Behavioral Ecology Advance Access originally published online on July 7, 2007
Behavioral Ecology 2007 18(5):910-915; doi:10.1093/beheco/arm057
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Sex and the selfish herd: sexual segregation within nonmating whirligig groups
a Department of Biology, State University of New York at Potsdam, Potsdam, NY 13676, USA b Department of Biology, Oberlin College, Oberlin, OH 44074, USA
Address correspondence to W.L. Romey. E-mail: romeywl{at}potsdam.edu.
Received 19 January 2007; revised 25 May 2007; accepted 26 May 2007.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
|---|
The fitness costs and benefits at different positions in fish shoals, bird flocks, and insect swarms can be asymmetric; a group's edge may provide more feeding opportunities, but also greater predator risk. Animals make trade-offs between these selection pressures based on individual differences in traits including satiation level, ability to avoid predators, and sex. Previous studies did not evaluate the impact of sex on group positioning in these types of nonhierarchical, nonmating groups called congregations. A controlled laboratory experiment was conducted, using marked whirligig beetles (Coleoptera: Gyrinidae), to test for sexual segregation and why different sexes might choose different positions. Soon after a disturbance, males often were found at the periphery and females at the center of groups. There was also an overlying influence of feeding on position; satiated individuals moved toward the center and hungry individuals toward the periphery. Several minutes after a disturbance, sexual segregation disappeared, but segregation due to hunger persisted. Sexual segregation in this study was best explained by the predator avoidance hypothesis, not the energy needs hypothesis. Females weighed less than males; this may make them more at risk to predation because of reduced swimming speed or less mechanical protection from their exoskeleton. No difference between the sexes was found in the volume of their defensive chemicals. This is one of the first studies to show that sex influences position of individuals within simple nonmating groups (congregations) and suggests that more attention should be given to positional sex differences within shoals, flocks, herds, and swarms.
Key words: congregation, Dineutes, grouping, gyrinidae, nondimorphic, predator avoidance, sexual segregation, spatial position, swarm, trade-offs, whirligig.
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
|---|
Gregarious individuals make adaptive decisions when choosing which and what part of a group to occupy (Krause et al. 1992
; Romey 1995). These individual choices can lead to segregation between or within groups based on particular traits including species, body size, parasite load, defenses, hunger state, age, and sex (Krause and Ruxton 2002). In this paper, we use the word "group" in the limited sense of the word "congregation" as defined in Parrish and Hamner (1997). They define a congregation as a group composed of individuals that are gregarious, have limited dominance hierarchies, can enter and exit without restriction, and are not necessarily related. This includes many of the more conspicuous groups found in nature (fish, birds, insects, and crustacea), but not pack-forming animals or eusocial insects. Herds of ungulates are sometimes excluded by this definition because of their well-developed dominance hierarchies but still exhibit similar within-group positioning differences (Prins 1989; Le Pendu et al. 1996; Michelena et al. 2004; Focardi and Pecchioli 2005). Visible sexual dimorphism is often lacking in true congregation-forming species, at least in characteristics visible to a predator such as coloration or body length that would lead one sex to stand out and be targeted (the oddity effect: Landeau and Terborgh 1986).
An individual's particular suite of traits determines how it makes trade-offs between conflicting (or reinforcing) selection pressures to arrive at a position in a congregation (Rayor and Uetz 1990, 1993; Romey 1995). Under many ecological circumstances, there is more risk of predation on the outside of a group, but also more food (Krause 1994). Peripheral and internal positions can be considered different patches, and an individual's patch use can be considered a trade-off between obtaining food and avoiding predators (Gilliam and Fraser 1987). Size stratification within groups has been documented in many species; large individuals move to the center more quickly than smaller individuals when a predator attacks (Hamilton 1971; Millinski 1977; Theodorakis 1989; Rayor and Uetz 1990; Krause 1994). Hunger state also influences group position; hungry individuals in a congregation are more likely to go to the periphery or front of a group (Romey 1995). Age and size also influence group position in some congregations. For example, in communal webs of some spiders, young occupy the periphery, whereas older ones occupy the center (Rayor and Uetz 1993). Also, individuals who perceive greater risk to themselves are likely to choose center positions in a group (Krause 1993, 1994). Although direct effects of sex on group positions during the mating season are well known (i.e., courting males surround grouped females or females surround male leks [Hoglund and Alatalo 1995]), the indirect effects of sex on group position during the rest of the year are not. One hurdle to this kind of study has been the difficulty of identifying the sex of sexually monomorphic individuals in congregation-forming species.
