Evolutionary Ecology 16: 399–413, 2002. Ó 2002 Kluwer Academic Publishers. Printed in the Netherlands.
Research article
Life history strategies and habitat templets of tropical butterflies in north-eastern Australia M. F. BRABY Department of Zoology, James Cook University of North Queensland, Townsville, Qld 4111, Australia; Present address: Museum of Comparative Zoology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, USA; and School of Botany and Zoology, The Australian National University, Canberra ACT 0200, Australia (e-mail:
[email protected])
Received 15 August 2001; accepted 3 June 2002 Co-ordinating editor: O. Leimar
Abstract. Three multivoltine species of satyrine butterflies in the genus Mycalesis (Lepidoptera: Nymphalidae) are narrowly sympatric in the wet–dry tropics of north-eastern Australia. They show a range of ecological strategies and adaptations associated with contrasting habitats and varying selective pressures. Two abiotic factors, namely favorability (the reciprocal of seasonal adversity) and predictability (broadly the reciprocal of disturbance), were examined as potential environmental selective forces in shaping their life histories. Comparison of several key life history traits of the ‘wet-season form’ revealed that the life histories of each species corresponded well with their habitat characteristics. M. perseus, which lives in habitats which are less favorable (i.e. adverse) and more unpredictable (i.e. temporary), shows many traits of an r-type strategy: smaller size, faster development, earlier maturation, higher fecundity, smaller egg size, and rapid population increase. By contrast, M. sirius and M. terminus, which live in more favorable and predictable (i.e. permanent) habitats, have many life history attributes and other characteristics in common which link them closer to K-type strategies. The only discrepancy is lower potential reproductive effort of M. perseus, which may be accounted for in terms of an evolutionary trade-off, such as with dispersal or dormancy. Other correlates associated with the M. perseus life history tactic include higher sex-size dimorphism, greater dispersal ability, better tolerance to adverse conditions, stronger phenotypic variation, greater degree of polyandry, and a more flexible breeding strategy. The life history patterns of these species are discussed in the context of evolutionary life history models, particularly the Southwood–Greenslade habitat templet. Key words: habitat templets, Lepidoptera, life history evolution, life history strategies, mating system, Mycalesis, Nymphalidae, r- and K-selection, Satyrinae, tropical ecology
Introduction Organisms exhibit tremendous variety in the way they allocate resources for growth, development, and production of offspring. This lifetime pattern of growth, development and reproduction of a species is referred to as its ‘life history’ (Begon et al., 1990). Ecologists interested in the adaptive significance
400 and evolution of life histories attempt to find pattern in this diversity and examine the factors or selective pressures that might have evolved a particular life history trait or combination of life history traits (Partridge and Harvey, 1988; Dingle, 1990). Indeed, an organism’s life history might be seen ‘as a set of coadapted traits designed by natural selection, to solve particular ecological problems’ (Stearns, 1976, 1977, 1992). A number of models have been developed in an attempt to find general patterns in life histories and to explain trait differences between species in an ecological and evolutionary context (e.g. MacArthur and Wilson, 1967; Pianka, 1970; MacArthur, 1972; Schaffer, 1974; Wilbur et al., 1974; Grime, 1977; Southwood, 1977, 1988; Calow and Sibly, 1983; Begon, 1985; Sibly and Calow, 1985; Caswell, 1989). Essentially the models predict that, under a particular set of selective pressures, specific combinations of traits (tactics) will be favored in a given population, within the physiological and genotypic constraints of the species. One approach of particular interest to field ecologists has been the development of habitat templet models for both plants and animals (Grime, 1977, 1979, 1988; Southwood, 1977, 1988; Whittaker and Goodman, 1979; Hildrew and Townsend, 1987; Kautsky, 1988; Taylor et al., 1990 among others). These models propose that life history traits (such as growth rate, fecundity, longevity etc.) are shaped by various selective forces generated by the habitat (the ‘templet’), the forces mediate their effects through individual fitness, and it is assumed that over evolutionary time fitness is