Gobius minutus, in the Ythan Estuary.J Zool 163:177-229. Hoglund J, Kills JA, Fiske P, 1992. The costs of secondary sexual characters in the lekking great snipe ...
Behavioral Ecology Vol. 9 No. 3: 297-300
Energetic constraints on mating performance in the sand goby Kai Lindstrom
Department of Ecology and Systematics, Zoological Laboratory, PO Box 17, University of Helsinki, Helsinki FIN-00014, Finland
A
nimals are generally constrained in their resource allocation patterns due to limited availability of resources (Roff, 1992). These constraints will lead to various trade-offs in reproductive decision making. This is an important assumption of indicator mechanisms of sexual selection (Andersson, 1994). A general constraint on animal activity is food availability and the need to forage. Reproducing individuals have to divide their time between feeding, mating, and parental care, activities that often are mutually exclusive. How much time an individual can devote to mating effort versus feeding depends on its present energetic condition. Individuals in good condition may, due to their higher energy reserves, be able to allocate more time to mating than individuals in poor condition. In studies where individuals have been given supplemental food, mating performance has improved. In the bicolor damselfish, Stegastes partitus, fed males maintained their courtship rate throughout the breeding season, whereas unfed males showed a decline in courtship rate (Knapp, 1995). In a wolf spider, males with high drumming rates are preferred by females, but a high drumming rate is also costly and lowers survival (Kotiaho et al., 1996; Mappes et al., 1996). Drumming rate of the males decreases over the season except in food-supplemented males, who can maintain a constant drumming rate (Mappes et aL, 1996). The purpose of this study was to test if the reproductive success of naturally breeding male sand gobies, Pomatoschistus minutus, is constrained by food availability. I compared the reproductive success of food-supplemented and non-foodsupplemented ("unfed") males in the field. The sand goby is a small marine fish species that breeds on shallow, soft bottoms. It lives only 1 year (Healey, 1971) but has a prolonged breeding season beginning in May and lasting until July—August during which males undertake repeated brood cycles and females spawn repeatedly (Lindstrom K, unpublished data). The male builds a nest under a suitable mussel shell or stone, which he then guards. The eggs of one or more females are laid in a monolayer in the ceiling of the nest. Being confined Received 22 May 1997; first revuion 2 September 1997; second revision 16 October 1997; accepted 14 November 1997. O 1998 International Society for Behavioral Ecology
to the nest will limit the male's opportunities to forage, and, because parental care is energetically costly (Lindstom 1998; Lindstrom and Hellstrdm, 1993), breeding males are likely to be severely food constrained. Because of the prolonged breeding season, sand gobies should experience a trade-off between investing in present reproduction and future reproduction. More intensively courting males are preferred by female sand gobies (Forsgren, 1997), and courtship has often been found to be energetically expensive (see, e.g., Andersson 1994), so it is possible that sand goby males must trade off mating for foraging. Several fish species store energy as nonpolar lipids and use these fat reserves during periods of exceptionally high energy demand or low food availability (Love 1970; Reznick and Braun, 1987). I therefore used the fat reserves of the males to quantify the energy reserves. MATERIALS AND METHODS This study was done during May 1995 at the Klubban Biological Station on the Swedish west coast (58°15' N, 11°28' E). The study site was a shallow bay situated close to the station. The bottom consists of fine sand with a water depth between 50 cm and 1 m. Natural nest sites are readily available, but sand gobies in the area also accept halved flower pots as nest sites. I put out 64 halved clay flower pots (diam 6 cm) at relatively constant water depths (maximum difference about 20 cm). The distance between flower pots was 1.5 m, and they were arranged in four squares of 4X4 pots on areas of clean sand with no vegetation or other objects. Once a nest had been colonized by a male, die male was randomly assigned to be either fed or not during the experimental period. The males in the fed group were offered small, 2 x 2 X 1 mm, pieces of mussel, Mytitus edulis, meat as food. Individual pieces of the food were delivered to the males using a clear plastic tube 35 cm in length. I only gave a male as much food as he would eat but no more than four pieces, and I took great care that no uneaten pieces of food were left in the vicinity of the nest that could attract other fish or egg predators to the nest I checked each nest every day by snorkeling and making notes on waterproof paper. When approaching a male's nest, I recorded whether he was away from the nest, at the nest, or in the nest. If he was in the vicinity of the nest, I recorded his
Downloaded from http://beheco.oxfordjournals.org/ by guest on October 29, 2012
I tested the effect of food addition on reproductive success in male sand gobies, Pomatoschistus minuius, by comparing foodsupplemented males with unfed, control males. The sand goby is a small marine fish with paternal egg care. The males were breeding in artificial nest sites in otherwise natural conditions in the field. I quantified energy reserves by extracting nonpolar lipids. The food supplement unproved the fat reserves of the fed males as compared to unfed males. Fed males spent more time at the nest, whereas unfed males spent a much smaller proportion of their time at the nest. As a consequence, fed males mated sooner than unfed males and tended to get more eggs. In the unfed group, mating speed was correlated to body length so that bigger males mated sooner. The results suggest that the reproductive success of breeding sand goby males is constrained by the availability of energy but that this constraint is most severe for small males and less severe for bigger males. Energy availability through its effect on condition will affect the investment in reproductive effort. Key words: condition dependence, fat reserves, mating success, Pomatoschistus minutus, sand goby, sexual selection. [Behav Ecol 9:297—300 (1998)]
Behavioral Ecology VoL 9 No. 3
298
a)
Table 1 A. comparison of ffco sod unfco m**** Variable
Fed males
Total length (mm) 60.0 ± 6.1 Colonization time (days) 3.1 ± 2 . 8
•
Unfed mala
2.5-
df
59.4 ± 7.2
0.200
18.6 .843
4.4 ± 4.0
0.880
18.9 388
Meant i SD for different variables and the results of t tests comparing the two groups are presented. Colonization time is the time until a male occupied a nest site. For both variables, the sample sizes are 9 and 12 for the fed and unfed males, respectively.
