Cleaning wrasse species vary with respect to dependency on the mutualism and behavioural adaptations in interactions

Interspecific mutualisms are an essential feature of life on earth, yet we know little about their evolution and stability. In many mutualisms several species are available as partners, raising questions about the similarity in function and behavioural repertoire depending on the partner species. Furthermore, variation between species in the quantity and quality of interactions resulting in variation in payoffs may allow us to infer the potential evolutionary origin of a multispecies mutualism complex. We addressed these issues in the marine cleaning mutualism, in which so-called 'cleaners' remove ectoparasites from so-called 'client' reef fish. We measured several parameters concerning the quantity and quality of cleaning interactions in six sympatric cleaner wrasse species. We found significant variation between cleaner species with respect to client diversity, the number of interactions with predatory clients, the duration of interactions, the frequency of client jolts as a correlate of 'cheating' by cleaners, and behaviours used for manipulation of client decisions. Exploratory correlations between cleaner species' dependency and our variables of interest suggest that cleaning originated as a conflict-free by-product mutualism and evolved towards more sophisticated behaviours, including strategic behaviours for interactions with predators, cheating and manipulation specifically adapted to the client type.

Influence of the number of queens on nestmate recognition and attractiveness of queens to workers in the Argentine ant, Iridomyrmex humilis (Mayr)

To investigate the influence of the number of queens per colony on nestmate recognition in Iridomyrmex humilis, comparative assays were performed to study the attraction of workers to queens. These assays demonstrated that a phenomenon of recognition is superimposed on the attraction of workers to queens. Workers could discriminate non-nestmate queens from their nestmate queen to which they were significantly more attracted. This discrimination is probably based on the learning by workers of queen and colony odour. The level of attraction of workers to non-nestmate queens was similar in monogynous and polygynous colonies, whereas the level of attraction of workers to nestmate queens was significantly lower in polygynous colonies. This difference in the level of attraction of workers to nestmate queens almost certainly resulted from a lower efficiency in nestmate recognition in polygynous colonies. It is hypothesized that the mixture of several pheromonal sources produced by less related individuals in polygynous colonies may result in a less distinct colony odour than in monogynous colonies. The results are discussed with regard to some implications of polygyny and particularly to the loss of intercolonial aggression in I. humilis as well as in other polygynous ant species

Effect of mating history on gender preference in the hermaphroditic snail physa acuta

Several internally fertilizing hermaphroditic animals can only perform one sexual role at a time. In such species, two individuals that engage in a copulation may have different interests in acting as male or female. A gender choice must be made which, if both individuals have the same preference, may give rise to a severe sexual conflict. Here we tested the hypothesis that gender choice could be influenced by mating history, using the freshwater snail, Physa acuta. We recorded the copulatory behaviour of 240 pairs composed of a focal individual and a partner, each either short- or long-isolated. We found that the time to the first copulation was unaffected by isolation status, suggesting that first contacts in this species are random processes. In contrast, the duration of copulations and the frequency of rejection behaviours suggested that individual gender preference switches from male biased to female biased as isolation increases. In addition, snails rejected copulations more frequently when presented to a partner with the same isolation status. Reciprocity, measured as the rate of gender swapping between the first and second copulations, was high irrespective of gender status. We suggest possible evolutionary causes for this gender preference switch and discuss its potential importance in natural population as well as its consequences for the maintenance of hermaphroditism

Social organization and mating system of free-ranging, greater white-toothed shrews, Crocidura russula

Indirect evidence from trapping suggests that Crocidura russula is less solitary and territorial than other shrews. To study the social organization and mating system, free-ranging adult and juvenile C. russula were tracked simultaneously throughout the year using a radioactive tracking technique. Coincident rest, coincident activity and home range overlap were measured. During winter, all individuals used the same communal nest and spent on average 84% of their total rest in coincident rest. This led to a large home range overlap (52% on average). Coincident activity was low (2% on average). At the onset of the reproductive season the females became, territorial and shared their nest with only one male. During pair formation, coincident activity and home range overlap were significantly greater between than within sexes. The social organization of C. russula appeared to be strongly influenced by season and differed in this respect from the other species in the genus Sorex which are territorial throughout the year.

Melanin-based colouration predicts aggressiveness and boldness in captive eastern Hermann's tortoises

Although body colouration is often used in social interactions, few studies have tested whether colouration is linked to a suite of behavioural traits. In the present study, we examined whether among captive adult male Eastern Hermann's tortoises (Eurotestudo boettgeri) behavioural patterns covary with eumelanic colouration of the shell. Dark eumelanic males were more aggressive in male-male confrontations and bolder towards humans. These relationships were independent of body size and ambient temperature. Activity level and exploration were not significantly associated with colouration. We conclude that at least in captivity shell colouration predicts agonistic behaviour towards conspecifics and fearfulness towards human (i.e. boldness).

