Túngara Frog., a Study
'
and Communication" Chicago Press, Chicago' Seleciion
University of
uãrllt fitn... in
biases. ,4n2. Nat' (SuþþI
Ph\salaemu.s þustuloius
in
) 139: S4-S35'
in the Amphibia. Copeia 1979: 297-306' R., 1990. Proximate determinants of sexual Shine, "^-"^ãiff..å"*s in adult body size' Amer' Nahn' 135"
(sexual selection for
278-283. L. J., Brooks, R. J', Barta, J' R and Desser' S' Shirose, """' s., ìsgd. interse*ual difrerences in growlh'.mortality' ãti¿..i- at maturity in bullfrogs in central Ontario' Can. J. Zool. 7lt 2363-2369'
EcoL Soeiobiol Sz 273-278'
M. I., Tuttle, M. D. and Rand, A' S" 1982' Bat Rvan. ^'-';t;à;ïi";u.t¿ t.*"ul advertisement in a neotropical '1rog. Am. N¿¿. l19: 136-139'
C., 1968. Crested îewq Tritunß Simms, "'^--^iu,r..t-tii,rs,
and maturation
Rvser, I., 1988. Determination of growth ^''-î';it; lo-r,,or, lrog' Rana-temþoraria' by skeleto-
Br. J. Herþ' 4': 43.
Smirina, E. M., t994. Age determination and longevity
loss, reproductive output'.and reproäuction in ihe common ltog' Rnna
Rvser, I., 1989. Weight --'"-ir,.'."u
D. Sassoon, "-""äì*".pt
8¿
i.
in amphibians . Gerontology 40: I 33-l46' frogs: Smith, D. C., 1987. Adult recruitment in chorus *"^--Jf..rt of sire and date at metamorphosis' Ecologl
264-268'
A. and Kelley, D B" 1986' The
sexually
68: 344-350.
larynx of Xínopus laeuis: development and
;;ã;;ä.; regilation.
Amer'
Reptiles"' Smith, M., 1951. "The British Amphibians and Collins, London. Smith, R. E', 1941. Mating behavior -in Taricha torosus aÁd related newts. Coþiia l94lz 255-262'
J' Anat' 177" 457472'
M., 1935. The influence of external factors on spawning date and migration of the-common lrog,'Rana lemporaria temþoraria' Proc' Zool' Soc''
R. Savaee, --
ñ;;
Lo;d.
R. L., 1984. "Sperm Competitionand the Evolution Smith, "^-^oi À"i*ul Mating SystemJ"' Academic Press' New York. de Snarreboom, M., 1984. Gedrag en voortplanting van
lgïl.49-98
R. M., 1961. "The Ecology and Life History of fie Common Frog". Pitman, London'
SavaEe.
R. -Schaaf,
T. and Carton,J' S',
"t-'*.ãi,..tulamanders
1970'.Raccoo-n predation
American tou[, au¡o americantt's' Herþetologica
àn ttt. 262 334-335.
chinensis. ln'eerta 43¿
sexual dimo-rphism'
Schwartz. I. -amphibians: I., 1987. The function of call alternation in .^-a test of three hypotheses' ui".uä
4614ll'
and Schwartz, .l' J' and Wells, K' D', 1985' Intra*-" i;;;pi.i:frc vocal behavior of the neotro,pical tree-
27-38'
effect of larval density on adult traits in Ambystoma oþúcum' Ecologl 75t
Scott, D. E., 1994' The *'"ä.-.g;"phic 1383-1396.
R' D', Semlitsch, "---^ïu."fiuriu.ly
lgsS Reproductive strategy of
a
paedomorpÉic v.lamander Amþstoma
telþlideutn. Oecologia 65: 305-3 13'
R' D., 1994. Evolutionary consequences of Semlitsch, --.tãrr-iurr¿om mating: do large males increase offtp.itg ni"... in thä anuranlufo bufo? Behøa Ecol' Sociobiol. S4z
SÞmns. I. A', 1983. Sexual selection, ""-"""i'i.*i,oriality. Pp' I69-204 jn ''Lizard Ecology: Si,rdi.t of a Módel'Organism", ed by R B . Huey' n. n. piutttu and T. Ù' Schoener' Harvard Univ' Press, Cambridge, Mass'
in
19-24'
of egg Semlitsch, R. D. and Gibbons, J' W" tgg0 Effects complex in larval"salamanders of size on success ."ui."nments' Ecology 7 lz 1789-1795' "qr-,uti.