maximized through evolutionary trade-off of traits to produce the optimal life history. The focus has been to identify and define the major selective forces in terms of environmental or habitat characteristics (i.e. abiotic and biotic factors) that may shape the evolution of life histories, and to predict which combinations of traits and trade-offs will evolve under these forces. Southwood (1977), for example, developed a quadrangular templet based on two major abiotic selective forces, ‘resource durational stability’ and ‘favorability’, mainly for predicting strategies for escape in time and space (i.e. diapause and migration, respectively) of insects. Durational stability refers to the length of time a habitat or resource is suitable for breeding in relation to an organism’s generation time; it considers the habitat in terms of its temporal variability or predictability, for example, ephemeral (temporary) vs. more predictable (permanent) resources. Favorability considers the resource level of the habitat, for example, rich vs. harsh environments, and is the inverse of the ‘adversity’ or ‘stress’ selective force recognized by Whittaker (1975) and Grime (1977). Southwood associated r-type and K-type traits under these two forces: r-strategists with temporary resources and K-strategists with permanent resources. Greenslade (1983) modified Southwood’s templet by examining the adversity axis in more detail: he proposed ‘adversity selection’ (A) as a third selection process and predicted certain life history characteristics
401 (A-strategists) for species living in predictably unfavorable habitats. His main life history correlates were long lifespan, late maturity, slow development rate, low fecundity, parthenogenesis, poor dispersal ability, low investment in defense mechanisms, and variable population density; these were contrasted against features of r- and K-strategists. Greenslade recognized that Southwood’s durational stability axis was broadly inversely related to the ‘disturbance’ axis identified earlier by Grime (1977). He also added ‘biotic unpredictability’ as a third vector to incorporate trophic complexity, specialization and density dependent interactions such as competition and predation. This third axis describes the impact of the biotic components of the environment; it is orientated as a diagonal across the templet since community interactions are predicted to increase with both increasing favorability and stability. A number of other templet models have been developed and more recently Southwood (1988) attempted to bring three of these models (i.e. those of Grime, Southwood–Greenslade, Hildrew–Townsend) together by reorienting the axes to show how different investigators were describing similar classifications of habitats. Southwood thus recognized three basic axes, two based on abiotic properties and one on biotic. The two abiotic axes are ‘disturbance’ (broadly the reciprocal of stability and predictability) which incorporates aspects of r/K theory in terms of predicting life history traits, and ‘adversity’ (the equivalent of stress, and the reciprocal of favorability and productivity) which predicts certain traits under A selection. The biotic axis is termed ‘biotic interactions’ and is greatest where both disturbance and adversity are lowest. Although several studies on insect life histories have provided extensive empirical data and tested the utility of some of these models (Solbreck, 1995; Townsend et al., 1997; Statzner et al., 1997; Yanoviak and Kaspari, 2000; Ribera et al., 2001), and there is an extensive literature on butterfly life history characteristics and theory, there appears to be little detailed work that has examined life history strategies of butterflies in the context of habitat templets and environmental selection pressures. Shapiro (1975), in Warren (1992), noted that high intrinsic rate of increase, high dispersal, good colonizing ability, and multivoltinism were usually correlated with disturbed habitats and wide geographical distribution, whereas comparatively low intrinsic rate of increase, low dispersal, poor colonizing ability, and univoltinism tended to be correlated with constant habitats and restricted geographical distribution. This paper compares a number of key life history traits between three butterfly species in the genus Mycalesis Hu¨bner (Lepidoptera: Nymphalidae: Satyrinae) from the Australian wet–dry tropics. Potential selection pressures are proposed to explain life history differences between them, and the patterns of life history variation are compared with contemporary habitat templet models.
