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Effects of competitor-to-resource ratio on aggression and size variation within groups of convict cichlids
ANIMAL BEHAVIOUR, 2005, 69, 1157–1163 doi:10.1016/j.anbehav.2004.07.019
Effects of competitor-to-resource ratio on aggression and size variation within groups of convict cichlids MICHELLE V. NOE¨ L, J AM ES W. A. G RA NT & JOS EPH G . CA RRI GA N
Department of Biology, Concordia University (Received 17 December 2003; initial acceptance 6 June 2004; final acceptance 27 July 2004; published online 24 February 2005; MS. number: A9774R)
Resource defence theory predicts that the intensity of competitive aggression, degree of resource monopolization, and variation in fitness will be highest at intermediate levels of the spatial clumping of resources. We tested for this predicted dome-shaped relationship by manipulating the spatial clumping of food via competitor-to-resource ratio (CRR), the number of potential competitors divided by the number of resource units. Groups of 10 convict cichlids, Archocentrus nigrofasciatus, were allowed to compete for a fixed amount of food in one of five CRR treatments (1, 1.43, 2, 5 and 10), created by varying the number of patches in which the food appeared (i.e. 10, 7, 5, 2 and 1 patch, respectively). As predicted, both the frequency of aggression and the coefficient of variation of body mass (a measure of the consequences of food monopolization and variation in a component of fitness within groups) increased significantly as CRR increased from 1 to 2, and then decreased significantly at CRRs of 5 and 10. In addition, mean growth rate decreased in groups with high rates of aggression, suggesting an important cost of aggression. Our study provides the first quantitative support for the predicted dome-shaped relationship and suggests that CRR is a useful measure of the degree of spatial clumping of resources. Ó 2005 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
The dispersion of resources in space and time is thought to affect how animals compete and the resulting distribution of those resources among the competitors (Brown 1964; Emlen & Oring 1977; Grant 1993). Of all the components of resource dispersion (see Warner 1980; Grant 1993), spatial clumping or patchiness has probably attracted the most attention in both theory and experiments. According to the theories of resource defence and mating systems, resources are more economically defensible and monopolizable as they become increasingly clumped in space (Emlen & Oring 1977; Grant 1993). At a local scale, an increase in the spatial clumping of a resource allows an individual to occupy a smaller home range or a smaller patch of resources, both of which will be easier to defend against intruders (Hixon 1980; Grant et al. 1992; Grant 1993). Many studies have now verified this prediction by showing an increase in aggression (Zahavi 1971; Rohwer & Ewald 1981; Robb & Grant 1998; Johnson et al. 2004), monopolization of food (Theimer 1987), or both (Magnuson 1962; Monaghan & Metcalfe 1985; Grant & Guha 1993; Ryer & Olla 1995; Kim et al. 2004) as a fixed amount of food is increasingly concentrated into a smaller patch. Correspondence: J. W. A. Grant, Department of Biology, Concordia University, 7141 Sherbrooke Street West, Montre´al, QC H4B 1R6, Canada (email: [email protected]). 0003–3472/04/$30.00/0
Similarly, male dunnocks, Prunella modularis, defend and monopolize females more easily when females occupy smaller home ranges in response to the addition of dense patches of food (Davies & Lundberg 1984). Few studies, however, have shown that short-term measures of monopolization translate to fitness differences among competitors (but see Blanckenhorn 1991; Bryant & Grant 1995). At a larger spatial scale, extremely clumped resources may attract many competitors from a great distance, making defence uneconomical (Carpenter 1987). In addition, extremely clumped resources may be locally superabundant and not worth defending (e.g. Grant et al. 2002). Hence, the defence and monopolization of resources are predicted to peak at intermediate levels of spatial clumping, when measured over a broad range of values (Carpenter 1987). However, we are unaware of any clear demonstration of such a dome-shaped relationship, perhaps because of the difficulty of measuring or manipulating resource dispersion over a broad range, particularly in the wild (Davies 1991). Operational sex ratio (OSR), the number of potentially mating males divided by the number of fertilizable females in a population at a time, was originally developed as an empirical predictor of the intensity of intrasexual competition and sexual selection (Emlen & Oring 1977). OSR is easier to measure than resource dispersion, and
1157 Ó 2005 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
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integrates how members of a breeding population map onto the dispersion of resources, mates, or predators in the wild (Emlen & Oring 1977). Competitor-to-resource ratio (CRR), the number of potential competitors divided by the number of resource units in a population at a time, is a general formulation of OSR that potentially applies to any resource, including both food and mates (Grant et al. 2000). Like OSR, CRR scales the abundance of competitors to resources and provides a quantitative measure of resource clumping in both space and time. The utility of CRR has been tested only once, where it was used to quantify the synchrony in arrival of food and mates and to predict the frequency of competitive aggression. Grant et al. (2000) demonstrated a dome-shaped relationship between the frequency of aggression and CRR, when the latter was used to quantify the clumping of food and mates in time. However, CRR has not yet been used to quantify the spatial clumping of resources or to predict the outcome of competition. In this paper, we extend the use of CRR in two important ways. First, we use CRR to quantify, for the first time, the spatial clumping of resources, rather than the temporal clumping of resources. CRR will only be a useful predictor of the intensity of competition across patches in space if individuals settle in direct proportion to the abundance of resources in those patches (i.e. an ideal free distribution; Fretwell & Lucas 1970). Then, the average number of competitors at a given patch will be equal to the overall CRR in a habitat or experimental treatment (see Grant et al. 2000). Second, we use CRR to predict the frequency of aggression and, for the first time, the consequences of resource monopolization within groups. We use size variation within groups of fish to estimate both the outcome of feeding competition and, because size is likely to be an important component of fitness, the variance in fitness. We assume that growth rate will be an important component of fitness in our species, because larger males monopolize breeding sites and mate with larger, more fecund females (Keenleyside 1985; Nuttall & Keenleyside 1993; Wisenden 1995). Specifically, we first tested the assumption that the average number of competitors at a given patch increases in direct proportion to CRR. We then tested the predictions of a dome-shaped relationship between the frequency of aggression versus CRR, and the degree of size variation within groups versus CRR.