Although sexual segregation within groups is not well studied, there is a broad literature on sexual segregation between groups, especially for vertebrates (see review in Ruckstuhl and Neuhaus 2005). The theory and findings from between-group sexual segregation are pertinent to within-group sexual segregation. Sexual segregation between groups is defined as a nonrandom distribution of males and females between social groups (Conradt 1998). Between-group sexual segregation in ungulates has been modeled as a result of sexual dimorphism in body weight (>20%) leading to differences in feeding requirements and predation risk and leading to differences in activity budgets (Ruckstuhl and Neuhaus 2002). For example, in ungulates, larger animals have more efficient digestion (Ruckstuhl and Neuhaus 2002) and may need less food and, therefore, would not need to graze and move as much. In nonungulates, however, one would expect larger animals to need more food (Schmidt-Nielsen 1997). Compounding the effects of body size dimorphism is the difference in ratio of muscle to fat tissue between the sexes. In many species, males have a greater ratio of muscle to fat than females, and because muscle metabolizes at a higher rate than fat, males are predicted to have greater energetic demands even if there was no weight dimorphism (Schmidt-Nielsen 1997).
Another explanatory element of between-group sexual segregation theory is that there is a difference in predation risk between the sexes (Ruckstuhl and Neuhaus 2005). For example, Croft et al. (2004) found that male guppies were more vulnerable to predators due to color differences and that they stayed in male-biased groups in safer habitats. In some ungulates, females with nursing young have a greater predation risk than males and therefore move to safer habitats (Ruckstuhl and Neuhaus 2002). Sexual dimorphism in body size can also lead to unequal predation risk between the sexes when there is a positive correlation between size and predator avoidance due to greater speed, larger defensive weapons (e.g., ungulate horns), more exterior plating (e.g., insect exoskeleton), or more chemical defenses (Evans and Schmidt 1990; Krause and Ruxton 2002).
We propose that some of the same mechanisms used to explain sexual segregation at larger scales (between groups) can explain sexual segregation within groups. Groups are not homogeneous habitats; the feeding and predator avoidance opportunities vary according to distance from the edge and front (Krause 1994; Romey 1995). The predation risk hypothesis, as applied to within-group differentiation, would lead to the prediction that the larger or better-defended sex would take up peripheral positions in a congregation (high food but greater predation risk). Perhaps, the sexes differ in defenses because of differing needs to defend territories or manufacture gametes. For insects, one would predict that the sex with the least defensive chemicals would choose to be at the group's center (safer but less foraging opportunities). The general form of the energy needs hypothesis, applied to within-group sexual segregation of nonungulates, would suggest that males, with their greater metabolic rate, would choose peripheral positions to obtain more food. Although the original sense of this hypothesis was for animals with high (>20%) sexual dimorphism (Ruckstuhl and Neuhaus 2002), we feel that it would apply even for slightly dimorphic species. Simulation models based on proximate movement rules also suggest that larger individuals should choose the periphery (Romey 1996; Hemelrijk and Kunz 2005).
In this study, we test for sexual segregation within a nonmating congregational species, the whirligig beetle (Coleoptera, Gyrinidae), by evaluating the position of individually marked animals in the laboratory immediately after a simulated predator scare and then several minutes later. In order to help differentiate among competing hypotheses for sexual segregation (i.e., energy needs vs. predation risk), we manipulated hunger state and measured the degree of sexual dimorphism in body size and defensive chemicals.