species
J. A" t993. Sexual size dimorphism *ith"ury-ptotic growth after maturity BioL J' Linn'
Stamps.
unison Schwarrz,J'J., 1991. Why stop.calling? A studyof "-^^ fo"lJitiging in a ne'otroþical trèefrog Anim Behaa' 42t 565-577 '
mi'øoceþhala' Coþeia 19852
28-35'
l5l-161.
female Schwartz, J. J., 1986. Male calling^behavior and choice in the Neotropical treefrog HyIa mi'croceþhala' Etholog 732 116-127 '
ir"g ìIyk
Paratiesotriton honhongensß en P'
M., 1994. On the sexual behaviour of the Soarreboom, "t-'t*ã.ã-iãir.d newt, Clnoþs ensicauda (Hallowell' l7z 1aøoj. mn""alungen uÁd Èerichte fiir Naturhunde
K., 1984' "scaling: Why anim-al size is Schmidt-Nielsen, ".-':.å irnpotruni". iambridge University Press' London'
Ettolution 4lz
cristahts'
double brooded in an indoor vivarium'
chronology...if. Zool. Lond' 216: 673-685'
7
of secondary sexual Eurycea qua'dridiginta' Copeòa 19762
830-833.
M. I., Tuttle, M. D. and Taft, L' K'' l98l' The Rvan. '-'-^.ftr. u'"¿ benefits of frog chorusingbehavior' Behat'
temþoraria. Oeiolo gia
69:.
dimorphism Shine, R., 1979. Sexual selection and sexual
,.r,io.y áxploir at ion). Ea o lu Li on 44t 305-Z | 4'
of
Ecolog
D. M., 1976. Induction Sever, -- -.íru.u.r.r"
M. I. and Rand, A. S', 1990' The sensory basis of Rvan. ' ..*t,ui selection [or complex calls in the túngara
lros.
Amblstoma to'tþoideum'
18.{-192.
M. I. and Keddy-Hector, A', 1992' Directional Rvan, ^'*'ri"ii"tit åi f.-ut.'mate choice and the role of
L"t".y
465
So¿.
50: 123-145. behavior of the
Staub, N' L., 1993. lntraspecific agonistic '"--tåf^Á""¿.r Aneides faaifunrtatus {Amphibia:
Þì.ì-ttããã"ti¿u.) with compârison to other plethodontid species . Herþetologtca 49:. 271-282' S. C. and Crandall, R' E, 1981' Quantitative Stearns, ""'-l..iail,iã"s of delayed maturity' Euolution 352
455463. Stewart, ---
M. M. and Bishop, P'.J"
1994'..Effects of
sound level of ädvertisement calls on calling ;;Ëi;;gt, Eleutherodactylus coqui' J' Herþetol 28z
in...ur.d
46-53. B' K., 1982a' Male mating behavio-ur in the Sullivan, "-'^^gì.ãtlr;i* ßad (Bufo cognatus)' Anim' Behat't' 302 939-940. selection in Woodhouse's Sullivan, "*";;ã B. K., 1982b. Sexual organization' Anim' Chorus I' ¡Bufo'uoodhou,szi) 680-686' 3Oz Behaa.
AMPHIBIAN BIOLOGY
466
Sullivan, B. K., 1983. Sexual selection in the great plains toad, (Bufo cognatus). Behaaiour
84:258-264.
Sullivan, B. K., 1984. Advertisement call variation and observations on breeding behavior of Bufo d,ebilis and
frogs (Hyþerokus marmorahs). Bioaeoustics 2t 47-53.
Sullivan, B. K., 1987. Sexual selection in Woodhouse's
Telford, S. and van Sickle, J., 1989. Sexual selecrion in an African toad (Bufo gutteralis): the roles of morphology, amplexus displacement and chorus
Sullivan, B. K., 1989. Mating
Thiesmeier, B. and Hornberg, C., 1990. Zur Fortpflanzung ; sowie zum Paarungsverhalten der Gebirgsmolche,
Bufo þunctatus.