METHODS
Experimental Subjects We chose juvenile convict cichlids as test subjects because they grow quickly and readily defend food patches in laboratory conditions (Grant & Guha 1993; Praw & Grant 1999). In the wild, adult convict cichlids are aggressive when defending offspring and nest sites, but neither adults nor juveniles have been observed to defend food resources (Wisenden 1995). Food defence in the laboratory occurs presumably because food is distributed in an economically defensible manner, unlike in the wild.
All fish in our experiment were taken from two broods (i.e. two separate pairs of adults) from our laboratory stock population. Fish from different broods were held in separate stock tanks (L ! W ! H: 90 ! 46 ! 38 cm) filled with dechlorinated tap water, maintained at 26–28 C on a 12:12 h light: dark cycle (lights on at 0700 hours). Both holding tanks were equipped with a 100-W submersible heater, a box filter, an under-gravel filter covered with coarse gravel to a depth of 3 cm, and an air stone attached to an air tube. We fed fish in stock tanks twice a day ad libitum with either commercial flake food, frozen brine shrimp (Artemia sp.) or ‘Fry Feed Kyowa’ pellets (BioKyowa, Cape Girardeau, Missouri, U.S.A). We established 25 groups of 10 fish per experimental tank, for a total of 250 fish, by choosing individuals from a single stock tank (i.e. brood) to minimize the initial size variation within groups. The two broods were evenly distributed across all treatments. We used immature fish to minimize mating behaviour and behavioural differences between the sexes. On average, fish weighed 0.587 g (range 0.309–0.904 g, N Z 250) at the beginning of trials with an initial coefficient of variation (CV, SD/mean) of body mass within groups of 0.138 (range 0.03–0.27, N Z 25).
Experimental Procedure We monitored the aggressive behaviour and size variation within the groups of 10 convict cichlids fed a constant ration, for their body size, in response to CRR. We created five levels of CRR by varying the number of food patches in which this fixed ration of food was made available for the 10 fish in each experimental aquarium (L ! W ! H: 60 ! 30 ! 35 cm). The five levels of CRR were: 10 (one patch), 5 (two patches), 2 (five patches), 1.43 (seven patches) and 1 (10 patches). Each treatment was replicated five times. A patch consisted of a single ‘cell’ cut from a standard blue ice cube tray (L ! W ! H: 5.3 ! 3.9 ! 3.0 cm). We introduced food patches twice a day for 15 min. We chose permanent patch locations and feeding times (3 h apart) to control for resource predictability in time and space. For a CRR of 10, the single patch was positioned in the centre of the tank (Fig. 1). For all other treatments, the patches were distributed evenly over the tank to maximize the distance between adjacent patches (Fig. 1). The experimental tanks were similar to stock tanks, except the experimental tanks lacked box filters, and the entire bottom of each experimental aquarium was lined with a series of yellow ice cube trays filled with sand to provide a platform into which patches were inserted. The blue feeding patches were extremely obvious against the yellow background and were readily discovered by the test fish. We also covered three sides of the tanks with white paper to minimize external disturbance. Because the 25 groups of fish were not identical in body size, the daily ration of food was adjusted to the total body mass of the group. The quantity of food, ‘Fry Feed Kyowa’ (proximate composition: crude protein not less than 55%, crude fat not less than 10%, crude fibre not more than 4%
NOE¨ L ET AL.: AGGRESSION AND SIZE VARIATION
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Figure 1. Top view of experimental tanks (L ! W: 60 ! 30 cm) showing the location of food patches (dark squares) in the five competitor-to-resource ratio (CRR) treatments.
and crude ash not more than 17%), given to each group twice daily was based on the amount of food that a 0.9-g fish could eat in 1 min (0.062 g or 38 pellets; Grant et al. 2002). We used the average weight of a group to calculate the twice-daily ration, and then distributed the required pellets equally among the patches of the trial. The average daily ration for 10 fish was 496 pellets of 500 mm in diameter (i.e. 0.587 g/0.9 g ! 10 fish ! 2 times a day ! 38 pellets Z 496 pellets). If metabolic rate and meal size scale as M0.75, then our method of calculating ration size may not be strictly allometrically correct (but see Grant et al. 2002). Hence, we tested for the effect of body size when examining growth rate. In summary, the amount of food that each group received was adjusted for the total body mass of the group. Hereafter, we call this the full daily ration. To prevent patches from floating, a glass marble was attached to the bottom of each patch (i.e. cell). Each patch was also covered with another ice cube cell to keep food in the patch when first placed into the water. We then fitted
the covered patches into the correct location and removed covers simultaneously. The food was mixed with 10 ml of sand in each feeding patch to increase the foraging time. Prior to each feeding, we turned off the air supply to signal that food was about to arrive. Trials lasted for a total of 15 days. On the first day we weighed fish prior to feeding and transferred them to experimental tanks. Fish were fed half-rations (i.e. ½ of the full daily ration) for the first 2 days to minimize growth while they were still learning how to feed in their new environment. We gave full rations from day 3 to day 8 and increased rations to 150% of the full daily ration from day 9 to day 14 to accommodate growth. Because fish behaviour typically stabilizes after a week of training, we videotaped the first daily feeding on day 9 and day 14 of the trial for a period of 10 min. Fish were weighed on day 15, 24 h after their last feeding, and were then moved to a ‘used fish’ tank.