Study species
Whirligig beetles are a useful study species to test for sexual segregation because they group well in the laboratory, are easily marked, and form 2-dimensional congregations at the water's surface (Romey 1995, 1997). In late summer and autumn, adults aggregate into large nonmating groups during the day, whose members react strongly to the slightest disturbances such as shadows from above or disturbances in the water. At night, they sometimes disperse but usually rejoin a group at dawn (Heinrich and Vogt 1980). In winter, they diapause underwater, then in the spring they lay eggs that hatch into aquatic larvae (Balfour-Browne 1950; Istock 1966; Heinrich and Vogt 1980). The primary function for grouping in whirligigs is predator avoidance (Vulinec and Miller 1989; Watt and Chapman 1998). A variety of fish and bird predators are known to prey on them, including largemouth bass (Micropterus salmoides), trout (Onchorhynchus mykiss), black ducks (Anas rubripes), and loons (Gavia immer) (Wilson 1923; Heinrich and Vogt 1980; Alvo and Campbell 2000; Eisner and Aneshansley 2000; Harlin 2005). Whirligigs produce defensive chemicals to help them avoid predation; they secrete gyrinidal from their pygidial gland when disturbed (Eisner and Aneshansley 2000). They eat randomly distributed food particles (usually other insects) trapped at the water's surface during the night and day, and beetles at the periphery of groups are more likely to obtain these food particles (Romey 1995). Dineutes discolor is nondimorphic (monomorphic): both sexes are dorsally black and ventrally straw colored. Although females have a slightly longer wing cover (elytra) than males, their overall body length is not significantly different from males (Ferkinhoff and Gunderson 1983). Little quantitative data exist on weight or fat differences between sexes in D. discolor or other species of Gyrinidae.
|
METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
|---|
Collection and preparation
Whirligigs (D. discolor) were collected by long-handled dip nets along the Raquette River in Potsdam, NY, USA (long 75°00', lat 44°40'N) on 30 June and 8 July 2004. Approximately 250 beetles were brought to The State University of New York at Potsdam each week and then returned after the experiment. Maintenance and marking of beetles was similar to that described elsewhere (Romey 1995
) unless otherwise mentioned. A 13:11 h light:dark cycle was maintained in the laboratory. Beetles were maintained at room temperature (21–23 °C) in 2 stock tanks (1.4 m diameter) filled to a depth of 8 cm with aged tap water. Beetles were acclimated for 3 days under a satiation diet of 4 mg freeze-dried bloodworms per beetle per day.
Beetles were then marked and separated into treatment groups (satiated and hungry males and females). We differentiated between sexes by their tarsal hairs (Ferkinhoff and Gundersen 1983). Teneral beetles were not used (recently emerged beetles have soft elytra for 1–2 weeks). Each beetle was marked with 2 spots of quick drying paint to signify sex and feeding treatment. Color used to signify a particular trait was alternated between weeks to prevent unknown color preferences/aversions from influencing their behavior. The 4 treatment groups were kept in replicated treatment tanks (circular blue polypropylene pools (0.54 m diameter, 0.58 m deep, filled to a depth of 20 cm with aged tap water). Half the males (60) continued on the satiation diet for 3 more days (satiated), whereas the other half (60) were given half this ration (hungry). Equal numbers of females (120) were also divided into the 2 feeding regimes. After the treatment period, groups of 24 beetles were assembled (6 hungry male, 6 satiated male, 6 hungry female, 6 satiated females) and placed into each of 6 treatment tanks. Experimental tanks were 1 m diameter circular blue plastic pools filled to a depth of 8 cm with aged tap water. These tanks were surrounded by 2-m-high black plastic blinds. Lighting consisted of three 120 W floodlights 1 m above the water and rows of overhead fluorescent room lights (32 W each) 2.7 m above the tanks.
Whirligigs were introduced into experimental tanks at 1700 h and left overnight to acclimate. To facilitate normal grouping behavior in the morning, we simulated a dawn period and predator disturbances. To simulate dawn, we turned on the light in 3 stages from 7:00 to 7:30 AM. To simulate predator disturbances, we passed a 12-cm diameter black circle 1 m above each group at 2 m/s twice during the "dawn" and once just prior to photographing them. Whirligigs respond strongly to visual disturbances such as this and adopt their typical protean display (whirling) for approximately 30 s, after which they stay relatively motionless in groups (Brown and Hatch 1929; Newhouse and Aiken 1985). In pilot observations, both aerial and aquatic disturbances seemed to provide equal stimuli to initiate grouping which then lasted the rest of the day (Romey WL, personal observation).
Photographs (instantaneous scan samples as per Altmann 1974) were taken of the grouped beetles 2 and 4 min after the final disturbance between 8:00 and 8:30 AM using a 5.1 megapixel Olympus C-5060 digital camera mounted 1.8 m directly above each tank on a mobile platform. A remote control was used to take the picture to minimize unplanned visual disturbances. A total of 30 replicate groups were filmed over a 2-week period. Beetles were resampled from stock tanks, so that within a week each beetle was probably used more than once but not with the same group members. On the first week, 6 tanks were filmed the first day (24 beetles per tank = 144 beetles total), then beetles were returned to stock tanks to feed and mix with other beetles (total of at least 250 beetles), resampled at random that evening, and reintroduced to experimental tanks that night. Three successive days of tests were done the first week with the first set of beetles. Then the second week, entirely new beetles were collected, marked, and 12 more tanks (more than 2 days) were photographed. Position and type of treatment tanks was rotated between days and weeks to minimize unintended effects, and week was added as an effect in statistical models.