J. Herþetol. 18: 406--41
1.
toad, (Bufo woodhousei) IIL Seasonal variation in male mating success. Anim. Behau. 35: 912-919.
system
variation in
Woodhouse's toad (Bufo uood,housei). Ethology 83: 60-68.
Sullivan, B. K., 1992. Sexual selection and calling behavior in the American toad (Bufo americaruts). Coþeia 1992t
l-7.
Sullivan, B. K. and Hinshaw, S. H., 1992. Female choice and selection on male calling behaviour in the grey treefrog Hyla aersicolor. Anim. Behaa. 44t 733-744.
Sullivan, B. K. and Sullivan, E. 4., 1985. Variation in advertisement calls and male mating success of Scaþhioptu bombifrons, S. couchi and, S. multiþlicahu (Pelobatidae). SW Natur. 302 349-355.
Summers, K., 1989. Sexual selection and intra-female competition in the gr:een poison-dart frog, Dend.robates auro.tuß. Anim. Behat.
37: 797-805.
Sutherland, W.
J., 1987. Random and
components ofvariance in mating
deterministic
success. Pp.
in "Sexual Selection: Testing the
209-219
Alternatives", ed by J. W. Bradbury and M. B. Andersson. John Wiley and Sons, Chichester.
Talavera, R., 1989. Evolución de Pelobatidae Peloditidae (Amphibia: Anura): morfología desarrpllo
del sistema esquelético. PhD.
y y
thesis,
Universidad Complutense de Madrid, Madrid. Tarkhnishvili, D. N., 1994. Breeding of the toad Bufo
sexual dimorphism and shifting spawnin g sires. Amphibia- Reþtilia I 5 : I 9 I - 1 98. Tejedo, M., 1988. Fighting for females in the toad Bufo rerrucosissimu.s:
calamita is affected by the operational sexratio. Anim Behaa. 36: 1765-1769.
Tejedo, M., 1989. Selección sexual y éxiro reproducror en el sapo corredor, Bufo calnmita. PhD. thesis, University ol Córdoba.
Tejedo, M. 1992a. Large male maring advantage in
natterjack toads, Bufo calamita. Sexual selection or energetic constraints? Anim. B ¿haa. 44:. 557 -569.
Tejedo, M., 1992b. Variation in viability during development and hatching success in embryos of the toad Bufo calamita. Herþetol. J. 2t 142-144.
Tejedo, M., 1992c. Effects of body size and timing of reproduction on reproductive success in female natterjack toads (Bufo calamita). J. ZooI. Lond. 22Bz 545-555.
Tejedo, M. and Reques, R., 1992. Effects of egg size and density on metamorphic traits in tadpoles of the natterjack toad (Bqo calnmitn).J. Herþetol.26z 146-152.
Telford, S. R. and Dyson, M. L., 1988. Some dererminants of the mating system in a population of painted reed lrogs (Hyþerolfus marmoratrc). Behnaim.r f 06: 265-278.
Telford, S. R. and Dyson, M. L., 1990. The effects of rainfall on interclutch interval in painted reed frogs ( H yþ er o Lius marmoratrc ). C oþ ia 1990 2 644-6 48. e
participation. Behatiour I
l0:
62-75.
Gattung Euþoctus (Gené), im Terrarium, unter besonderer Berücksichtigung von Euþroctus asþer (Dugès, 1852). Salamandra 262 63-82.
Thomas, E. O., Tsang, L. and Licht, P., 1993. Comparative histochemistry of the sexually dimorphic skin glands of anuran amphibians. Coþeia 1993l. 133-143.
Thomas, J. S., 1989. Courtship, male-male comperirion, and male aggressive behavior of the salamander Eurycea bislineata. MSc Thesis, University of Southwestern Louisiana, Lafayette.
Thornhill, R. and Alcock, J., 1983. "The Evolution of
Insect Mating Systems", Harvard Univ.
Press,
Cambridge, Mass.