Data Analysis Behaviour of interest was scored from the video recordings. As in previous experiments with groups of convict cichlids, almost all aggressive interactions were chases, unidirectional bursts of increased swimming directed towards another individual (e.g. Grant & Guha 1993; Praw & Grant 1999). We counted the total number of chases by all individuals in each tank when fish were actively foraging (i.e. food was present). This foraging period varied between treatments and ended when fish ceased active foraging and primarily hovered over the patches. We confirmed this assumption during training by removing patches to determine whether any pellets remained. The average foraging period for CRR levels of 1, 1.43, 2, 5 and 10 were approximately 1.0, 1.5, 2.0, 2.5 and 2.5 min, respectively. We also evaluated the effects of varying CRR on aggression for a constant time period across all trials by counting the total chases within the first 5 min after removal of patch covers. We averaged the data obtained on day 9 and day 14 and used a one-way ANOVA to test for the effect of CRR on rates of aggression. We present only the data for aggression during the foraging periods, because the patterns of aggression were virtually identical when we used the behaviour during the first 5 min. To estimate the actual CRR of each trial, we counted the number of fish within one body length of each patch during 10 scan samples that were evenly spaced over the foraging period. We estimated size variation within groups by calculating the final CV of body mass. We used the initial CV of mass as a covariate in an ANCOVA when investigating the effects of CRR on final CV of mass within groups. Mean growth was calculated by subtracting the initial mean weight of fish from the final mean weight of fish in each group. To meet the assumptions of parametric tests, we log10 transformed the number of fish per patch. RESULTS If fish distribute themselves equally among patches, as predicted by an ideal free distribution (Fretwell & Lucas
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20 10 5
2 1 0.5
1
2
5
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CRR Figure 2. The mean (GSE, N Z 5) number of convict cichlids within one body length of a given food patch in relation to competitor-toresource ratio (CRR). The dashed line is the expected number of fish per patch assuming an ideal free distribution (i.e. one-to-one line), whereas the dotted line is the expected number of fish per patch assuming an ideal free distribution of the fish within one body length of patches. Note that both axes are plotted on a logarithmic axis, and SE bars are often obscured by the symbols depicting the mean.
20
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(b) 0.35 CV of body mass
1970), then the average number of fish per patch should increase in direct proportion to CRR (Fig. 2). Consistent with this assumption, the average number of fish within one body length of a given patch increased with increasing CRR (ANOVA: F4,20 Z 262.3, P ! 0.0001; Fig. 2). However, more fish than expected (i.e. the one-to-one line was below the 95% confidence limit) were observed per patch, assuming an ideal free distribution (sensu Fretwell & Lucas 1970), at CRRs of 1 and 1.43, whereas fewer fish than expected (i.e. the one-to-one line was above the 95% confidence limit) were observed per patch at higher CRRs. If we consider only those fish within one body length of a patch, then the fish were distributed between patches as expected based on an ideal free distribution (i.e. dotted line, Fig. 2) for CRRs of 2, 5 and 10, but even more fish than expected were observed at patches for CRRs of 1 and 1.43 (Fig. 2). The rate of aggression was affected by CRR, whether measured only when food was present (ANOVA: F4,20 Z 26.21, P ! 0.0001; Fig. 3a), or during the first 5 min of each trial (not shown; F4,20 Z 21.49, P ! 0.0001). As predicted, rate of aggression followed a dome-shaped curve; aggression was low at a CRR of 1, increased and peaked at a CRR of 2 (Fisher’s LSD post hoc test: P Z 0.0013), and then decreased to its lowest level at a CRR of 10 (Fisher’s LSD post hoc test: P ! 0.0001). The initial CV of mass, on average 0.138, did not differ significantly between treatments (ANOVA: F4,20 Z 0.154, P Z 0.96). CV of body mass within groups increased over the experiment in all 25 trials (paired t test: t24 Z 11.48, P ! 0.0001). The final CV of mass (mean Z 0.276) was positively related to the initial CV of mass (ANCOVA: F1,19 Z 20.98, P Z 0.0002). After statistically controlling for the effect of initial CV of body mass, CRR had a significant effect on the final CV of body mass (ANCOVA: F4,19 Z 4.05, P Z 0.015; Fig. 3b). As predicted, final
Fish per patch
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CRR Figure 3. The mean (GSE, N Z 5) (a) rate of aggression of 10 convict cichlids and (b) final coefficient of variation (CV, SD/mean) in body mass within groups of 10 convict cichlids, in relation to competitor-to-resource ratio (CRR). Note CRR is plotted on a logarithmic scale.
CV also followed a dome-shaped relationship; it was low at a CRR of 1, increased and was highest at a CRR of 2 (Fisher’s LSD post hoc test: P Z 0.012), then decreased at CRRs of 5 (Fisher’s LSD post hoc test: P Z 0.0088) and 10 (Fisher’s LSD post hoc test: P Z 0.028). The initial mass of fish did not differ significantly between treatments (F4,20 Z 0.84, P Z 0.49). On average, fish grew in all 25 trials (paired t test: t24 Z 22.11, P ! 0.0001). If aggression is energetically costly, we might expect growth rate to be lower in tanks with higher rates of aggression. The mean growth rate of all 10 fish in a tank was not affected by CRR (ANOVA: F4,20 Z 2.51, P Z 0.074), but was negatively correlated with the aggression rate when food was present (Pearson’s correlation: r23 Z ÿ0.521, P Z 0.0075) and the aggression rate during the first 5 min of each trial (r23 Z ÿ0.558, P Z 0.0037; Fig. 4). Mean growth rate was not significantly related to the initial size of fish in each tank (r23 Z ÿ0.01, P Z 0.96). DISCUSSION The distribution of fish across patches was similar to what was expected based on an ideal free distribution. Not
NOE¨ L ET AL.: AGGRESSION AND SIZE VARIATION
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Growth rate (g)
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Figure 4. Mean (GSE, N Z 5) gain in mass of convict cichlids over 15 days in relation to the total rate of aggression during the first 5 min after food patches were added.
surprisingly, some fish were more than one body length from any patch during the scan samples. Some of these individuals were probably moving between patches, whereas others were excluded from patches by aggressive behaviour. The higher than expected number of fish per patch at CRRs of 1 and 1.43, when patches were close together, was probably caused by some dominant fish attempting to defend more than one patch at a time. In addition, subordinate fish may have been reluctant to be alone on a patch for antipredator reasons, as is often observed in birds (e.g. Beauchamp 1998; Johnson et al. 2004). Our experiment provided strong support for the predicted dome-shaped relationship between the frequency of competitive aggression and the spatial clumping of food, as quantified by CRR. Aggression was initially low at a CRR of 1, presumably because of a low encounter rate between the 10 fish that were dispersed among the 10 food patches. As CRR increased to 2, aggression also increased as fish more frequently encountered another individual at a patch. However, the decrease in aggression at CRRs of 5 and 10 occurred despite more potential encounters with competitors, indicating that defence of the patch was no longer feasible. Convict cichlids competing for food showed a peak in aggression at a CRR of 2, just like Japanese medaka, Oryzias latipes, competing for both food and mates (Grant et al. 2000). A CRR of 2 is of particular interest because it has been well described by animal contest theory (e.g. Parker 1984). The hawk–dove model predicts that a hawk strategy will be evolutionarily stable at a CRR of 2, if the benefit of the resource is greater than the cost of injury (Parker 1984). While aggression is expected at a CRR of 2, the actual value of CRR where aggression is most intense or frequent will probably depend on the value of the resource and the variability among individuals in competitive ability (see Dubois et al. 2003). As predicted by resource defence theory, variation in a component of fitness within groups, as measured by CV of body mass, also peaked at an intermediate level of CRR.
