Selfish herd effects depend on prey crypsis

Abstract

Determining why some animals form groups while others remain solitary is a longstanding goal in behavioural ecology. Group formation can help mitigate predation risk through various mechanisms, including risk dilution and group vigilance. The selfish herd hypothesis proposes that prey can reduce their risk by minimizing the area around which all points in that area are closer to them than to another conspecific (i.e. by minimizing their ‘domain of danger’ (DOD)). This hypothesis assumes that an individual's predation risk is proportional to the size of its DOD; however, the relationship between risk and proximity to conspecifics may depend on additional factors. Specifically, approaching conspecifics may be costly for prey that rely on crypsis because group formation increases detectability. Using plasticine model prey, we experimentally manipulated prey coloration as well as the DOD, and then tracked their ‘survival’ under natural field conditions. We found that an individual's predation risk increased with their DOD for conspicuous (red) prey, but decreased with the DOD in cryptic (green) prey. Our results are consistent with patterns in natural systems and indicate that the relationship between predation risk and DOD depends on additional factors like prey coloration.

1. Introduction

Ecologists and evolutionary biologists have long sought to explain the wide variation in animal grouping behaviour. Many proposed explanations centre on how group formation reduces an individual's risk of predation through mechanisms such as increased vigilance [1], predator confusion [2], risk dilution [3] or by enhancing aposematic signal efficacy [4,5]. The selfish herd hypothesis is another influential explanation which proposes that group formation can result from individual prey seeking to reduce their predation risk by moving closer to other individuals [6]. In so doing, individual prey minimize the area within which all points in that area are closer to them than to another conspecific (i.e. they minimize their ‘domain of danger’ (DOD)) [6,7]. This behaviour is ‘selfish’ because it reduces predation risk to that individual by increasing predation risk to the individual(s) it approaches. Unlike some other hypotheses for grouping behaviour, the selfish herd mechanism does not rely on inclusive fitness to confer a selective advantage to individuals that exhibit grouping behaviour [6]. Central to the selfish herd hypothesis is the assumption that an individual's risk of predation is proportional to the size of its DOD. By presenting groups of artificial seals to great white sharks, De Vos & O'Riain [8] provide the only robust test of this assumption in a natural system, and the extent to which it holds across a wider range of systems or contexts remains unclear. Further, researchers recently failed to detect selfish herd dynamics in birds under threat casting doubt on the broad applicability of the hypothesis [9].

While gregariousness can have many benefits, group formation carries costs, such as increased predation risk to individuals on the periphery [10,11], increased visibility of groups to predators [12–14] and reduced food availability [10]. Grouping should be favoured only when the costs of group formation (e.g. increased detectability) are exceeded by the benefits gained via individual or kin selection [5,12–14]. Yet, the costs and benefits of grouping behaviour may differ between cryptic and conspicuous prey. Cryptic prey rely on the protection afforded by colours and patterns that reduce their detectability, which can be undermined by an increase in predator detection rates when they form groups [14,15]. By contrast, conspicuous prey may not suffer similar increases in detectability following group formation [5], but should still benefit from processes such as risk dilution and minimizing their DOD.

Following this reasoning, predation risk would decline for conspicuous prey as they reduce their DOD as predicted by the selfish herd hypothesis, but should increase in cryptic prey that seek to reduce their DOD. In the natural world, variation in gregariousness is often accompanied by concurrent variation in prey conspicuousness, with cryptic prey tending to be solitary and conspicuous prey are more often forming groups [15–17]. Although a variety of evolutionary hypotheses can help explain these patterns, particularly as they relate to aposematic prey [12], clearly there is reason to expect that the relationship between the DOD and predation risk could depend on prey coloration (see also [18]).

