Group size adjustment to ecological demand in a cooperative breeder

1. Introduction

In cooperatively breeding animals subordinates help raise offspring produced by dominant breeders [1–3]. Subordinates contribute to many different tasks such as cooperative hunting and foraging [4–6], territory defence and maintenance [7–9], sentinel behaviour [10,11], and direct brood care such as provisioning [12–14], guarding of young [15–18], and cleaning eggs and larvae [19,20]. This can increase the fitness of the breeding individuals, for instance, by raising offspring production [2,3,19,21–24]. The mere presence of subordinate group members can generate positive fitness effects on other group members as well, for instance, by dilution effects, predator confusion and deterrence [25–27]. The different fitness benefits accrued to dominant and other group members by subordinate helpers are not mutually exclusive.

Subordinates can also impose costs to breeding individuals, for instance by participating in reproduction and competing for resources, which can reduce reproduction or growth of breeders [18,28–30]. The cost–benefit ratio of the presence of subordinates in the group depends strongly on the environmental conditions [19,31,32]. For example, if the subordinates' contribution to territory defence provides a benefit to breeders, subordinate group members are more beneficial to have under high risk of predation or competition for territories. Dominant individuals, which often have control over group size, can strategically adjust group size to changes in the cost–benefit ratio by evicting subordinates from the group if they become too costly [31,33,34]. For example, in several cooperatively breeding mongooses, dominant females often expel pregnant subordinate females as they impose high costs particularly to the dominant female [28,33,35].

While the regulation of group size by dominant breeders through eviction of subordinates has been commonly observed in different cooperatively breeding species [31,33,36], the opposite possibility of extending cooperative groups by allowing immigration into the group if required by environmental conditions has been scarcely documented. Evidence that dominant breeders accept additional helpers more readily with increasing benefits of help exists from pied kingfishers (Ceryle rudis), where experimental clutch enlargement increased helper presence [37]. An opposite regulatory effect was observed in the clown anemonefish (Amphiprion percula), where dominant group members prevent immigration when the group is saturated [36]. Indirect evidence for group size adjustment to demand exists from baywings (Agelaioides badius), where more helpers were present when nests were parasitized by cowbirds (Molothrus spec.), which resulted in a higher begging intensity in the nest [38]. In the cooperatively breeding cichlid, N. pulcher, evicted offspring can be reaccepted when competition for the territory is experimentally increased, suggesting that breeders in this species are able to estimate their need for help [31]. Hitherto it is unknown, however, whether cooperative breeders respond to variation of predation risk by adjusting their acceptance of alien immigrants into the group. An effect is expected given that one major benefit of additional group members results from their contribution to territory defence [7,23,31] and dilution and predator confusion effects [25,26,39]. Neolamprologus pulcher provides excellent opportunities to investigate experimentally the response of dominant breeding individuals to changes in their cost–benefit ratio that might be associated with the presence of additional group members. It breeds in cooperative groups of up to about 30 individuals [7,39,40]. Smaller group members are queueing for breeding positions in sex-specific hierarchies or for opportunities to disperse into neighbouring territories [41–43]. Subordinates of both sexes and various sizes participate in brood care by cleaning and fanning the eggs [19,44], in territory defence against predators, space competitors and conspecific intruders [7,19,31,45], as well as in territory maintenance ([19], for review see [46]). Thereby, helpers specialize on different tasks depending on their body size [47]. Helper presence enhances survival of fry in the territory [23] and allows the breeder female to reduce energy investment and to produce larger clutches [19,48]. Nevertheless, helpers also impose costs by reducing growth rate of female breeders [30] and sometimes participating in reproduction, which can lead to eviction of costly subordinates from the territory [18,29,44].