Tilley, S. G., 1980. Life histories and
compar.ative
demography of two salamander populations. Coþeia
Summers, K., 1992. Mating straregies in two species of dart-poison frogs: a comparative study. Anim. Behau. 43: 907-919.
É--
Telford; S., Dyson, M. L. and Passmore, N. I., 1989. Mate choice only occurs in small choruses ofpainted reed
1980:806-821. Tilley, S. G. and Hausman, J. S., 1976. Allozymic varia-
tion and occurrence of multiple inseminations in populations of the salamander Desmograthus
ochroþhaeus. Coþeia 197 6z 7 34-7 41.
Tinsley, R. C., 1990. The influence of parasire infection on mating success in spadefoot toads, Scaþhioþtu couchü. Amer, Zool.302 313-324. Townsend, D. S., 1984. The adaptive significance of male parental care in a neotropical frog. PhD. thesis, State University of New York, Albany. Townsend, D. S, and Stewart, M. M., 1994. Reproductive ecology of the Puerto Rican frog Eleutherodacehu coqui.
J. Herþetol. 28:3440.
J., 1983. Variation in development patterns of larval anurans in temporary ponds. L Persistent
Travis,
variation within a Hyla gratiosa population. Eaolution 37: 496-512. Travis, J., Emerson, S. B. and Blouin, M. L., 1987. A quantitative-genetic analysis of larval life-history traits in Hyla crucifer. Eulution 4l: 145-156.
Trivers, R. L., 1972. Parental invesrment and sexual selection. Pp. 136-179 iz "Sexual Selection and the Descent of Man", ed by B. Campbell. Heinemann, London-
Turner, F. 8., 1958. Life-history of the wesrern spotted frog in Yellowstone National Park. Herþetologica l4z 96-100.
Turner, F. B., 1960. Population srructure and dynamics
of the western spotted frog,
Rana þ. pretiosa Baird
and Girard, in Yellowstone Park, Wyoming.
Ecol.
Monogr. 30t 251-278.
Tyler, M. J., 1976. "Frogs". The Ausrralian Naturalist Library. Collins, Sydney.
Verrell, P. 4., 1982. The sexual behaviour of the redspotted îewq Notoþhthalntu uiridesceru (Amphibia: Urodela: Salamandridae). Anim. Behau. 30: 1224-1236.
HALLIDAYandTEJEDO:INTRASEXUALSELECTIoNANDALTERNATIVEMATING46T P. 4., 1983a. The influence of the ambient sex Verrell, ratio uná intermale competition on the sexual newt, Notoþhthalmas behavior of the ied-spotted úridescen's (Amphibia: Urodela: Salamandridae)' Behat. EcoI. Sociobiol. 13: 307-3
l3'
Verrell, P. 4., 1983b. An unusual population of toads' Brit. Herþ. Soc. BuIL 8¿ 3l-32.
Verrell, P. 4., 1984. Sexual interference and sexual deíense in the smooth newt, Trituns oulgark (Amphibia, Urodela, Salamandridae)' Z' Tierpslchol' 662 242-254.
4., 1986. Wrestling in the red-spotted newt (Nitophthalmus airùlescenl: resource value and contéstant asymmetry determine con-test duration and outcome. .,4 nim. Behatt. 34': 398402'
P. Verrell, -
Verrell, P. 4., 1987a. Growth in the smooth newt (Triturus tulgøris) during the aqullic phase of the annual cycle. Herþetol.
J' lz
137-140'
4., 1987b' Limited male mating capacity. in thé male smooth newt, Triturus uulgaris (Amphibia)' l. Comþ. PsYchol. l00z 291-295'
P. Verrell, -
P. A' and Brown, L. E', 1993' Competition Verrell, u-orlg ferhales for mates in a.species with male pu...täl care, the midwife toad Alytes obstetricar¿s' EthoLogl
9*
247-2b7.
Verrell, P. and Donovan,4., 1991' Male-male aggression in' the plethodontid salamander Desmognathus ochroþhaeus. J. Zool. Lond' 223l. 203-212'
Verrell, P. and Halliday, T', 1985' Re productive
rlvnamics of a population of smooth newLs' Trilurus uLlgaris, in sort^hern England' Herþetologica 41" 386-395.