We investigated the relationship between the DOD and predation risk using artificial caterpillars and tested whether this relationship differs between cryptic and conspicuous prey. Specifically, we experimentally manipulated the colour and spacing of plasticine caterpillars and tracked avian predation under natural field conditions. Caterpillars are a suitable system for such an experiment because they vary in both their conspicuousness and grouping behaviour [17,19,20], and insectivorous birds readily attack model caterpillars deployed in the field (e.g. [21,22]). We hypothesized that (1) the probability that a group of prey is attacked depends on both prey colour and how tightly spaced prey are within groups and (2) predation risk for individual prey would be related to their colour and DOD. Specifically, we predicted that (i) groups of conspicuous prey and groups that were more tightly spaced would experience higher attack rates and (ii) an individual's predation risk would increase with its DOD in conspicuous prey, but decrease with the DOD in cryptic prey.

2. Methods

(a) . Study site

Our experiment took place in Peterborough, ON, Canada, in a mixed deciduous forest. Potential predators of our models included several species of insectivorous birds observed during our experiment (e.g. Poecile atricapillus, Sitta carolinesis and Picoides pubescens; full list in the electronic supplementary material). Caterpillars similar to our models which were active when we conducted our study include members of Saturnidae (e.g. Actias luna, Antheraea polyphemus and Callosamia promethea), Sphingidae (e.g. Sphinx chersis and Eumorpha pandorus), Noctuidae (e.g. Acronicta clarescens and Noctua pronuba) among others. Air temperature during trial one and two and averaged 17̊C and 14̊C, respectively.

(b) . Field methods

Model caterpillars made from plasticine (40 mm × 10 mm) were created by hand and deployed along tree branches to test our hypotheses. Our experiment followed a 4 × 2 factorial design. Specifically, each tree received a single group of four caterpillars, following one of four prey spacing treatments (2, 4, 8 or 16 cm between individuals) and one of two prey colour treatments (green or red). Differences in prey spacing allowed us to establish prey with a variety of DODs. The colour treatments were selected to examine the effect of prey conspicuousness (green = cryptic, red = conspicuous), as has been done previously (e.g. [23–25]). Our characterization of green plasticine models as cryptic and red plasticine models as conspicuous from the viewpoint of insectivorous birds is supported by previous work (e.g. [22,26]). Further, human vision detects most of the relevant variation in colour within the visible range and is a valid proxy for avian colour perception [27,28].

While the DOD can be quantified in several ways, we arranged prey along tree branches so that the DOD could be manipulated and calculated along a single dimension. Specifically, we calculated the DOD as the linear distance within which the target prey is closer than any of the other prey items, up to a maximum of two prey body lengths on either side of the prey (i.e. a limited DOD). Each prey therefore had one of seven different DODs (6, 8, 12, 13, 14, 16 and 20 cm).

Prey were deployed as two 10-day trials (27 September–7 October 2022, and 14 October–24 October 2022), each with five replicates of each treatment (i.e. n = 320 prey total). Between the two trials we left a 10-day rest period to avoid possible acclimation effects in the predator community. Treatment was assigned randomly to each tree, and trees with groups of prey were separated by no less than 1 m. The tree species we used were Fagus grandifolia, Carpinus caroliniana and Ulumus sp. Models were deployed at least 15 m away from hiking trails on branches that were at least 64 cm long and between 1 and 2 m from the ground. Models were checked daily between 12.00 h and 14.00 h and considered attacked when birds left beak imprints on the model. Attacked models were photographed and immediately replaced with another model of the same treatment to maintain a constant DOD for all prey throughout the experiment.