402 Materials and methods Study animals Mycalesis is a large Old World genus restricted to the Oriental and Australian Regions where most species occur in the tropical latitudes of the Indo-Australian region. More than 25 species are recorded from mainland New Guinea (Parsons, 1998). In Australia, there are three species which occur in northern part of the continent and which are narrowly sympatric in north-eastern Queensland (Qld). All of these species extend further north and west through mainland New Guinea and its adjacent islands to Maluku in Indonesia, with one (M. perseus) reaching India. They are relatively sedentary insects and form a conspicuous component of the Australian tropical butterfly fauna. Their natural history, distributions, habitat preferences and ecology have been well studied (Braby, 1994a–c, 1995a–d, 1996; Braby and Jones, 1994, 1995; Moore, 1986, 1999). The tropical monsoonal environments in which they live are characterized by a short and unpredictable wet season, when nearly all the years rain falls, followed by a long and equally unpredictable dry season when very little rain falls. The three species show a range of ecological strategies and adaptations to survive the relatively harsh dry season, briefly summarized below. M. perseus (Fabricius, 1775) has the broadest distribution in north-eastern Australia and is by far the commonest of the three species. It is especially abundant in lowland savannah woodland and eucalypt open-forest with a grassy understorey; it is scarce in habitats with a closed canopy such as rainforest. Females oviposit and larvae feed on a wide range of grasses, with Themeda triandra being frequently used. The breeding season lasts only a few months, coinciding with the wet season which varies greatly from year to year in terms of the timing, amount and duration of rainfall. During the long dry season when larval food quality declines adults retreat to and aggregate in moist refugia, such as along dry creek beds and river banks, and females stop breeding and enter reproductive diapause. Following the first substantial prewet season rains and abundant new growth of larval food plants, females move out of refugia, start breeding and populations increase rapidly. During this period several generations are completed and there is considerable local dispersal and range expansion, taking advantage of the seasonally favorable conditions. M. sirius (Fabricius, 1775) has the narrowest distribution of the three species in Qld and populations are very patchy, being restricted largely to higher rainfall areas in lowland coastal paperbark (Melaleuca) woodland and swampland where its primary larval food plant Ischaemum australe and other grasses grow. It also occurs irregularly in the adjacent eucalypt open-forests,
403 especially after good wet years when populations are higher. In contrast to M. perseus, females breed for much of the year but egg production declines as the dry season progresses and may cease late in the season. Populations are most abundant during the early and mid dry season (i.e. after the wet season) but decline towards the late dry season and tend to contract to the swamplands where the habitat is more favorable for breeding. The dry season aggregation behavior is less well defined than in the two other species but late in the season adults may be found in moist refugia. M. terminus (Fabricius, 1775) is distributed widely in the moist coastal lowlands of Qld where it occurs in many different habitats. Its preferred habitat is rainforest edge and it is particularly abundant in the damper shaded areas along the forest margins or along creeks and rivers of gallery forest where the main larval food plant Oplismenus and other grasses grow. It also extends into wet upland areas, and occurs in eucalypt open-forest, especially with rainforest elements in the understorey, and along moist riparian habitats within the drier savannah where conditions are in general more favorable for breeding. Like M. sirius, females breed for much of the year, but egg production declines as the dry season progresses and may cease late in the season depending upon the severity of local conditions. Populations are most abundant in the early and mid dry season following the abundant new growth of the larval food plants (i.e. after the wet season). During the late dry season populations contract to moist refugia, particularly along dry creek beds supporting gallery forest. Like M. perseus, they do not migrate but there is considerable local dispersal during and immediately after the wet season. The three species thus show an array of reproductive strategies, breeding patterns and other characteristics associated with contrasting habitats and different selective pressures. Some of these population and behavioral characteristics are summarized in Table 1. All three species show the capacity to arrest reproductive activity during adverse conditions, but this is most pronounced in M. perseus. Reproductive arrest (which may or may not be a true diapause) in Mycalesis probably represents the primary survival strategy during the dry season and is believed to be an adaptation to minimize poor larval success when larval food plant quality is low. Other distinguishing dry season attributes that may enhance fitness, include pronounced egg size variability (larger eggs are produced during the dry season), larval polyphenism (M. perseus only), pupal polyphenism (pupae are brown rather than green during the winter dry season), adult seasonal polyphenism (adults have a distinctive ‘dry-season form’, especially M. perseus and M. terminus), and adult size variation (adults are generally larger during the dry season, especially M. perseus and M. terminus). The species thus serve a good model system to examine how potential environmental selective forces may have shaped their life histories.