We assume that the increased variability in growth rate at intermediate levels of CRR was primarily due to an uneven distribution of food amongst competitors when food was economically defensible. Support for this assumption comes from our previous work showing a positive relationship between amount of aggression and the degree of food monopolization within groups (e.g. Grant & Guha 1993; Bryant & Grant 1995). In addition, the amount of food eaten is typically the best predictor of growth rate in a competitive social environment (e.g. Bryant & Grant 1995; Praw & Grant 1999). It is possible that part of the effect of CRR on size variation in our study was caused by the social stress that dominants impose on subordinates (e.g. Abbott & Dill 1989; Praw & Grant 1999). Dominant fish typically grow faster than subordinates, independent of the amount of food eaten (Abbott & Dill 1989; Dou et al. 2004). Because social stress and food monopolization both probably increase with increasing levels of aggression, both mechanisms could potentially explain growth rate variation in groups of fish at intermediate levels of CRR. In our study, however, rate of aggression explained no additional variation in the final CV of body size, after the effects of initial CV of body size and CRR were first entered in the model (ANCOVA: effect of aggression during the feeding period: F1,18 Z 0.32, P Z 0.58; effect of aggression during the first 5 min: F1,18 Z 0.56, P Z 0.46). Hence, a parsimonious interpretation of our results suggests that CRR affects aggression, which affects the monopolization of food, which affects size variation within groups. Nevertheless, the social stress hypothesis is an interesting alternative mechanism that deserves further study. Hence, CRR may affect growth rate, an important component of fitness for fish, via two different mechanisms, which are both related to aggressive behaviour. The decline in size variation within groups at high levels of CRR may initially seem at odds with the common observation of increasing size variation within cohorts with increasing population density (qomnicki 1988). In our experiment, however, the per capita food abundance was held constant, whereas it probably decreases as population density increases in the wild. The decline in CV of body size at high levels of CRR may also have implications for mating systems theory, where it is often assumed that the intensity of aggression and sexual selection will continue to increase with ever-increasing levels of OSR (e.g. Michener & McLean 1998; but see Emlen & Oring 1977). If the intensity of sexual selection is primarily driven by the intensity of male interference competition, then resource defence theory predicts a decline in sexual selection at extremely high levels of OSR. Female choice for attractive males, however, could cause the intensity of sexual selection to increase with increasing OSR, even as the intensity of male–male aggression decreases. The decrease in average growth rate in tanks with high levels of aggression suggests that aggression has an important energetic cost. We assume the rates of aggression that were observed for only 5 min per day were not sufficient to generate the growth differences depicted in Fig. 4. It is possible that the differences in aggression across CRR
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treatments persist for much of the day, albeit at a reduced level, because aggression decreases outside of the foraging period (Robb 1996). In addition to the direct energetic costs of aggression, the lower growth may also have been related to the elevated stress levels of both dominant (e.g. Praw & Grant 1999) and subordinate (e.g. Abbott & Dill 1989) fish in tanks with high levels of aggression. Taken together, our results suggest that high levels of CRR will minimize the rate of competitive aggression and growth rate variation within groups, and will maximize average growth rate. Because these are also the goals of the aquaculture industry (e.g. Noakes & Grant 1992), CRR may be a useful tool for both pure and applied behavioural ecologists. Acknowledgments We thank Cindy Breau for help in the laboratory and Stefan Steingrı´msson, Diana Hews and two anonymous referees for comments on the manuscript. This research was financially supported by a Discovery Grant from the Natural Sciences and Engineering Research Council of Canada to J.W.A.G. References Abbott, J. C. & Dill, L. M. 1989. The relative growth rate of dominant and subordinate juvenile steelhead trout (Salmo gairdneri) fed equal rations. Behaviour, 108, 104–113. Beauchamp, G. 1998. The effect of group size on mean food intake rate in birds. Biological Reviews, 73, 449–472. Blanckenhorn, W. U. 1991. Fitness consequences of foraging success in water striders (Gerris remigis; Heteroptera: Gerridae). Behavioral Ecology, 2, 46–55. Brown, J. L. 1964. The evolution of diversity in avian territorial systems. Wilson Bulletin, 76, 160–169. Bryant, M. J. & Grant, J. W. A. 1995. Resource defence, monopolization and variation of fitness in groups of female Japanese medaka depend on the synchrony of food arrival. Animal Behaviour, 49, 1469–1479. Carpenter, F. L. 1987. Food abundance and territoriality: to defend or not to defend? American Zoologist, 27, 387–399. Davies, N. B. 1991. Mating systems. In: Behavioural Ecology (Ed. by J. R. Krebs & N. B. Davies), pp. 263–294. Oxford: Blackwell Scientific. Davies, N. B. & Lundberg, A. 1984. Food distribution and a variable mating system in the dunnocks, Prunella modularis. Journal of Animal Ecology, 53, 895–912. Dou, S. Z., Masuda, R., Tanaka, M. & Tsukamoto, K. 2004. Size hierarchies affecting the social interactions and growth of juvenile Japanese flounder, Paralichthys olivaceus. Aquaculture, 233, 237–249. Dubois, F., Giraldeau, L.-A. & Grant, J. W. A. 2003. Resource defense in a group-foraging context. Behavioral Ecology, 14, 2–9. Emlen, S. T. & Oring, L. W. 1977. Ecology, sexual selection, and the evolution of mating systems. Science, 197, 215–223. Fretwell, S. D. & Lucas, H. J., Jr. 1970. On territorial behavior and other factors influencing habitat distribution in birds. Acta Biotheoretica, 19, 16–36. Grant, J. W. A. 1993. Whether or not to defend? The influence of resource distribution. Marine Behaviour and Physiology, 23, 137–153.