Images were analyzed for group position using Image-J software (Rasband 2004). Scaled coordinates for each beetle's body were recorded along with its satiation level and sex. Beetles more than 10 body lengths away from others, or climbing the tank's side, were not included in analysis as they had left the group. On average, 80% of whirligigs in any particular group satisfied these criteria for grouping, and there was no significant bias for those not joining (chi-squared test, P = 0.20, 
2 = 1.65, degrees of freedom [df] = 1). Group centroid was calculated for each group (average XY coordinate), and distance of each beetle to that centroid was determined within 1 mm. Distance to center is an appropriate measure for group centrality in cases such as whirligig aggregations that are spherical and where individuals are regularly spaced (Stankowich 2003; Christman and Lewis 2005).
In addition to the position analysis, we also examined differences in chemical defenses and weight of the beetles. In July 2005, we determined the sex-specific volume of gyrinidal (their defensive compound) following the methods of Meinwald et al. (1972). Beetles were obtained from the same section of river, and equal numbers of males and females were frozen at –10 °C for 24 h. When thawed, we collected the extruded gyrinidal in a micropipette. The volume of this exudate was measured to the nearest half millimeter, as a proxy for volume (1 mm = 0.15 µl). In July 2006, sexual dimorphism in body weight was determined by comparing the live weights of 885 beetles. Whirligigs were collected every week for 3 weeks along the same section of river, dried on a paper towel, placed into a microcentrifuge tube (to reduce movement), then weighed to the nearest 0.0001 g.
Statistical analysis
A mixed-model analysis of variance (ANOVA) was used to test the influence of sex and hunger (fixed effects) on the distance of each beetle to the center of a group, with group as a random effect in the model (SPSS v 11.5). Week of collection was also included as a fixed nominal variable. The distances to center had significant departures from normality (Kolmogorov–Smirnov test < 0.05), so the distance of each beetle to the center of its group was first log transformed (natural log of original datum + 1). All ANOVAs were performed on these transformed data, but marginal means and error bars for figures are shown for untransformed data. A 2-sampled t-test was used to compare weight and gyrinidal between sexes.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
|---|
Two minutes after a simulated predator attack, males were significantly more likely (Table 1, Figure 1) to be on the periphery of a group than females (mean [standard error, SE] distance to the center (DTC) for males = 5.52 [0.30] cm and for females = 4.71 [0.31]), and hungry whirligigs were significantly more likely to be on the periphery compared with satiated beetles (mean [SE] DTC for hungry = 5.52 [0.30] cm and for satiated = 4.72 [0.30]). Overall, satiated females were at the very center of a congregation and hungry males at the periphery (Figure 1). Four minutes after the attack, there was no longer any sexual segregation, but the group remained significantly stratified by hunger (Table 2). Females were 4% lighter than males (2-sampled t-test, P < 0.001, t = 4.349, df = 884, mean weight [SE] for females = 0.069 [0.0004] g and for males = 0.072 [0.0004] g). Males and females did not differ in the amount of gyrinidal that they released (2-sampled t-test, P = 0.47, t = 0.73, df = 29, mean [SE] of gyrinidal for females = 1.63 [0.30] mm and for males = 1.92 [0.28] mm). The beetles grouped more tightly (significantly smaller distance to the center) during the second week of replicates (Table 1).
|
|
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
|---|
Sexual segregation within the group occurred in whirligigs as an immediate and short-lived response to the predator attack, whereas segregation due to hunger state was consistent over the study period. As in studies of other species of whirligig (Romey 1995
), individuals that were hungry took up peripheral positions that allow them to obtain more food, but at a cost of additional predation risk (Figure 1). The current study expands that study by showing that hunger influences group position in other species of whirligig and occurs equally in both males and females. Hunger structures many other species of congregations in a similar manner: as a simultaneous balance between predation risk and foraging (Krause and Ruxton 2002). The observed within-group sexual segregation, however, is previously undocumented for congregations and appears to be explained by the predation risk hypothesis rather than the energy needs hypothesis (Ruckstuhl and Neuhaus 2002).