404 Table 1. Summary of population, behavioral, habitat and life history attributes for the three Mycalesis species Attribute Population and behavioral characteristics Spatial distribution Dispersal ability (adult movement during favorable period) Rate of population increase (during favorable period) Reproductive strategy Breeding season Dormancy (length of reproductive diapause during unfavorable period) Tolerance to adversity (egg survival in relation to temperature variation) Habitat characteristics Favorability Predictability
M. perseus
M. sirius
M. terminus
Broad High
Narrow Medium–low
Medium Medium
High
Low
Medium
Opportunistic Continuous– seasonal Short Long Long Short
Continuous– seasonal Long Short
High
Low
Medium
Low Low
Medium Medium
Medium Medium
Life history characteristics (wet-season form) High Medium Low Sex-size dimorphisma (ratio of pupal weight, f:m) (1.20) (1.14) (1.05) Body sizea (mean pupal weight (mg), reared Small Medium Large on Panicum at 25 °C and 12:12 L:D cycle) (m 184; f 222) (m 201; f 230) (m 221; f 233) Developmental ratea (mean s.e. egg High Medium Low physiological time (degree days)) (63.3 3.1) (71.9 4.3) (79.4 5.8) Time to maturitya (mean total development Short Medium Long time (days) from egg to adult, reared on (m 40.4; f 43.1) (m 44.9; f 47.6) (m 47.3; f 50.4) Panicum at 25 °C and 12:12 L:D cycle) Egg sizeb (mean sd egg weight (mg) Small Large Large of females fed on rotting fruit) (0.46 0.06) (0.66 0.09) (0.68 0.06) Realized fecundity b (mean sd number High Low Low of eggs laid by females fed on rotting fruit) (164 62) (110 46) (110 49) Reproductive output b (mean sd product Same Same Same of egg weight (mg) and realized fecundity (i.e. (77.3 34.9) (71.8 28.2) (75.3 36.4) total egg mass) for females fed on rotting fruit) Potential reproductive effort b (mean sd Small Medium Large product of egg weight and potential (0.48 0.13) (0.58 0.09) (0.73 0.15) fecundity divided by pupal weight for females fed on rotting fruit) Degree of polyandry c (mean sd High Medium Small number of spermatophores per female) (2.00 0.714) (1.82 0.751) (1.41 0.520) a
Data from Braby and Jones (1994). Data from Braby and Jones (1995). c See Table 2 for data and analysis. b
405 Life history traits Life history and habitat data of the three Mycalesis species were derived from previous published work (see Braby, 1994a–c, 1995a–d, 1996; Braby and Jones, 1994, 1995) based primarily on field and laboratory studies of populations at three coastal lowland sites (Cardwell, Rollingstone, Townsville) in northeastern Qld. The following studies, in particular, provide detailed comparative information on: their habitat characteristics, together with seasonal changes in relative abundance and the spatial distribution of adult populations (Braby, 1995a); aspects of their mating system (Braby, 1995b; 1996); their developmental biology, particularly the influence of temperature and larval food plants on developmental rate, survival and body size (Braby and Jones, 1994); and their reproductive patterns and resource allocation, including fecundity, longevity, egg size and reproductive effort in relation to phenotype and adult diet (Braby and Jones, 1995). Patterns of egg size variation, particularly its adaptive significance in relation to larval food plant quality, is discussed in more detail in Braby (1994a). As noted above there is considerable temporal (seasonal) variation in some of these life history traits (especially body size, egg size and fecundity) which are correlated with complex phenotypic shifts in adult form. That is, ‘wetseason forms’ are, in general, smaller and produce smaller and more eggs compared with ‘dry-season forms’, and Braby and Jones (1995) have demonstrated that reproductive diapause in the ‘dry-season form’ of M. perseus represents a substantial cost to reproduction. Therefore, in order to make meaningful comparisons of life history traits between the three species it is crucial that the phenotypic form be standardized. In this study all life history characteristics are compared between the ‘wet-season form’, which is the more reproductively active phenotype. Mating system The mating system employed is another kind of life history trait. Females of the three species are polyandrous (Braby, 1996) but in order to compare the extent of polyandry the effects of relative age and season need to be considered. Mating frequency, as revealed by spermatophore counts, in Mycalesis varies significantly with wing-wear category (as a subjective estimate of age-class), being highest in ‘older’ individuals and lowest in ‘younger’ females (Braby, 1996). More importantly, significant differences in spermatophore counts between the species hold only in the older age-class and do not persist among the younger age-classes. Mating frequency also varies seasonally, particularly in M. perseus in which diapausing non-reproductive ‘dry-season form’ females in the dry season tend to contain only one spermatophore, whereas breeding ‘wet-