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Effects of competitor-to-resource ratio on aggression and size variation within groups of convict cichlids MICHELLE V. NOE¨ L, J AM ES W. A. G RA NT & JOS EPH G . CA RRI GA N
Department of Biology, Concordia University (Received 17 December 2003; initial acceptance 6 June 2004; final acceptance 27 July 2004; published online 24 February 2005; MS. number: A9774R)
Resource defence theory predicts that the intensity of competitive aggression, degree of resource monopolization, and variation in fitness will be highest at intermediate levels of the spatial clumping of resources. We tested for this predicted dome-shaped relationship by manipulating the spatial clumping of food via competitor-to-resource ratio (CRR), the number of potential competitors divided by the number of resource units. Groups of 10 convict cichlids, Archocentrus nigrofasciatus, were allowed to compete for a fixed amount of food in one of five CRR treatments (1, 1.43, 2, 5 and 10), created by varying the number of patches in which the food appeared (i.e. 10, 7, 5, 2 and 1 patch, respectively). As predicted, both the frequency of aggression and the coefficient of variation of body mass (a measure of the consequences of food monopolization and variation in a component of fitness within groups) increased significantly as CRR increased from 1 to 2, and then decreased significantly at CRRs of 5 and 10. In addition, mean growth rate decreased in groups with high rates of aggression, suggesting an important cost of aggression. Our study provides the first quantitative support for the predicted dome-shaped relationship and suggests that CRR is a useful measure of the degree of spatial clumping of resources. Ó 2005 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
The dispersion of resources in space and time is thought to affect how animals compete and the resulting distribution of those resources among the competitors (Brown 1964; Emlen & Oring 1977; Grant 1993). Of all the components of resource dispersion (see Warner 1980; Grant 1993), spatial clumping or patchiness has probably attracted the most attention in both theory and experiments. According to the theories of resource defence and mating systems, resources are more economically defensible and monopolizable as they become increasingly clumped in space (Emlen & Oring 1977; Grant 1993). At a local scale, an increase in the spatial clumping of a resource allows an individual to occupy a smaller home range or a smaller patch of resources, both of which will be easier to defend against intruders (Hixon 1980; Grant et al. 1992; Grant 1993). Many studies have now verified this prediction by showing an increase in aggression (Zahavi 1971; Rohwer & Ewald 1981; Robb & Grant 1998; Johnson et al. 2004), monopolization of food (Theimer 1987), or both (Magnuson 1962; Monaghan & Metcalfe 1985; Grant & Guha 1993; Ryer & Olla 1995; Kim et al. 2004) as a fixed amount of food is increasingly concentrated into a smaller patch. Correspondence: J. W. A. Grant, Department of Biology, Concordia University, 7141 Sherbrooke Street West, Montre´al, QC H4B 1R6, Canada (email: [email protected]). 0003–3472/04/$30.00/0
Similarly, male dunnocks, Prunella modularis, defend and monopolize females more easily when females occupy smaller home ranges in response to the addition of dense patches of food (Davies & Lundberg 1984). Few studies, however, have shown that short-term measures of monopolization translate to fitness differences among competitors (but see Blanckenhorn 1991; Bryant & Grant 1995). At a larger spatial scale, extremely clumped resources may attract many competitors from a great distance, making defence uneconomical (Carpenter 1987). In addition, extremely clumped resources may be locally superabundant and not worth defending (e.g. Grant et al. 2002). Hence, the defence and monopolization of resources are predicted to peak at intermediate levels of spatial clumping, when measured over a broad range of values (Carpenter 1987). However, we are unaware of any clear demonstration of such a dome-shaped relationship, perhaps because of the difficulty of measuring or manipulating resource dispersion over a broad range, particularly in the wild (Davies 1991). Operational sex ratio (OSR), the number of potentially mating males divided by the number of fertilizable females in a population at a time, was originally developed as an empirical predictor of the intensity of intrasexual competition and sexual selection (Emlen & Oring 1977). OSR is easier to measure than resource dispersion, and
1157 Ó 2005 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
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integrates how members of a breeding population map onto the dispersion of resources, mates, or predators in the wild (Emlen & Oring 1977). Competitor-to-resource ratio (CRR), the number of potential competitors divided by the number of resource units in a population at a time, is a general formulation of OSR that potentially applies to any resource, including both food and mates (Grant et al. 2000). Like OSR, CRR scales the abundance of competitors to resources and provides a quantitative measure of resource clumping in both space and time. The utility of CRR has been tested only once, where it was used to quantify the synchrony in arrival of food and mates and to predict the frequency of competitive aggression. Grant et al. (2000) demonstrated a dome-shaped relationship between the frequency of aggression and CRR, when the latter was used to quantify the clumping of food and mates in time. However, CRR has not yet been used to quantify the spatial clumping of resources or to predict the outcome of competition. In this paper, we extend the use of CRR in two important ways. First, we use CRR to quantify, for the first time, the spatial clumping of resources, rather than the temporal clumping of resources. CRR will only be a useful predictor of the intensity of competition across patches in space if individuals settle in direct proportion to the abundance of resources in those patches (i.e. an ideal free distribution; Fretwell & Lucas 1970). Then, the average number of competitors at a given patch will be equal to the overall CRR in a habitat or experimental treatment (see Grant et al. 2000). Second, we use CRR to predict the frequency of aggression and, for the first time, the consequences of resource monopolization within groups. We use size variation within groups of fish to estimate both the outcome of feeding competition and, because size is likely to be an important component of fitness, the variance in fitness. We assume that growth rate will be an important component of fitness in our species, because larger males monopolize breeding sites and mate with larger, more fecund females (Keenleyside 1985; Nuttall & Keenleyside 1993; Wisenden 1995). Specifically, we first tested the assumption that the average number of competitors at a given patch increases in direct proportion to CRR. We then tested the predictions of a dome-shaped relationship between the frequency of aggression versus CRR, and the degree of size variation within groups versus CRR.
METHODS
Experimental Subjects We chose juvenile convict cichlids as test subjects because they grow quickly and readily defend food patches in laboratory conditions (Grant & Guha 1993; Praw & Grant 1999). In the wild, adult convict cichlids are aggressive when defending offspring and nest sites, but neither adults nor juveniles have been observed to defend food resources (Wisenden 1995). Food defence in the laboratory occurs presumably because food is distributed in an economically defensible manner, unlike in the wild.