Sexual segregation (males on the periphery, females at the center) occurred in our study directly after the simulated attack (2 min), but not later (4 min). Sexual differences in defense may therefore influence how whirligigs make trade-offs in group position. One explanation for this is the size difference between males and females; females weighed significantly less than males and may be more at risk to predators because of decreased speed or other defenses. This is similar to other studies of size segregation (Krause et al. 1998) in which smaller individuals (but of unknown sex) are at greater risk and maintain center positions because they are safer. Fish attack the periphery of whirligig congregations significantly more often than the center (Romey WL, unpublished data). Smaller individuals are likely to swim more slowly and have less resistance to being eaten. Although there are many studies of swimming and movement in whirligigs (Tucker 1969; Newhouse and Aiken 1985; Fish and Nicastro 2006), none of them have compared sex differences in swimming speeds or looked at different rates of activity in males and females. In future, it would be useful to determine if there is differential predation between the sexes. It is not known whether our observed weight differences persist through autumn. Studies of a related whirligig genus did not find a weight difference (or fat difference) between males and females in the autumn (Svensson 2005). However, females do loose weight rapidly when they lay their eggs in the spring (Svensson 2005).
We also tested for a difference in defensive chemicals between sexes; we predicted that the sex with the least gyrinidal would be at the center. Despite a wide literature on gyrinidal (Meinwald et al. 1972; Henrikson and Stenson 1993; Harlin 2005), no one has examined the role of sex on gyrinidal. There is potentially a trade-off in females on whether lipids are converted to gyrinidal (a steroid derivative) (Meinwald et al. 1972) or invested in egg production (although not necessarily in autumn). We found no significant difference in gyrinidal volume in our study, so must reject the explanation that sexual segregation is due to differences in amount of defensive chemicals. More work should be done to follow up on this, such as examining the relative concentration of active ingredients in the exudate. Few authors have studied sex differences in defensive chemicals of insects (Eisner 2003).
In contrast to our findings, the energy needs hypothesis for sexual segregation would predict a long-lasting difference in positions of males and females. This hypothesis was not supported because only short-term sexual segregation was observed (Table 1 vs. Table 2). Even so, the observation that males were on the outside and females on the inside would have been supported because males had a greater weight and therefore would have had greater per-individual energy needs. Whirligigs feed in the daytime and once satiated will move to more central positions (Romey 1995). Sexual differences in dispersal could also play a role in differing energy budgets for males and females in some species of whirligig. In Gyrinus marinus, males were more likely to fly than females during spring but not in late summer (van der Eijk 1983). However, in a study of D. assimilis, no sex difference in migration rates was found (Nürnberger and Harrison 1995). The effects of sex and hunger reinforced themselves in our study; the interaction effect between the 2 factors was not significant (Tables 1 and 2).
The proximate mechanism for how females arrive at the center and males at the periphery was not directly examined in this study. However, ethograms comparing the sexes show differences that might relate to segregation (Freilich 1986; Vulinec and Kolmes 1987; Romey and Rossman 1995). Fitzgerald (1987) reported that female D. discolor "bump" other individuals more often than males do, and that bumping is correlated to movement toward the center after 10 s. But, bumping may be a byproduct of their movement toward the middle, not a show of aggression. Position of beetles within a group could be a result of targeted movement or a byproduct of preferred nearest neighbor distances (Romey 1995). Romey (1995) showed a correlation between position in a group and nearest neighbor distance; hungry individuals had both a larger nearest neighbor distance and were at the periphery. Another proximate mechanism for sexual segregation is a difference in activity levels, as shown by simulation models (Romey 1996; Ruckstuhl and Kokko 2002; Hemelrijk and Kunz 2005). In insects, activity levels are closely related to temperature, and it was shown in other studies that warmer whirligigs are more active and that this can lead to occupancy of outer positions (Fitzgerald 1987; Romey and Rossman 1995). Sexual size differences could even influence temperature and lead to males being warmer and more active. The between-week difference in grouping in our study (Table 1) may have been a result of differences in field temperature (prior to coming into the laboratory) or prior feeding levels.