Verrell, P. 4., Halliday, T. R. and Griffiths, M' L" 1986' The annual repróductive cycle of the smooth newt (Tritunu aulgarisS in England'./' Zool' Lond' 6) 2l0z l
01-l
19.
Verrell, P. A. and McCabe, N., 1988' Field observations
on the sexual behaviour of the smooth newq Triturlrs xulgaris aulgaris (Amphibia: Salamandridae)'
J'
Zool'
Lond.2l4z 533-545.
Vilter, V. and Vilter, 4., 1960. Sur la gestation de la sálamandre noire des Alpes, la Salamandra atra Laut' Comþtes Rendus de Ia Socilté de Biologie
154:290-294'
Vincent, 4.. Ahnesjö, I., Berglund' A' and Rosenqvist' c.,'ßd2. PipeÉshes and ieahorses: are they all sex .oi. ..u..ted? Trends Ecol. EaoI' 7t 237-241' Wasner. W. E., 1989a. Fighting, assessment and frequency 'alteration in Blanchärd'i cricket frog Bchaa' Ecol' Sociobiol.2Sz 429436.
Wagner, W' E., 1989b' Social correlates of variation in '-ule calling behavior in Blanchard's cricket frog' Acris
øeþitu^ blnnchardi. Etholog
822
2745'
Walls, S. C. and Altig, R., 1986. Female reproductrve
biology and larval life history of Ambystomn salamänders: a comparison of egg size, hl"Hlrrg size, and larval
growih. Herþetologica 422 334-345'
Warner, S. ó., Dunson, W. A. and Travis,J', l99l' Interactíon of pH, density, and priority effects on the
survivorship and grówth
of two
tadpoles. Oecologia (Berlin) 88l. 33
s^p^e^cies
of hylid
l-339'
Wells, K. D,, 1976. Multiple egg clutches in the green lrog (Rana chmitans). Herþetologtca 32: 85-87' Wells, K. D., I977a. The social behaviour of anuran amphibians. Anim. Behnzt. 25¡ 666-693'
Wells,
K. D., 1977b. Territoriality and male mating i.t the green Írog (Rana clnmitatts)' Ecology
success
58.750-762. 1977c. The courtship of frogs' Pp-' 233-262 Reproductive Biology of Amphibianf ' ed by D. H. Täylor and S' I. Guttman' Plenum Press' New York.
Wells, K.
D.,
n ln
Wells, K. D., 1978a. Territoriality in the green fro$(Rana eiamitan"s): vocalizations and agonistic behaviour' Anim. Behau. 26: l05l-1063.
Wells, K. D., 1978b. Courtship and parental behavior in
a- Pa.tamanian poison-arrow frog
(Dendrobates
aurattu). Herþetologica 34: 148-155'
Wells, K. D., 1979. Reproductive behavior and male mating success in a Ñeotropical toad, Bufo tyþhoni:r' BiotroPica
Il: 30l-307
Wells, K. D., 1980a. Social behavior and communication of a dendrobatid frog (Cotostethus trinitatis)' Herþetologba
36: 189-199.
Wells, K. D., 1980b' Behavioral ecology and. social o.gurrirutiott of a dendrobatid frog -(Colostethus in{uinalis). Behat-t. Ecol. Sociobiol' 6: I99-209' Wells, '' - K. D., 1981. Parental behavior of male and fe male i.ont. Pp. 184-197 iz "Natural Selection and Social g"fiavior: Recent Research and New Theory"' ed by
R. D. Alexander and D. W' Tinkle' Chiron Press'
New York. Wells, K. D., 1988. The effect of social interactions on ar,uran uocal behavior. Pp.433454 in "The Evolution of the amphibian Auditóry System", ed by.B' Fritzsch' Vl. t. nvuit, W. Wilczynski. Í. E' Hetherington and W."Waliowiak. WileY, New York' Wells, K. D. and Schwartz,J.J',
l984
Vocal communica-
tion in a neotropical treefrog, Hyla advertisement calls.' Anim.