(c) . Data analysis

We used Cox proportional hazards regression to analyse patterns of survival. This approach uses a continuous measure of survival as the response variable and has been widely used to analyse the survival of model prey deployed in the field (e.g. [23,29,30]). Separate models were created to evaluate ‘survival’ at the group level (i.e. time until a group member is attacked) and ‘survival’ of individual prey. Each analysis was stratified by trial to account for possible differences in baseline hazard. We included survival data from prey that were added to replace attacked prey. Prey not attacked on the final day of each trial were censored at that time. The group-level analysis tests whether prey colour, spacing or their interaction, influenced the probability that a group was attacked (hypothesis 1). The individual-level analysis tests whether the prey colour, DOD or their interaction influenced the survival of individual prey (hypothesis 2). Spacing and DOD were treated as continuous variables. All analyses were conducted in R v.4.0.1 [31], using the survival package [32]. The assumption that hazard functions are proportional over time was tested using the cox.zph function.

3. Results

In total, 56 individual prey were attacked over the course of our experiment (24 green, 32 red), reflecting attacks on 55 prey groups (24 green, 31 red). More individual green prey were attacked when group spacing was tight, and more red prey were attacked when group spacing was wide (χ² = 8.20, d.f. = 3, p = 0.042).

We found no evidence to indicate that colour, spacing or their interaction influenced the time until a group received an attack (table 1, figure 1). At the individual level, the main effects of colour and DOD were not significant (p > 0.05, table 1); however, we detected a significant colour × DOD interaction reflecting colour-dependent changes in hazard as the DOD increased (z = 2.01, p = 0.042; table 1, figure 2). Specifically, red prey experienced an approximately 5% increase in risk of attack with every 1 cm increase in their DOD (hazard ratio = 1.045), whereas green prey experienced an approximately 7% reduction in hazard with every 1 cm increase in their DOD (hazard ratio = 0.928). Correspondingly, red prey were more likely to be attacked when they were on the edge of a group, whereas green prey were more likely to be attacked when they were in the centre of tightly spaced groups (figures 1; electronic supplementary material, figure S1). A separate Cox proportional hazards model found that colour, position within the group (i.e. inside versus edge), and the colour × position interaction did not significantly predict differences in survival (all p > 0.10, electronic supplementary material, table S1).

Table 1.

Output from Cox proportional hazards models evaluating ‘survival’ of red or green model prey affixed to trees in the field. Separate analyses were conducted to evaluate predictors of survival for prey groups and individual prey. The colour variable represents the change in risk for red prey relative to the reference level (green prey).

	coefficients	hazard ratio	lower 95% CI	upper 95% CI	z	p
groups
colour (red)	−0.359	0.698	0.274	1.780	−0.752	0.45
spacing	−0.029	0.971	0.899	1.050	−0.739	0.46
colour × spacing	0.080	1.083	0.980	1.197	1.559	0.12
individuals
colour (red)	−1.291	0.275	0.056	1.344	−1.595	0.11
domain of danger	−0.075	0.928	0.852	1.011	−1.711	0.087
colour × domain of danger	0.118	1.126	1.005	1.261	2.039	0.042

Figure 1.

Examples of model prey deployment in the field; (a) depicts the green (cryptic) prey treatment with 2 cm spacing between individuals. Red lines illustrate the domain of danger for each prey item; (b) depicts the red (conspicuous) prey treatment with 2 cm spacing between individuals. The inset image depicts an ‘attack’ by an insect-eating bird on a green model.

Figure 2.

(a,b) Survival plots illustrating the survival time (hours) for groups of green (cryptic) versus red (conspicuous) prey from one of four different prey spacing treatments. (c,d) Survival plots comparing the survival probability over time (hours) for red and green prey in each of seven different ‘domain of danger’ treatments. (e,f) Survival plots comparing the survival probability over time (hours) for red and green prey on the inside or edge of a group.

4. Discussion

We found opposing relationships between predation risk and the DOD, with only conspicuous prey showing the positive relationship expected under the selfish herd hypothesis. The use of artificial prey enabled us to eliminate possible effects of group vigilance and predator confusion, and avoid other confounding factors related to behavioural and phenotypic variation among prey (see also [8]). In our experiment, prey colour and spacing did not appear to influence attack rates on groups of prey; however, whether the DOD had a positive or negative effect on an individual's predation risk depended on prey colour. By demonstrating that the effect of grouping behaviour on predation risk is not independent of prey coloration, our work illustrates how natural selection can shape distinct suites of defensive traits among prey types.