jo o
I
1.5.
E u.
1.0.
I followed the nesting cycle of 21 males. Out of these, 9 males were assigned to the fed group and the remaining 12 to the unfed group. The first males occupied a nest site on the first day after the nest sites were put out in the field. The last nest was colonized on day 9. There was no difference between fed and unfed males in colonization time (Table 1); on average the nest sites were colonized within 5.9 days (SD " 3-5, n ™ 21). Males were on average 59.7 mm (SD - 6.6, n = 21) in length, and there was no difference in length between the males assigned to the two groups (Table 1). To test the effect of treatment on condition, I did a mulnvariaje analysis of variance on fresh weight dry weight and fat weight with body length as a covariate. All weight vaiiaBtw dearly increase with body size, the relationship being weakest for fat weight (Figure 1). The weight measures do, however, increase more steeply with body size for the fed group than for the unfed group (MANOVA, heterogeneity of regressions, multivariate FXK = 11.999, p < .001, Wilk's X - 0.294; uni-
°lcV O
0.0-
b)
07n 0.6
0.50.4-
•o o
0.30.2-
P. ° o ot o 8
0.1. 0.0
C) 0.025,
0.020-
O> 0.015-
3> %
0.010
0.005-
o o»
8 0.000 4 4 4 8 5 2 5 6 6 0 6 4 6 8 7 2 7 6
Total length, mm Figure 1 Male condition measured as weights plotted against male body length, (a) Male fresh weigh, (b) dry weight and (c) fat weight Filled circles represent fed males; open circles represent unfed
Downloaded from http://beheco.oxfordjournals.org/ by guest on October 29, 2012
RESULTS
o
2.0-
0.5-
activity. Males belonging to the manipulation group were fed after the observations. A daily check always consisted of checking the nests three times. The time interval between consecutive checks varied from 15 to 30 min depending on the number of colonized nests. Males were always fed during the first check. However, this applied only if the male was already present on the first visit If he was not, I fed him the first time he was at the nest. I checked the nests for eggs by carefully tilting the flower pot. If new eggs had been deposited in the nest since the previous check, I marked the perimeter of the egg mass on the flower pot using a pencil. Sometimes I found a female in the nest spawning. I then left the nest and returned when spawning was completed to mark the egg mass. By later transferring the egg mass markings onto paper and weighing the piece of paper corresponding to the egg mass, I estimated the size of the brood a male had received. This measure is an unbiased estimate of area, and the area of an egg mass is tightly correlated to the number of eggs (r « .955, p < .001, df = 45). Here the measure is used as an estimate of reproductive success. At the end of the experiment I caught the males using an aquarium fish nee The males were brought to the laboratory, where I recorded their total length and fresh weight They were then killed in ethyl /Kuninobenzoate (benzocaine) and dried for 24 h in 60°C The dry fish were weighed and then homogenized. The homogenized fish were reweighed and nonpoiar lipids were extracted using the Soxhlet method with petroleum ether as the lipid solvent (Knapp, 1995). The fish were kept for 5-4 h in the extractor, where the nonpoiar lipids accumulated in the solvent, which was then allowed to evaporate, and the remaining lipids were weighed.