Here, we manipulated perceived risk of predation for groups of N. pulcher to test whether this affects acceptance of an additional, unknown and unrelated subordinate in their territory. We exposed experimental groups either to predators of juvenile and adult fish (Lepidiolamprologus elongatus) or eggs and larvae (Telmatochromis vitattus). We predicted that the propensity to accept further helpers rises with increasing predation pressure. Specifically, we made two diverging predictions contingent on the type of benefit breeders might attain from additional group members; (i) if breeders mainly benefit from ‘safety-in-numbers’ effects (dilution and predator confusion), enhanced immigrant acceptance should be confined to increased risk of predation resulting from large predators that prey on fish, and it should be largely independent of immigrant size; (ii) if breeders mainly benefit from the contributions of subordinates to territory defence, they should generally accept immigrants when predation pressure is increased, also when this includes predators of eggs and larvae. Egg predators do not prey on fish of breeder size and accordingly, breeders would not benefit from accepting immigrants if the major benefit derived from additional group members is risk dilution. Thus, immigrant acceptance in the egg predator treatment should be raised only if their active contribution to territory defence yields fitness benefits to the breeders. In control trials, N. pulcher groups were exposed either to no intruders at all or to strictly herbivorous cichlids that would not cause benefits from group augmentation neither by risk dilution nor from enhanced territory defence.

2. Material and methods

(b) Experimental set-up

The experiment was conducted in 200l tanks at the Ethologische Station Hasli, Institute of Ecology and Evolution, University of Bern, Switzerland, between February and July 2011 under the license 16/09 of the Veterinäramt Bern. Experimental 200 l tanks (100 × 40 × 50 cm) were subdivided into three compartments: a main compartment (60 cm length) inhabited by a pair of breeders, an immigrant compartment (15 cm length) and a stimulus compartment (25 cm length) containing the respective stimulus fish (figure 1a).The main compartment was separated from the helper compartment by a clear partition and contained four flower pots halves as shelters. The stimulus compartment was separated by an opaque partition to prevent visual contact between stimulus fish and N. pulcher. In the middle of the partition was a sliding door connecting the stimulus compartment to a clear stimulus tube (50 cm length and 14.5 cm diameter), covered by a net on one end. This stimulus tube reached into the centre of the main compartment to allow the stimulus fish to swim into the territory while preventing direct physical contact between stimulus fish and N. pulcher. The immigrant compartment contained three small flower pot halves and a semi-opaque plastic bottle suspended next to the surface as an additional hide. The stimulus compartment contained a shelter to reduce stress of the stimulus fish.

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3. Results

(a) Acceptance of immigrants in groups

The probability of being accepted as a subordinate in the territory depended on the treatment. Immigrants in the fish predator and egg predator treatments experienced a higher probability of being accepted as group members compared with the two control treatments (figure 2, table 1a). The acceptance rate in the fish predator treatment did not differ significantly from the acceptance rate in the egg predator treatment. Furthermore, the two controls did not differ significantly from each other (figure 2, table 1a). Besides the treatment, the difference between female body size and immigrant body size influenced the probability of acceptance as a group member (figure 2, table 1a); immigrants with a large size difference to the breeder female were more readily accepted. The absolute body size and the difference in body size between male breeder and immigrant had no influence on the probability of acceptance (both p > 0.1).

Table 1.Statistical models for (a) the acceptance of subordinates (N = 100), (b) aggression against subordinates (N = 99), the attacks of (c) males (N = 75), (d) females (N = 75) and (e) accepted immigrants (N = 38) against predators. See §2 for explanation for diverging sample sizes.

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	estimate ± s.e.	z-value	p-value
(a)
empty control (intercept)	−2.43 ± 0.94	−2.60	<0.01
herbivore	0.03 ± 0.63	0.05	0.96
fish predator	1.58 ± 0.69	2.28	0.02
egg predator	1.66 ± 0.69	2.40	0.02
fish predator versus herbivore	−1.54 ± 0.64	2.41	0.02
fish predator versus egg predator	0.08 ± 0.69	0.11	0.91
egg predator versus herbivore	−1.62 ± 0.65	-2.51	0.01
difference SL female-immigrant	0.08 ± 0.04	2.16	0.03
(b)
male breeder (intercept)	1.04 ± 0.19	5.58	<0.01
female breeder	−0.06 ± 0.10	−0.60	0.55
status (evicted)	0.72 ± 0.22	3.29	<0.01
sex*status (evicted)	−0.24 ± 0.12	−1.96	<0.05
(c)
fish predator (intercept)	3.19 ± 0.47	6.86	<0.01
egg predator	−1.54 ± 0.67	−2.29	0.02
herbivore	0.42 ± 0.60	0.69	0.49
egg predator versus herbivore	1.95 ± 0.62	−3.16	<0.01
(d)
fish predator (intercept)	1.50 ± 0.43	3.50	<0.01
egg predator	0.16 ± 0.60	0.26	0.79
herbivore	2.22 ± 0.55	4.06	<0.01
egg predator versus herbivore	2.06 ± 0.55	−3.78	<0.01
(e)
fish predator (intercept)	−1.60 ± 0.85	−1.89	0.06
egg predator	4.26 ± 1.03	4.12	<0.01
herbivore	1.51 ± 1.12	1.34	0.18
egg predator versus herbivore	−2.75 ± 0.94	2.91	<0.01