We believe that the predation risk hypothesis explains the observed sexual segregation better than the energy needs hypothesis, but there are still other hypotheses. One could argue that whirligigs are still in their mating season and that sexual segregation was related to mating. However, whirligigs mate primarily in spring and early summer, and they do this primarily in territories along shore (Fitzgerald 1987). Although we saw an occasional mating attempt within our study animals, it was unusual. By late summer, most overwintered adults have died, and recently emerged adults do not mate till spring (Istock 1966). Another argument is that within-group sexual segregation is a product of kin selection. This is unlikely because most individuals in these groups are of similar age (within 2 months), and they disperse widely in early summer to different water bodies and reform in different groups within those ponds every morning (Heinrich and Vogt 1980; Nürnberger and Harrison 1995). Last, one could argue that there is a dominance hierarchy where females aggressively take the group's middle when predators threaten. This is not supported by our data because males were larger. In a study of aggression within groups, Fitzgerald (1987) found that males and females did not have significant differences in aggressive acts. Also, our observations differ from the studies of size segregation in fish and arthropods where the large individuals (of undetermined sex) move to the group's center when attacked (Krause 1994).
In conclusion, our findings are some of the first to find sexual segregation in nonmating congregations. The explanation for our data fits within the framework of adaptive individual trade-offs under conflicting selection pressures as well as sexual segregation theory traditionally applied between groups of ungulates. In our study, hungry individuals remained at the periphery and satiated ones at the center. When attacked, females initially moved toward the center. The specific duration of this sexual segregation should be examined in more detail in future studies, although we know that hunger stratification can be reversed in less than 24 h (Romey 1995). In addition, it would be interesting to determine whether the degree of sexual dimorphism in body size in different species of whirligig beetles influences the degree of within-group sexual segregation. Our findings suggest that sexual segregation may occur generally in other congregational species such as large fish shoals and bird flocks. We hope that our study stimulates research into this phenomenon. For taxa in which sex is difficult to determine, such as juvenile fish, development of rapid genetic assays might be useful.
|
FUNDING |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
|---|
National Science Foundation (IBN–0315474) to W.L.R.
|
ACKNOWLEDGEMENTS |
|---|
We wish to thank M. Botham, E. Jakob, and J. Schreer for their helpful comments on previous versions of this article. Also, we thank E. Galbraith, A. Walston, W. Donelan, and S. LaBuda for helping conduct and analyze experiments.
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
|---|
Altmann J. Observational study of behavior: sampling methods. Behaviour (1974) 48:227–267.
Alvo R, Campbell D. Pre-fledged common loon, Gavia immer, on an acidic lake dies with food bolus in esophagus. Can Field-Natur (2000) 114:700–702.
Balfour-Browne F. British water beetles. (1950) London: Bernard Quaritch Ltd.
Brown CR, Hatch MH. Orientation and "fright" reactions of whirligig beetles (Gyrinidae). J Comp Psychol (1929) 9:159–189.[CrossRef][Web of Science]
Christman MC, Lewis D. Spatial distribution of dominant animals within a group: comparison of four statistical tests of location. Anim Behav (2005) 70:73–82.[CrossRef][Web of Science]
Conradt L. Could asynchrony in activity between the sexes cause intersexual social segregation in ruminants. Proc R Soc Lond B Biol Sci (1998) 265:1359–1363.[Medline]
Croft DP, Botham MS, Krause J. Is sexual segregation in the guppy, Poecilia reticulata, consistent with the predation risk hypothesis? Environ Biol Fishes (2004) 71:127–133.
Eisner T. For love of insects. (2003) Harvard (UK): Harvard University Press.
Eisner T, Aneshansley DJ. Chemical defense: aquatic beetle (Dineutes hornii) vs. fish (Micropterus salmoides). Proc Natl Acad Sci USA (2000) 97:11313–11318.
Evans DL, Schmidt JO. Insect defenses; adaptive mechanisms of prey and predators. (1990) Albany (NY): State University of New York Press.
Ferkinhoff WD, Gundersen RW. A key to the whirligig beetles of Minnesota and adjacent states and Canadian provinces (Coleoptera: Gyrinidae). Sci Pub Sci Mus Minn (1983) 5:53.