All fish in our experiment were taken from two broods (i.e. two separate pairs of adults) from our laboratory stock population. Fish from different broods were held in separate stock tanks (L ! W ! H: 90 ! 46 ! 38 cm) filled with dechlorinated tap water, maintained at 26–28 C on a 12:12 h light: dark cycle (lights on at 0700 hours). Both holding tanks were equipped with a 100-W submersible heater, a box filter, an under-gravel filter covered with coarse gravel to a depth of 3 cm, and an air stone attached to an air tube. We fed fish in stock tanks twice a day ad libitum with either commercial flake food, frozen brine shrimp (Artemia sp.) or ‘Fry Feed Kyowa’ pellets (BioKyowa, Cape Girardeau, Missouri, U.S.A). We established 25 groups of 10 fish per experimental tank, for a total of 250 fish, by choosing individuals from a single stock tank (i.e. brood) to minimize the initial size variation within groups. The two broods were evenly distributed across all treatments. We used immature fish to minimize mating behaviour and behavioural differences between the sexes. On average, fish weighed 0.587 g (range 0.309–0.904 g, N Z 250) at the beginning of trials with an initial coefficient of variation (CV, SD/mean) of body mass within groups of 0.138 (range 0.03–0.27, N Z 25).
Experimental Procedure We monitored the aggressive behaviour and size variation within the groups of 10 convict cichlids fed a constant ration, for their body size, in response to CRR. We created five levels of CRR by varying the number of food patches in which this fixed ration of food was made available for the 10 fish in each experimental aquarium (L ! W ! H: 60 ! 30 ! 35 cm). The five levels of CRR were: 10 (one patch), 5 (two patches), 2 (five patches), 1.43 (seven patches) and 1 (10 patches). Each treatment was replicated five times. A patch consisted of a single ‘cell’ cut from a standard blue ice cube tray (L ! W ! H: 5.3 ! 3.9 ! 3.0 cm). We introduced food patches twice a day for 15 min. We chose permanent patch locations and feeding times (3 h apart) to control for resource predictability in time and space. For a CRR of 10, the single patch was positioned in the centre of the tank (Fig. 1). For all other treatments, the patches were distributed evenly over the tank to maximize the distance between adjacent patches (Fig. 1). The experimental tanks were similar to stock tanks, except the experimental tanks lacked box filters, and the entire bottom of each experimental aquarium was lined with a series of yellow ice cube trays filled with sand to provide a platform into which patches were inserted. The blue feeding patches were extremely obvious against the yellow background and were readily discovered by the test fish. We also covered three sides of the tanks with white paper to minimize external disturbance. Because the 25 groups of fish were not identical in body size, the daily ration of food was adjusted to the total body mass of the group. The quantity of food, ‘Fry Feed Kyowa’ (proximate composition: crude protein not less than 55%, crude fat not less than 10%, crude fibre not more than 4%
NOE¨ L ET AL.: AGGRESSION AND SIZE VARIATION
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CRR
5
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Figure 1. Top view of experimental tanks (L ! W: 60 ! 30 cm) showing the location of food patches (dark squares) in the five competitor-to-resource ratio (CRR) treatments.
and crude ash not more than 17%), given to each group twice daily was based on the amount of food that a 0.9-g fish could eat in 1 min (0.062 g or 38 pellets; Grant et al. 2002). We used the average weight of a group to calculate the twice-daily ration, and then distributed the required pellets equally among the patches of the trial. The average daily ration for 10 fish was 496 pellets of 500 mm in diameter (i.e. 0.587 g/0.9 g ! 10 fish ! 2 times a day ! 38 pellets Z 496 pellets). If metabolic rate and meal size scale as M0.75, then our method of calculating ration size may not be strictly allometrically correct (but see Grant et al. 2002). Hence, we tested for the effect of body size when examining growth rate. In summary, the amount of food that each group received was adjusted for the total body mass of the group. Hereafter, we call this the full daily ration. To prevent patches from floating, a glass marble was attached to the bottom of each patch (i.e. cell). Each patch was also covered with another ice cube cell to keep food in the patch when first placed into the water. We then fitted
the covered patches into the correct location and removed covers simultaneously. The food was mixed with 10 ml of sand in each feeding patch to increase the foraging time. Prior to each feeding, we turned off the air supply to signal that food was about to arrive. Trials lasted for a total of 15 days. On the first day we weighed fish prior to feeding and transferred them to experimental tanks. Fish were fed half-rations (i.e. ½ of the full daily ration) for the first 2 days to minimize growth while they were still learning how to feed in their new environment. We gave full rations from day 3 to day 8 and increased rations to 150% of the full daily ration from day 9 to day 14 to accommodate growth. Because fish behaviour typically stabilizes after a week of training, we videotaped the first daily feeding on day 9 and day 14 of the trial for a period of 10 min. Fish were weighed on day 15, 24 h after their last feeding, and were then moved to a ‘used fish’ tank.
Data Analysis Behaviour of interest was scored from the video recordings. As in previous experiments with groups of convict cichlids, almost all aggressive interactions were chases, unidirectional bursts of increased swimming directed towards another individual (e.g. Grant & Guha 1993; Praw & Grant 1999). We counted the total number of chases by all individuals in each tank when fish were actively foraging (i.e. food was present). This foraging period varied between treatments and ended when fish ceased active foraging and primarily hovered over the patches. We confirmed this assumption during training by removing patches to determine whether any pellets remained. The average foraging period for CRR levels of 1, 1.43, 2, 5 and 10 were approximately 1.0, 1.5, 2.0, 2.5 and 2.5 min, respectively. We also evaluated the effects of varying CRR on aggression for a constant time period across all trials by counting the total chases within the first 5 min after removal of patch covers. We averaged the data obtained on day 9 and day 14 and used a one-way ANOVA to test for the effect of CRR on rates of aggression. We present only the data for aggression during the foraging periods, because the patterns of aggression were virtually identical when we used the behaviour during the first 5 min. To estimate the actual CRR of each trial, we counted the number of fish within one body length of each patch during 10 scan samples that were evenly spaced over the foraging period. We estimated size variation within groups by calculating the final CV of body mass. We used the initial CV of mass as a covariate in an ANCOVA when investigating the effects of CRR on final CV of mass within groups. Mean growth was calculated by subtracting the initial mean weight of fish from the final mean weight of fish in each group. To meet the assumptions of parametric tests, we log10 transformed the number of fish per patch. RESULTS If fish distribute themselves equally among patches, as predicted by an ideal free distribution (Fretwell & Lucas
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20 10 5
2 1 0.5
1
2
5
10
CRR Figure 2. The mean (GSE, N Z 5) number of convict cichlids within one body length of a given food patch in relation to competitor-toresource ratio (CRR). The dashed line is the expected number of fish per patch assuming an ideal free distribution (i.e. one-to-one line), whereas the dotted line is the expected number of fish per patch assuming an ideal free distribution of the fish within one body length of patches. Note that both axes are plotted on a logarithmic axis, and SE bars are often obscured by the symbols depicting the mean.