o
Lindstrdm * Energetic constraints on mating performance
a)
o
•o
•
299
O
8012-
o
60-
•
10-
•
•• o
§
40-
•
o
0-
45
6-
55
O
o o
50
O O
•
o O
8-
o
8
20-
O
60
65
70
O*
•
4-
•
• •
75
2-
*o o •
• O - i
0.12 n 0.10-
variate tests: fresh weight, f, 17 = 8.650, p = .009; dry weight, FU1 = 20.526, p < .001; fat weight, Ful = 10.468, p = .005). Over the range of body sizes in this study, the condition measures for the fed fish lie above those for the unfed fish, especially the amount of body fat (Figure 1). This suggests that food addition improved the energy budgets of the malesSupplemental feeding should decrease the need of a male to search for food outside his territory. Because of the additional food, fed males were in better energetic condition and should have therefore been able to spend more time at the nest courting females and/or caring for the eggs. I used the proportion of visits on which a male was present at his nest as a measure of his residence time. I did this for the time period before the male received eggs, as after a male has mated, his time allocation will also be influenced by parental activities. On average, unfed males were found at their nest on 38.4% (SD « 33.8, n «• 12) of the visits, whereas the corresponding value for fed males was 54.3% (SD » 29.9, n = 9). In the unfed group, larger males spent more time at their nest than smaller males (ANCOVA, proportion of time at the nest with male total length as a covariate, test for homogeneity of slopes, Fui7 - 5.270, p = .035; Figure 2). This difference in time at the nest disappeared after mating, probably due to die need for parental care activities (Mann-Whitney U = 67.5, />•= .092). The time until a male received his first eggs varied between 2 and 13 days, and on average males mated on day 5 (SD = 2.6, n «= 21). Fed males mated sooner (mean day = 3.8, SD = 0.8, n = 9) than unfed males (mean day = 6.0, SD = 3.1, n = 12; t test, t .003, »* = .572). This relationship was absent for the fed males, in which time to mating was independent of body size (b = -0.050, df = 7, p = .332, T2 =» .010; ANCOVA, test for homogeneity of slopes, /", „ = 6.084, p = .025; Figure 3). This relationship indicates that large, unfed males would receive eggs simultaneously widi fed males, but small, unfed males would have to wait longer for eggs. There was also a tendency for fed males to receive more
0.08S?
0.06-
"o (D
.a
0.04. 0.020.00 44
48
52
56
60
64
68
72
76
Total body length, mm Figure S Male reproductive success plotted against male body length, (a) Time until mating and (b) size of egg mass. Filled circles represent fed males; open circles represent unfed
eggs than unfed males during the experiment (ANCOVA on egg area estimate with body length as a covariate; treatment FliS =• 3.505, p = .078), as well as a trend for larger males to receive more eggs (body length Fila = 3.361, p = .083). I excluded die interaction between die covariate and die treatment from this analysis because the slopes were homogeneous (heterogeneity of slopes, Fun < 0.001, ns). DISCUSSION
Fed sand goby males were found more frequently at dieir nests, and reproductive success improved among fed males, suggesting that food availability severely limits the breeding performance of these fish. Although die analysis of condition measures was complicated by the fact that the weight measures increased more steeply widi body size in die fed than in die unfed group, fed fish had higher fat reserves dian unfed fish. This suggests that die food addition benefited die energy budgets of die fed fish. Fed males mated sooner than unfed males. Tune to mating
Downloaded from http://beheco.oxfordjournals.org/ by guest on October 29, 2012
b)
o o
—
Male body length, mm Figure 2 The proportion of time a male spent at his nest before he mated plotted against male body length. Filled circles represent fed males; open circles represent unfed i)aW
O
300
Condition may be strongly influenced by an interaction between the environment and an individual's genes and therefore exposed to several opposing selection pressures (Rowe and Houle, 1996). Thus there should be high genetic variation in condition. The results of this study suggests that a male's mating effort would be under strong directional sexual selection, but they also show that mating effort is strongly condition dependent Condition dependence could maintain high genetic variation in sexually selected traits despite strong directional selection (Rowe and Houle, 1996). I thank EUsabet Forsgren, Anna Karlsson, Lotta Kvarnemo, Nilla Rosenquiit, and Sara dsthrod for help in the field and lab. Bo G. Svensson and Khibban biological station provided excellent facilities to complete this study. The fat extraction was done while I was visiting the University of Kentucky using Craig Sargent's facilities. I thank Craig Sargent and Brian Wisenden for numerous discussions during the preparation of the manuscript. The manuscript was greatly ira-