Fish FE, Nicastro AJ. Aquatic turning performance by the whirligig beetle: constraints on maneuverability by a rigid biological system. J Exp Biol (2006) 206:1649–1656.[CrossRef]
Fitzgerald VJ. Social behavior of adult whirligig beetles Dineutes nigrior and D. discolor (Coleoptera: Gyrinidae). In: Am Midl Nat (1987) 118:439–448.[CrossRef]
Focardi S, Pecchioli E. Social cohesion and foraging decrease with group size in fallow deer (Dama dama). Behav Ecol Sociobiol (2005) 59:84–91.[CrossRef][Web of Science]
Freilich JF. Contact behavior of the whirligig beetle Dineutes assimilis (Coleoptera: Gyrinidae). Entomol News (1986) 97:215–221.[Web of Science]
Gilliam JF, Fraser DF. Habitat selection under predation hazard: test of a model with foraging minnows. Ecology (1987) 68:1856–1862.[CrossRef][Web of Science]
Hamilton WD. Geometry for the selfish herd. J Theor Biol (1971) 31:295–311.[CrossRef][Web of Science][Medline]
Harlin C. To have and have not: volatile secretions make a difference in gyrinid beetle predator defence. Anim Behav (2005) 69:579–585.[CrossRef][Web of Science]
Heinrich B, Vogt D. Aggregation and foraging behavior of whirligig beetles (Gyrinidae). Behav Ecol Sociobiol (1980) 7:179–186.[CrossRef][Web of Science]
Hemelrijk CK, Kunz H. Density distribution and size sorting in fish schools: an individual-based model. Behav Ecol (2005) 16:178–187.
Henrikson BI, Stenson JAE. Alarm substance in Gyrinus aeratus (Coleoptera, Gyrinidae). Oecologia (1993) 93:191–194.[CrossRef][Web of Science]
Hoglund J, Alatalo RV. Leks. (1995) Princeton (NJ): Princeton University Press.
Istock CA. Distribution, coexistence, and competition of whirligig beetles. Evolution (1966) 20:211–234.[CrossRef][Web of Science]
Krause J. The effect of "schreckstoff" on the shoaling behaviour of the minnow: a test of Hamilton's selfish herd theory. Anim Behav (1993) 45:1019–1024.[CrossRef][Web of Science]
Krause J. Differential fitness returns in relation to spatial position in groups. Biol Rev (1994) 69:187–206.[Medline]
Krause J, Bumann D, Todt D. Relationship between the position preference and nutritional state of individuals in schools of juvenile roach (Rutilus rutilus). Behav Ecol Sociobiol (1992) 30:451–456.
Krause J, Reeves P, Hoare D. Positioning behavior in roach shoals: the role of body length and nutritional state. Behaviour (1998) 135:1031–1039.
Krause J, Ruxton GD. Living in groups. (2002) Oxford: Oxford University Press.
Landeau L, Terborgh J. Oddity and the "confusion effect" in predation. Anim Behav (1986) 34:1372–1380.[CrossRef][Web of Science]
Le Pendu Y, Maublanc M-L, Briedermann L, Dubois M. Spatial structure and activity in groups of Mediterranean mouflon (Ovis gmelini): a comparative study. Appl Anim Behav Sci (1996) 46:201–216.[CrossRef][Web of Science]
Meinwald J, Opheim K, Eisner T. Gyrinidal: a sesquiterpenoid aldehyde and the defensive glands of the gyrinid beetles. Proc Natl Acad Sci USA (1972) 69:1208–1210.
Michelena P, Bouquet PM, Dissac A, Fourcassié V, Lauga J, Gerard J-F, Bon R. An experimental test of hypotheses explaining social segregation in dimorphic ungulates. Anim Behav (2004) 68:1371–1380.[CrossRef][Web of Science]
Millinski M. Do all members of a swarm suffer the same predation? Z Tierpsychol (1977) 45:373–388.[Web of Science]
Newhouse NJ, Aiken RB. Protean behaviour of a neustonic insect: factors releasing the fright reaction of whirligig beetles (Coleoptera: Gyrinidae). Can J Zool (1985) 64:722–726.
Nürnberger B, Harrison RG. Spatial population structure in the whirligig beetle Dineutes assimilis: evolutionary inferences based on mitochondrial DNA and field data. Evolution (1995) 49:266–275.[CrossRef][Web of Science]
Parrish JK, Hamner WM. Animal groups in three dimensions. (1997) Cambridge (UK): Cambridge University Press.