20
Chases per minute
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10
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0
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2
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(b) 0.35 CV of body mass
1970), then the average number of fish per patch should increase in direct proportion to CRR (Fig. 2). Consistent with this assumption, the average number of fish within one body length of a given patch increased with increasing CRR (ANOVA: F4,20 Z 262.3, P ! 0.0001; Fig. 2). However, more fish than expected (i.e. the one-to-one line was below the 95% confidence limit) were observed per patch, assuming an ideal free distribution (sensu Fretwell & Lucas 1970), at CRRs of 1 and 1.43, whereas fewer fish than expected (i.e. the one-to-one line was above the 95% confidence limit) were observed per patch at higher CRRs. If we consider only those fish within one body length of a patch, then the fish were distributed between patches as expected based on an ideal free distribution (i.e. dotted line, Fig. 2) for CRRs of 2, 5 and 10, but even more fish than expected were observed at patches for CRRs of 1 and 1.43 (Fig. 2). The rate of aggression was affected by CRR, whether measured only when food was present (ANOVA: F4,20 Z 26.21, P ! 0.0001; Fig. 3a), or during the first 5 min of each trial (not shown; F4,20 Z 21.49, P ! 0.0001). As predicted, rate of aggression followed a dome-shaped curve; aggression was low at a CRR of 1, increased and peaked at a CRR of 2 (Fisher’s LSD post hoc test: P Z 0.0013), and then decreased to its lowest level at a CRR of 10 (Fisher’s LSD post hoc test: P ! 0.0001). The initial CV of mass, on average 0.138, did not differ significantly between treatments (ANOVA: F4,20 Z 0.154, P Z 0.96). CV of body mass within groups increased over the experiment in all 25 trials (paired t test: t24 Z 11.48, P ! 0.0001). The final CV of mass (mean Z 0.276) was positively related to the initial CV of mass (ANCOVA: F1,19 Z 20.98, P Z 0.0002). After statistically controlling for the effect of initial CV of body mass, CRR had a significant effect on the final CV of body mass (ANCOVA: F4,19 Z 4.05, P Z 0.015; Fig. 3b). As predicted, final
Fish per patch
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CRR Figure 3. The mean (GSE, N Z 5) (a) rate of aggression of 10 convict cichlids and (b) final coefficient of variation (CV, SD/mean) in body mass within groups of 10 convict cichlids, in relation to competitor-to-resource ratio (CRR). Note CRR is plotted on a logarithmic scale.
CV also followed a dome-shaped relationship; it was low at a CRR of 1, increased and was highest at a CRR of 2 (Fisher’s LSD post hoc test: P Z 0.012), then decreased at CRRs of 5 (Fisher’s LSD post hoc test: P Z 0.0088) and 10 (Fisher’s LSD post hoc test: P Z 0.028). The initial mass of fish did not differ significantly between treatments (F4,20 Z 0.84, P Z 0.49). On average, fish grew in all 25 trials (paired t test: t24 Z 22.11, P ! 0.0001). If aggression is energetically costly, we might expect growth rate to be lower in tanks with higher rates of aggression. The mean growth rate of all 10 fish in a tank was not affected by CRR (ANOVA: F4,20 Z 2.51, P Z 0.074), but was negatively correlated with the aggression rate when food was present (Pearson’s correlation: r23 Z ÿ0.521, P Z 0.0075) and the aggression rate during the first 5 min of each trial (r23 Z ÿ0.558, P Z 0.0037; Fig. 4). Mean growth rate was not significantly related to the initial size of fish in each tank (r23 Z ÿ0.01, P Z 0.96). DISCUSSION The distribution of fish across patches was similar to what was expected based on an ideal free distribution. Not
NOE¨ L ET AL.: AGGRESSION AND SIZE VARIATION
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Growth rate (g)
0.7 0.6 0.5 0.4 0.3 0.2 0
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Figure 4. Mean (GSE, N Z 5) gain in mass of convict cichlids over 15 days in relation to the total rate of aggression during the first 5 min after food patches were added.
surprisingly, some fish were more than one body length from any patch during the scan samples. Some of these individuals were probably moving between patches, whereas others were excluded from patches by aggressive behaviour. The higher than expected number of fish per patch at CRRs of 1 and 1.43, when patches were close together, was probably caused by some dominant fish attempting to defend more than one patch at a time. In addition, subordinate fish may have been reluctant to be alone on a patch for antipredator reasons, as is often observed in birds (e.g. Beauchamp 1998; Johnson et al. 2004). Our experiment provided strong support for the predicted dome-shaped relationship between the frequency of competitive aggression and the spatial clumping of food, as quantified by CRR. Aggression was initially low at a CRR of 1, presumably because of a low encounter rate between the 10 fish that were dispersed among the 10 food patches. As CRR increased to 2, aggression also increased as fish more frequently encountered another individual at a patch. However, the decrease in aggression at CRRs of 5 and 10 occurred despite more potential encounters with competitors, indicating that defence of the patch was no longer feasible. Convict cichlids competing for food showed a peak in aggression at a CRR of 2, just like Japanese medaka, Oryzias latipes, competing for both food and mates (Grant et al. 2000). A CRR of 2 is of particular interest because it has been well described by animal contest theory (e.g. Parker 1984). The hawk–dove model predicts that a hawk strategy will be evolutionarily stable at a CRR of 2, if the benefit of the resource is greater than the cost of injury (Parker 1984). While aggression is expected at a CRR of 2, the actual value of CRR where aggression is most intense or frequent will probably depend on the value of the resource and the variability among individuals in competitive ability (see Dubois et al. 2003). As predicted by resource defence theory, variation in a component of fitness within groups, as measured by CV of body mass, also peaked at an intermediate level of CRR.