Previous attempts to evaluate whether the DOD governs an individual's risk have grappled with the fact that targeted predation of peripheral prey can generate a similar pattern. If an individual's risk of predation is more strongly impacted by its position within a group than its DOD per se, this could argue against the selfish herd mechanism. Using a Daphnia–stickleback system, Milinski [18] found that predation risk to singleton prey (strays) increased as the density and conspicuousness of an adjacent prey group increased. Similarly, we found that when prey were conspicuous more peripheral individuals were attacked, but when prey were cryptic more attacks were directed at the centre of tight groups (electronic supplementary material, figure S1). Importantly, supplementary analysis failed to detect an effect of position on survival, indicating that the patterns observed here were better explained by colour-dependent variation in predation risk related to differences in their DOD.

Neither prey colour nor spacing strongly determined whether a group of prey was attacked. Jackson et al. [14] similarly found that the degree of prey clustering did not significantly influence detection. Interestingly, these authors also found that horizontally oriented groups were easier to detect than circular or vertically arranged groups, and that groups of four prey were detected quicker than smaller groups, with further increases in group size having little effect on detection ([14], see also [5]). Our prey were arranged as horizontal groups of four which may have maximized group detectability. Interestingly, Ioannou et al. [33] found that both densely packed groups of prey and densely packed areas within prey groups were more conspicuous resulting in greater targeting of these prey than expected under the selfish herd hypothesis. Regardless, previous work has shown that cryptic individuals have lower detectability than groups of cryptic or conspicuous individuals [14–16]. As a result, we should expect predation risk in cryptic prey to be lowest when they are distant from conspecifics, in contrast with the expectations of the selfish herd hypothesis.

Our results suggest that natural selection could generate the observed pattern of solitary prey tending to be cryptic and conspicuous prey frequently living in groups, even in the absence of kin selection, group defence, or reinforcement of aposematic signals [14–16]. Yet, some cryptic prey do form groups, indicating that additional benefits from group formation can influence the optimal strategy. For example, a recent study found that a cryptic fish (Psuedogobius sp.) responds to alarm cues by reducing their distance to conspecifics in order to transmit social information about predation risk, despite being a non-shoaling species with limited social attraction to conspecifics [34]. It may be that socially transmitted information about predation risk is more valuable in mitigating risk than reducing proximity to conspecifics, even for some cryptic prey [35]. By contrast, a solitary lifestyle may minimize predation risk for cryptic prey that have limited ability to perceive temporal variation in predation risk [14], or cannot rapidly escape or defend themselves following detection [36]. Clearly, the relationship between predation risk and grouping behaviour is context-specific, as was similarly suggested by researchers who failed to detect selfish herd dynamics in free-ranging birds [9]. We acknowledge that our results could be affected by the previous experience of birds, their perception of models as caterpillars versus fruit, and time of year. Future work should continue investigating how the relationship between the DOD and predation risk varies with additional traits of the prey, predators and environment in which they interact.

Ethics

This research was reviewed and approved by the Trent University Animal Care Committee (protocol: 26657).

Data accessibility

Data and code are available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.8kprr4xr5 [37].

The data are provided in the electronic supplementary material [38].

Authors' contributions

H.P.: conceptualization, data curation, formal analysis, investigation, methodology, project administration, writing—original draft and writing—review and editing; D.B.: methodology, supervision and writing—review and editing; T.J.H.: conceptualization, data curation, formal analysis, investigation, methodology, project administration, resources, supervision, validation, visualization, writing—original draft and writing—review and editing.

All authors gave final approval for publication and agreed to be held accountable for the work performed therein.

Conflict of interest declaration

We declare we have no competing interests.

Funding

We received no funding for this study.