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(b) Territory defence

Accepted immigrants contributed most in territory defence against egg predators and showed very low contributions to territory defence against fish predators and herbivore intruders (figure 3; table 1e). Male breeders attacked fish predators and herbivore intruders significantly more often than egg predators, whereas female breeders attacked herbivore intruders significantly more often than fish or egg predators (figure 3, table 1c, d).

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4. Discussion

Our data show that the exposure of N. pulcher groups to predators of eggs, larvae, juveniles and adults raises the acceptance rate of previously unknown and unrelated individuals into their group. This is likely to be an adaptive response to enhanced predation pressure. In the case of fish-eating predators, breeders in larger groups might enjoy the advantage of common territory defence and increased dilution effects [39,60,61]. However, the contribution of the accepted subordinates to territory defence against fish predators was low and only marginally significant. This suggests that the main benefits breeders gain from accepting immigrants of this size in the fish predator treatment arise from risk dilution or predator confusion effects, which is consistent with correlative data from the field [34]. In contrast, when predation on eggs is concerned, such dilution effects cannot occur. Instead, breeders might benefit from an increase in defence against egg predators by the accepted immigrants, as helpers specialize in such defence also in the field [7,47]. Indeed accepted immigrants contributed to defence against egg predators more than against any other type of intruder. We suggest that these two mechanisms, joint predator defence and risk dilution, both yield substantial fitness benefits of additional group members to the dominant breeders. These benefits outweigh the costs that additional group members may cause to breeders, such as enhanced brood parasitism, cannibalism and growth reduction [18,19,30].

An alternative explanation to deliberately enhanced immigrant acceptance by breeders could be that immigrants were more eager to stay in the territory under high perceived predation pressure. However, our data suggest that increased immigrant acceptance was rather caused by a strategic decision of the breeders: first, immigrant acceptance was explained by lower aggression rates from breeders towards immigrants. Second, the probability of immigrant acceptance was observed to be high in the egg predator treatment, whereas, for an immigrant, only a fish predator enhances the immediate benefit of being accepted in a safe territory.

Egg predators were presented in this experiment at a time when the breeding pair had not yet spawned. This implies that at the time when the breeders decided about immigrant acceptance, the egg predators had no possibility to hamper N. pulcher reproduction. Nevertheless, the egg predator treatment raised immigrant acceptance to the same level as in the fish predator treatment. This suggests that breeders of this species might be able to anticipate a potential future threat and adjust their behaviour strategically to maximize fitness in the future rather than at the time of the decision to accept or repel an immigrant. This process seems to resemble future planning as shown in birds and apes [62,63], but further experiments are needed to unravel the mechanisms underlying this seemingly anticipatory behaviour and conclusively rule out alternative explanations.

Strategic adjustments of group size by immigration and eviction are particularly likely to be important in cooperative systems with task specialization, because individuals engage in divergent tasks that can be of different importance under certain ecological circumstances [47]. However, this argument holds only in social systems where direct benefits to helpers provide an important incentive to help. Cooperative breeders matching these criteria are found across many taxa including fish (size-dependent task specialization [7,47]; birds (age-dependent engagement of helpers in incubation and provisioning of nestlings) [2,64]; social mammals (age-dependent polyethism [65] or division of labour [66]); and social insects (division of labour [67,68]). Recent evidence suggests that direct fitness benefits might be more important than previously thought, even among primitively eusocial insects [69,70].