We assume that the increased variability in growth rate at intermediate levels of CRR was primarily due to an uneven distribution of food amongst competitors when food was economically defensible. Support for this assumption comes from our previous work showing a positive relationship between amount of aggression and the degree of food monopolization within groups (e.g. Grant & Guha 1993; Bryant & Grant 1995). In addition, the amount of food eaten is typically the best predictor of growth rate in a competitive social environment (e.g. Bryant & Grant 1995; Praw & Grant 1999). It is possible that part of the effect of CRR on size variation in our study was caused by the social stress that dominants impose on subordinates (e.g. Abbott & Dill 1989; Praw & Grant 1999). Dominant fish typically grow faster than subordinates, independent of the amount of food eaten (Abbott & Dill 1989; Dou et al. 2004). Because social stress and food monopolization both probably increase with increasing levels of aggression, both mechanisms could potentially explain growth rate variation in groups of fish at intermediate levels of CRR. In our study, however, rate of aggression explained no additional variation in the final CV of body size, after the effects of initial CV of body size and CRR were first entered in the model (ANCOVA: effect of aggression during the feeding period: F1,18 Z 0.32, P Z 0.58; effect of aggression during the first 5 min: F1,18 Z 0.56, P Z 0.46). Hence, a parsimonious interpretation of our results suggests that CRR affects aggression, which affects the monopolization of food, which affects size variation within groups. Nevertheless, the social stress hypothesis is an interesting alternative mechanism that deserves further study. Hence, CRR may affect growth rate, an important component of fitness for fish, via two different mechanisms, which are both related to aggressive behaviour. The decline in size variation within groups at high levels of CRR may initially seem at odds with the common observation of increasing size variation within cohorts with increasing population density (qomnicki 1988). In our experiment, however, the per capita food abundance was held constant, whereas it probably decreases as population density increases in the wild. The decline in CV of body size at high levels of CRR may also have implications for mating systems theory, where it is often assumed that the intensity of aggression and sexual selection will continue to increase with ever-increasing levels of OSR (e.g. Michener & McLean 1998; but see Emlen & Oring 1977). If the intensity of sexual selection is primarily driven by the intensity of male interference competition, then resource defence theory predicts a decline in sexual selection at extremely high levels of OSR. Female choice for attractive males, however, could cause the intensity of sexual selection to increase with increasing OSR, even as the intensity of male–male aggression decreases. The decrease in average growth rate in tanks with high levels of aggression suggests that aggression has an important energetic cost. We assume the rates of aggression that were observed for only 5 min per day were not sufficient to generate the growth differences depicted in Fig. 4. It is possible that the differences in aggression across CRR
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treatments persist for much of the day, albeit at a reduced level, because aggression decreases outside of the foraging period (Robb 1996). In addition to the direct energetic costs of aggression, the lower growth may also have been related to the elevated stress levels of both dominant (e.g. Praw & Grant 1999) and subordinate (e.g. Abbott & Dill 1989) fish in tanks with high levels of aggression. Taken together, our results suggest that high levels of CRR will minimize the rate of competitive aggression and growth rate variation within groups, and will maximize average growth rate. Because these are also the goals of the aquaculture industry (e.g. Noakes & Grant 1992), CRR may be a useful tool for both pure and applied behavioural ecologists. Acknowledgments We thank Cindy Breau for help in the laboratory and Stefan Steingrı´msson, Diana Hews and two anonymous referees for comments on the manuscript. This research was financially supported by a Discovery Grant from the Natural Sciences and Engineering Research Council of Canada to J.W.A.G. References Abbott, J. C. & Dill, L. M. 1989. The relative growth rate of dominant and subordinate juvenile steelhead trout (Salmo gairdneri) fed equal rations. Behaviour, 108, 104–113. Beauchamp, G. 1998. The effect of group size on mean food intake rate in birds. Biological Reviews, 73, 449–472. Blanckenhorn, W. U. 1991. Fitness consequences of foraging success in water striders (Gerris remigis; Heteroptera: Gerridae). Behavioral Ecology, 2, 46–55. Brown, J. L. 1964. The evolution of diversity in avian territorial systems. Wilson Bulletin, 76, 160–169. Bryant, M. J. & Grant, J. W. A. 1995. Resource defence, monopolization and variation of fitness in groups of female Japanese medaka depend on the synchrony of food arrival. Animal Behaviour, 49, 1469–1479. Carpenter, F. L. 1987. Food abundance and territoriality: to defend or not to defend? American Zoologist, 27, 387–399. Davies, N. B. 1991. Mating systems. In: Behavioural Ecology (Ed. by J. R. Krebs & N. B. Davies), pp. 263–294. Oxford: Blackwell Scientific. Davies, N. B. & Lundberg, A. 1984. Food distribution and a variable mating system in the dunnocks, Prunella modularis. Journal of Animal Ecology, 53, 895–912. Dou, S. Z., Masuda, R., Tanaka, M. & Tsukamoto, K. 2004. Size hierarchies affecting the social interactions and growth of juvenile Japanese flounder, Paralichthys olivaceus. Aquaculture, 233, 237–249. Dubois, F., Giraldeau, L.-A. & Grant, J. W. A. 2003. Resource defense in a group-foraging context. Behavioral Ecology, 14, 2–9. Emlen, S. T. & Oring, L. W. 1977. Ecology, sexual selection, and the evolution of mating systems. Science, 197, 215–223. Fretwell, S. D. & Lucas, H. J., Jr. 1970. On territorial behavior and other factors influencing habitat distribution in birds. Acta Biotheoretica, 19, 16–36. Grant, J. W. A. 1993. Whether or not to defend? The influence of resource distribution. Marine Behaviour and Physiology, 23, 137–153.
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