B
ehaa' 322
ebraccata:
405420'
Werner, E. E., 1986. Amphibian metamorphosis: growth
rate, predation rate, and th9 9g¡imal size at transformátion. Am. Na| 128: 319-341'
M' J., 1983. Sexual selection, social competition, anð speciation ' Quart' Rea' Bìo1 58"
West-Eberhard, 155-183.
Wagner, W. E., 1992. Deceptive or honest signalling-of 'nghri"g abilityl A test ôf alternative hypotheses for th"e fuñction óf .hrng.. in call dominant frequency by male cricket frogs. Anim' Behaa' Mt 449462'
Weygoldt, P., 1981. Beobachtungel '-9,1 |91pn1"'L.tgiUiologie von Phlllod)-tes lute-olzs (Wied 1824) im
Waiehts. V., submitted. Female sexual interference in the "smooth newt Triturtu a uulgaris'
t.ä ierritorialitv in a dendrobatid ftog Dendtobates neptili'a l5z 17 l-l8l Whitney, C. L. and Krebs, J' R', 1975' Spacing and
Walkowiak, W., 1992. Acoustic communication in the frre-beilied. toad: ân integrative neurobiological approach. Ethol. Ecol. Et'tol. 4" 63-74'
Teriarium. S¿Iamandra
l7: l-ll'
van Wiinsaarden, R. and van Gool, S', 1994' Site fidelity granuliferus.,+mþhibia-
.ufíi"g in Pacific tree frogì, Hyla regilla' 53: l5l9-1527.
Can'
J'
Zool'
468
AMPHIBIAN BIOLOGY
Wilbur, H. M. and Alford, R. A., 1985. priority effects in cxperimental pond communities: responses of Hyla to Bufo and Rana. Ecologl 66: t 106-l I 14. Wilbur, H. M., Rubenstein, D. I. and Fairchild, L., 1978.
in toads: the roles of female choice and male body size. Eaolution 322 264-270. Sexual selection
Williams, G. C., 1975. "Sex and Evolution". princeton Univ. Press, Princeton, New Jersey. Wise, S. 8., 1991. Territorial conflicts by tail-autotomizing salamanders: males play asymmetric games. Masters Thesis, U. of Southwestern Louisiana, Lafayette.
Woodward, B. D. and Travis, J., 1991. paternal effects on juvenile growrh and survival in spring peepers (Hyla crucifer). EuoL Ecol.5: 40-51. Woodward, B. D., Travis, J. and Mitchell, S., 1987. The effects of the mating system on progeny performance in Hyla .cntcifer (Anura: Hylidaè). Euotution 42t
. 784-794. Woolbright, L. L., 1983. Sexual selection and dimorphism in anuran Amphibia. Amer. Natur.
ll0-11q.
Woodward, B. D., 1982a. Sexual selection and nonrandom mating patterns in desert anurans (Bufo uoodhousei, Scaþhioþus eouchi, S. multiplicatus bombifrons). Coþeia 1982: 35 l-355.
and-ï.
Woodward, B. D., 1982b. Male persistence and mating success in Woodhouse's toacl (Bufo uoodhotueil. Ecologl 63t 583-585.
Woodward, B. D., 1986. Parernal effecrs on juvenile growth in Seaþhioþus rnultiþkcahu (The New Mexico spadefoot toad). Amer. Natur. l28z 58-6b. Woodward, B. D., 1987. Parernal effecrs on offspring
traits in
Woodward, B. D. and Mitchell, S., 1990. predation on frogs in breeding choruses. SW Natur. Z\t 44g4b0.
Scaþhioþus couchi
Oerologia 732 626-629.
(Anura:
pelobatidae)-.
size
l2l:
Woolbright, L. L., 1989. Sexual dimorphisminEleutherodactylus eoqui: selection pressures and growth rates. Herþetologica 452 68-7 4.
Woolbright, L. L., Greene, E.J. and Rapp, G. C., 1990. Density-dependent mate searchinþ strategies of male woodfrogs. Anitn. Behaa. 40t 155-142.Zuiderwijk, A. and Sparreboom, M., 1986. Territorial behaviour in crested newt Triturus cristahu and marbled newr T. mo.nnorahß (Amphibia, Urodela). Bijdragen tot de Dierkunde 56: 205-213.