Previous studies in cooperatively breeding birds suggest that the acceptance of subordinate group members can be contingent upon provisioning demands of nestlings [37,38]. Furthermore, agonistic interactions with rivalling conspecifics can influence sociability [71,72] and cooperative propensity in humans [73] and other animals. In the cooperatively breeding green woodhoopoe (Phoeniculus purpureus), for instance, more affiliative behaviour is directed from breeders to subordinates when they move into zones of their territories where aggressive encounters with rival groups are more frequent [74]. In N. pulcher, increased competition by conspecifics and heterospecifics for the territory, which includes shelters, breeding substrate and food for young, has been shown to affect aggression from breeders towards subordinate group members and to facilitate reacceptance of previously evicted helpers [31]. This apparent effect of resource competition on group stability impinges on group size like the incorporation of alien conspecifics into the group as demonstrated in our study. However, divergent proximate and ultimate mechanisms underlie these different group size adjustments. In the experiments of Taborsky [31], familiar offspring of the pair that had been recently expelled were allowed access to the territory again when space competitors were introduced; both individual and kin recognition have been demonstrated in N. pulcher [75,76]. At the ultimate level, such sharing of resources and tasks between breeders and offspring may be explained by kin selection. In contrast, there is no scope for kin selection in our study as the presented conspecifics were neither related nor familiar to the breeders. Furthermore, the ecological challenge we used was predation pressure on offspring or adults. Predation risk as an ecological cause of the acceptance of alien immigrants into groups of cooperative breeders was hitherto unknown. We argue that strategic group size adjustments to ecological requirements might be more common than appreciated. More generally, the effects of predation pressure on social interactions might be much more important than currently acknowledged.

Apart from perceived predation risk, the size difference between female breeder and the potential immigrant influenced the probability to accept a helper, whereas absolute immigrant size and the relation to the size of the male breeders had no influence on the probability of being accepted in the territory. This corroborates results from previous studies suggesting that the potential costs for breeders caused by subordinate group members increase with the latter's size [19,30,31,44]. Subordinates in our experiment were randomly chosen from a pool of fish on the verge of sexual maturation and therefore included both sexes. This might suggest that costs of subordinates are not primarily due to female–female competition as shown in other cooperatively breeding vertebrates [77,78]. Instead, regardless of the sex of the subordinates, individuals that are only slightly smaller than female breeders might induce higher potential costs to the pair, including for example an increased risk of egg cannibalism, as the submissive status of large helpers is an important precondition for them to care for eggs instead of eating them [79]. Unlike in cooperatively breeding mammals, where eviction is under female control [33,77], in N. pulcher both males and females participate in regulating group size [80]. Generally, the potential costs caused to breeders by opposite-sex subordinates are presently not well understood in cooperatively breeding vertebrates.

It seems surprising that the herbivore intruders were attacked very often by the pair, especially by female breeders. It has been shown that in N. pulcher attack rates are contingent on the risk individuals face when defending the territory [31,45]. This might be responsible for the high attack rates observed in breeders: as the risk is much smaller when attacking a herbivore than a fish predator, high attack rates on these intruders might reflect a low cost, low benefit strategy, as the risk of injury is probably negligible. The high attack rates against herbivore intruders might provide some insight into the cognitive mechanisms involved in the experimentally enhanced immigrant acceptance, implying that simple ‘attack-counting’ of breeders to determine the need for help is not responsible for the acceptance of additional group members. Rather, it seems that the presence of predators per se, regardless whether a risk to current group members or future eggs and larvae, raises the tolerance towards subordinate conspecifics.

It is yet unclear whether the recognition of threat is innate or learned. However, the fact that the fish showed adequate responses to predators even though all N. pulcher used in our experiment had never had direct contact to predators and herbivores before suggests that predator recognition in this species is innate and independent of learning. It is presently unknown which cues N. pulcher use to recognize predators. In the experiments both visual and olfactory cues could be used. If olfactory cues were important, they cannot include Schreckstoff or the smell of digested conspecifics (cf. [81]), as no conspecific was harmed by a predator during the experiment and all stimulus fish were fed on a flake food diet. This topic will be scrutinized in future studies.

5. Conclusions

Environmental conditions determine the cost–benefit ratio of accepting additional group members. This study shows that social interactions in a highly social vertebrate are contingent on the perceived risk of predation. Specifically, our experiment suggests that in N. pulcher, (i) enhanced predation risk increases the propensity to accept unknown and unrelated immigrants; (ii) predation pressure on group members and eggs has similar effects despite diverging benefits derived from additional group members; and (iii) immigrant acceptance is raised also when the potential benefit from receiving additional help (i.e. defence against potential predators of eggs and larvae) occurs only in the future.