Prins HHT. Buffalo herd structure and its repercussions for condition of individual African buffalo cows. Ethology (1989) 81:47–71.[Web of Science]
Rasband W. 2004. Image J 1.32j [Internet]Bethesda, (MD): National Institutes of Health; [cited 2007 June 15]. Available from: http://rsb.info.nih.gov/ij/Java 1.3.1.
Rayor LS, Uetz GW. Trade-offs in foraging success and predation risk with spatial position in colonial spiders. Behav Ecol Sociobiol (1990) 27:77–85.[CrossRef][Web of Science]
Rayor LS, Uetz GW. Ontogenetic shifts within the selfish herd: predation risk and foraging trade-offs change with age in colonial web-building spiders. Oecologia (1993) 95:1–8.[Web of Science]
Romey WL. Position preferences within groups: do whirligigs select positions which balance feeding opportunities with predator avoidance? Behav Ecol Sociobiol (1995) 37:195–200.[CrossRef][Web of Science]
Romey WL. Individual differences make a difference in the trajectories of simulated schools of fish. Ecol Modell (1996) 92:65–77.[CrossRef][Web of Science]
Romey WL. Inside or outside? Testing evolutionary predictions of positional effects. In: Animal groups in three dimensions—Parrish JK, Hamner WM, eds. (1997) Cambridge (UK): Cambridge University Press. 174–193.
Romey WL, Rossman DS. Temperature and hunger alter grouping trade-offs in whirligig beetles. Am Midl Nat (1995) 134:51–62.[CrossRef]
Ruckstuhl KE, Kokko H. Modelling sexual segregation in ungulates: effects of group size, activity budgets and synchrony. Anim Behav (2002) 64:909–914.[CrossRef][Web of Science]
Ruckstuhl KE, Neuhaus P. Sexual segregation in ungulates: a comparative test of three hypotheses. Biol Rev (2002) 77:77–96.[Medline]
Ruckstuhl KE, Neuhaus P. Sexual segregation in vertebrates: ecology of the two sexes. (2005) Cambridge (UK): Cambridge University Press.
Schmidt-Nielsen K. Animal physiology, adaptation and environment. (1997) Cambridge (UK): Cambridge University Press.
Stankowich T. Marginal predation methodologies and the importance of predator preferences. Anim Behav (2003) 66:589–599.[CrossRef][Web of Science]
Svensson BW. Seasonal fat content fluctuations in a gyrinid beetle: comparison between an arctic and a temperate zone population (Coleoptera: Gyrinidae). Aquat Insects (2005) 27:11–19.[CrossRef]
Theodorakis CW. Size segregation and the effects of oddity on predation risk in minnow schools. Anim Behav (1989) 38:496–502.[CrossRef][Web of Science]
Tucker VA. Wave-making by whirligig beetles (Gyrinidae). Science (1969) 166:897–899.
van der Eijk RH. Population dynamics of gyrinid beetles I: flight activity of Gyrninus marinus Gyll. Oecologia (1983) 57:55–64.[CrossRef][Web of Science]
Vulinec K, Kolmes SA. Temperature, contact rates, and interindividual distance in whirligig beetles (Coleoptera: Gyrinidae). J N Y Entomol Soc (1987) 95:481–486.
Vulinec K, Miller MC. Aggregation and predator avoidance in whirligig beetles (Coleoptera: Gyrinidae). J N Y Entomol Soc (1989) 97:438–447.
Watt PJ, Chapman R. Whirligig beetle aggregations: what are the costs and the benefits? Behav Ecol Sociobiol (1998) 42:179–184.[CrossRef][Web of Science]
Wilson CB. Water beetles in relation to pondfish culture, with life histories of those found in fishponds at Fairport, Iowa. Bull US Bur Fish (1923) 39:231–345.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  A. De Vos and M. J. O'Riain Sharks shape the geometry of a selfish seal herd: experimental evidence from seal decoys Biol Lett, September 30, 2009; (2009) rsbl.2009.0628v1. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. J. Morrell and W. L. Romey Optimal individual positions within animal groups Behav. Ecol., July 1, 2008; 19(4): 909 - 919. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
W. L. Romey and E. Galbraith Optimal group positioning after a predator attack: the influence of speed, sex, and satiation within mobile whirligig swarms Behav. Ecol., March 1, 2008; 19(2): 338 - 343. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
W.L. Romey, A.R. Walston, and P.J. Watt Do 3-D predators attack the margins of 2-D selfish herds? Behav. Ecol., January 1, 2008; 19(1): 74 - 78. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||