406 season forms’ frequently mate twice or more than twice (Braby, 1995b). The data was therefore reanalyzed taking into account the variables of ‘relative age’ and ‘season’: these were controlled by reducing the dataset to include only those females that were ‘older’ (i.e. having wing-wear categories of ‘worn’ (margins of two or more wings chipped, 6–25% scales missing) and ‘very worn’ (margins of all wings very chipped, >25% scales missing)), and that were collected from January to May or June, that is, the months when the ‘wetseason form’ of the three species was present at Cardwell in 1989 and 1990 (Braby, 1994c).
Results and discussion The Southwood–Greenslade templet identifies two abiotic axes or selective forces: habitat favorability and habitat predictability (see Southwood, 1988 for review). Favorability is the inverse of adversity, and in the wet–dry tropics of northern Australia the major form of adversity for many phytophagous insects is the dry season when larval resources either disappear or decline in quality (Jones, 1987). All three Mycalesis spp. face this seasonal problem of resource deficiency, but M. perseus generally occurs in habitats which are somewhat drier and harsher (in terms of lower grass moisture content) than those favored by M. sirius and M. terminus, especially during the dry season (Braby, 1995a, c). Predictability refers to the temporal availability of food resources as a function of the generation time of a species. Larval food plants (grasses) are the most important food resource to Mycalesis (Moore, 1986; Braby and Jones, 1994; Braby, 1995d), and their availability is regulated by rainfall. Because rainfall in the Australian wet–dry tropics is highly unpredictable in timing and in extent (see Jones, 1987; Braby, 1995a) it follows that the larval foods favored by satyrines are also largely unpredictable, at least in the time frame of a single season. However, evidence collected on habitat distribution and breeding phenology (Braby, 1995a–c) suggests that M. sirius and M. terminus, which have a longer breeding season, live in moister and more predictable environments where larval resources are in general more persistent and buffered from climatic extremes. By contrast, M. perseus lives in habitats where larval resources are more temporary and unpredictable: it has a shorter breeding season, remaining reproductively dormant throughout much of the dry season, and breeds only during the rain periods when conditions are ephemerally favorable. These differences in habitat characteristics between the Mycalesis species are summarized in Table 1. Key life history characteristics, including sex-size dimorphism, body size, developmental rate, time to maturity, egg size, realized fecundity, reproductive output and potential reproductive effort, are also summarized in Table 1. For
407 Table 2. Degree of polyandry of ‘older’ females of the ‘wet-season form’ of the three species of Mycalesis Number of spermatophores
M. perseus
M. sirius
M. terminus
n
(%)
n
(%)
n
(%)
1 2 3 4
11 31 7 2
(21.6) (60.8) (13.7) (3.9)
27 32 12 1
(37.5) (44.4) (16.7) (1.4)
42 26 1 0
(60.9) (37.7) (1.4)
Total Mean sd
51 2.00 0.714
72 1.82 0.751
69 1.41 0.520
Polyandry is the mating frequency, determined by the mean number of spermatophores per female. ‘Older’ females are those having wing-wear categories of ‘worn’ (margins of two or more wings chipped, 6–25% scales missing) and ‘very worn’ (margins of all wings very chipped, >25% scales missing). ‘Wet-season forms’ are those individuals which were sampled from January to May or June 1989–1990 at Cardwell, Qld. The extent of polyandry is significantly different between the three species (v2 ¼26.28, df=6, p