proved by comments from Janne Kotiaho, Sarah Kraak, and two anonymousreferee*.This study was funded by the Finnish Academy and the University of Helsinki. REFERENCES Abrahams MV, 1993. The trade-off between foraging and courting in male guppies. Anim Behav 45:673-681. Andersson M, 1994. Sexual selection. Princeton, New Jersey: Princeton University Press. Forsgren E, 1997. Mate sampling in a population of sand gobies. Anim Behav 53:267-276. Halliday TR, 1987. Physiological constraints on sexual selection. In; Sexual selection: testing the alternatives (Bradbury JW, Andersson M, eds). New York: John Wiley & Sons; 247-264. Healey MC, 1971. The distribution and abundance of sand gobies Gobius minutus, in the Ythan Estuary.J Zool 163:177-229. Hoglund J, Kills JA, Fiske P, 1992. The costs of secondary sexual characters in the lekking great snipe (GalUnago vudia). Behav Ecol Soriobiol 30:309-315. Karino K, 1995. Male-male competition and female mate choice through courtship display in the territorial damselfish Stegastes nigricans. Ethology 100:126-138. Knapp RA, 1995. Influence of energy reserves on the expression of a secondary sexual trait in male bicolor damselfish, SugasUs partitus. Bull Mar Sci 57:672-681. Knapp RA, Kovach JT, 1991. Courtship as an honest indicator of male parental quality in the bicolor damselfish, Stegaslts partitus. Behav Ecol 2:295-230. Kotiaho J, Alatalo RV, Mappes J, Parri S, 1996. Sexual selection in a wolf spider male drumming activity, body size, and viability. Evolution 50:1977-1981. Lindstrdm K, 1998. Effects of costs and benefits of brood care on filial cannibalism in the sand goby. Behav Ecol Sociobiol 42:101-106. Lindstrom K, HetUtrom M, 1993. Male size and parental care in the sand goby, Pomatoschistus minutus. Ethol Ecol Evol 5:97-106. Love RM, 1970. Chemical biology offishes.New York: Academic Press. Mappes J, Alatalo RV, Kotiaho J, Parri S, 1996. Viability costs of condition-dependent sexual male display in a drumming wolf spider. Proc R Soc Lond B 263:785-789. Nicoletto PF, 1993. Female sexual response to condition-dependent ornamnets in the guppy Potdlia rtticulata. Anim Behav 46:441—450. Reznick D, Braun B, 1987. Fat cycling in the mosquitofish (Gambusia affinis): fat storage as a reproductive adaptation. Oecologia 73:401413. Roff DA, 1992. The evolution of life histories. New York: Chapman & Hall. Rowe L, Houle D, 1996. The lek paradox and the capture of genetic variance by condition dependent traits. Proc R Soc Lond B 263: 1415-1421. Vehrencamp SL, Bradbury JW, Gibson RM, 1989. The energetic cost of display in male sage grouse. Anim Behav 38:885-896.
Downloaded from http://beheco.oxfordjournals.org/ by guest on October 29, 2012
decreased with increasing body size among the unfed males, whereas this relationship was missing for the fed group. There was also a tendency for the fed males to get more eggs than the unfed males. Thus body size seemed to be less important for the mating success of food-supplemented males. This suggests that the additional energy gained through the added food removed an energetic constraint on the mating performance of smaller males. How much energy a male has available for sustaining reproductive activities could be determined by his condition and the food available. Large males had relatively more fat reserves, which they probably could allocate to mating effort. Therefore, their mating success was less affected by the additional feeding than the mating success of smaller males. Courtship has often been found to be energetically expensive (Halliday, 1987; Hdglund et al., 1992; Vehrencamp et aL, 1989) and therefore requires good energy reserves or food intake to be sustained over a longer time period. In the sand goby, only males with adequate fat reserves initiate nest building (Iindstrdm 1998). When guppy males are given a choice between feeding and courting, they always feed before they start courting (Abrahams, 1993). In many species, including the sand goby, females prefer males with a high courtship rate (Forsgren, 1997; Earino, 1995; Nicoletto, 1993), and in some species courtship rate is correlated to male condition (Knapp, 1995; Knapp and Kovach, 1991; Mappes et al., 1996; Nicoletto, 1993). In the present study I observed courtship much too rarely to be able to get a good estimate of a male's courtship rate. Instead, I used a male's time present at the nest as an estimate of his ability to invest in mating. Courting typically takes place in the vicinity of the nest (Forsgren, 1997; Lindstdm K, per. sonal observation). Staying at the nest would greatly impair a male's foraging opportunity, as foraging males travel several meters away from the nest where it is quite likely that they will miss females passing their territory. The need to forage is therefore a major constraint on a male's mating effort. Forsgren (1997) found that in the field male courtship intensity explained female choice in the sand goby and that male courtship intensity was correlated to male size. Courtship intensity also decreased over the breeding season, but even at the end of the season females preferred only males with a high courtship intensity. This suggests that sand goby males may have energetic problems in maintaining their courtship level over a longer time. Food supplementation seemed to remove the need to forage aad therefore allowed the males to spend more time at their nests and also perhaps to maintain a higher courtship intensity. Future studies will have to be conducted to show if courtship rate in the sand goby depends on condition.
Behavioral Ecology Vol. 9 No. 3