Wood ants protect their brood with tree resin

Social insects use multiple lines of collective defences to combat pathogens. One example of a behav- ioural group defence is the use of antimicrobial plant compounds to disinfect the nest. Indeed, wood ants collect coniferous tree resin, and the presence of resin in their nest protects them against fungal and bacterial pathogens. Many questions remain on the mechanisms of resin use, including which factors elicit resin collection and placement within nests. Here, we investigated whether the presence of brood induces Formica paralugubris workers to collect more resin, and whether the workers preferentially place resin near the brood. We also tested whether the collection and placement of resin depends on the presence of the fungal entomopathogen Beauveria bassiana. Workers brought more resin to their nest when brood was present, and preferentially placed the resin near the brood. In contrast, workers did not increase resin collection in response to exposure to B. bassiana, nor did they place resin closer to contaminated brood or contaminated areas of the nest. This lack of response may be explained by a limited effect of resin against the germination and growth of B. bassiana in vitro. Overall, our main result is that woods ants actively position resin near the brood, which probably confers prophylactic protection against other detrimental microorganisms.

Melanin-based colouration predicts natal dispersal in the barn owl, Tyto alba

Searching for a suitable breeding site is an important decision in the life of most animals. The decisions where to settle and how far to travel before doing so depend on many factors. Individual differences in dispersal distance could result from different strategies (e.g. specialists versus generalists), which might result in similar reproductive success in different habitats, or different competitive abilities to acquire a territory close to the natal site. The barn owl is polymorphic in melanic coloration, which is associated with many physiological and behavioural traits such as habitat choice, stress response and docility, raising the possibility that the coloration is also related to dispersal. We studied natal dispersal (from rearing site to site of first breeding attempt) and breeding dispersal (from one breeding site to the next) in barn owls using a long-term data set. Darker reddish individuals moved further than paler individuals during natal dispersal, but not during breeding dispersal. A cross-fostering experiment showed that the colour of the biological and foster parents had no influence on dispersal distance. The distance dispersed by parents and same-sex offspring was correlated, whereas natal and breeding dispersal were not repeatable within individuals, indicating that they are two different processes. Given that the distance travelled in natal dispersal appears to be heritable, the underlying genes might be coupled to those related to coloration. We discuss hypotheses to explain the potential adaptive function of the link between coloration and natal dispersal.

Nestling barn owls beg more intensely in the presence of their mother than in the presence of their father

Nestling begging behaviour may be an honest signal of need used by parents to adjust optimally both feeding rate and within-brood food allocation. Although several studies showed that mothers and fathers can be differentially responsive to nestling begging behaviour with one parent showing a stronger tendency to feed the offspring that beg the most, little information is yet available on whether offspring beg for food at different intensities from the mother than father. In the present study, we investigated in nestling barn owls whether the intensity of vocal begging behaviour in the presence of the mother and in the presence of the father is different. A difference is expected because reproductive tasks are divided between the sexes with fathers bringing more food items to the nest than mothers. The results show that although mothers transfer their prey item to one of the offspring more rapidly than fathers once in their nestbox, nestlings begged more intensely in the presence of their mother than in the presence of their father. To our knowledge, this is the first empirical evidence that offspring vocalize to different levels in the presence of their mother than in the presence of their father.

Corticosterone mediates the condition-dependent component of melanin-based coloration

The handicap principle of sexual selection theory states that colourful phenotypic traits signal aspects of individual quality because only individuals in prime condition can afford to produce and bear conspicuous traits. Melanin-based pigments participate in the elaboration of many secondary sexual characters and, given their role in sexual selection, melanin-based coloration may therefore honestly reject individual quality. Although the expression of melanism is usually under genetic control, in some species it is condition dependent. However, the underlying physiological mechanism is yet unknown. Based on the negative feedback link between corticosterone and melanogenesis ( melanocortins, tyrosinase) in response to stressful environmental factors, we hypothesize that corticosterone mediates the condition-dependent component of melanism. This hypothesis predicts that stressful factors induce a rise in circulating corticosterone which inhibits the secretion of melanocortins and tyrosinase and in turn melanin production. We tested this prediction by manipulating the level of corticosterone at the time of melanin production in nestling barn owls, Tyto alba, a species showing heritable variation in the degree of phaeomelanism from reddish-brown to white. The finding that corticosterone-implanted nestlings produced feathers with less phaeomelanic coloration than placebo-implanted nestlings is consistent with the hypothesis that the environment-mediated reduction in the degree of melanism is, at least in part, caused by a rise in corticosterone. In species in which the expression of melanin-based coloration is condition dependent, we now need a test showing that individuals with less corticosterone and more melanin-based signals are individuals in better condition.

Vocal sib-sib interactions: how siblings adjust signaling level to each other

Game theory states that iterative interactions between individuals are necessary to adjust behaviour optimally to one another. Although our understanding of the role of begging signals in the resolution of parent-offspring conflict over parental investment rests on game theory implying repeated interactions between family members, empiricists usually consider interactions at the exact moment when parents allocate food among the brood. Therefore, the mechanisms by which siblings adjust signalling level to one another remain unclear. We tackled this issue in the barn owl, Tyto alba. In the absence of parents, hungry nestlings signal vocally to siblings their intention to contest vigorously the next, indivisible, food item. Such behaviour deters siblings from competing and begging when parents return to the nest. In experimental two-chick broods, nestlings producing the longest calls in the absence of parents, a signal of hunger level, were more successful at monopolizing the food item at the first parental feeding visit of the night. Moreover, nestlings increased (versus decreased) call duration when their sibling produced longer (versus shorter) calls, and an individual was more likely to call again if its sibling began to vocalize before or just after it had ended its previous call. These results are in agreement with the hypothesis that siblings challenge each other vocally to reinforce the honesty of sib-sib communication and to resolve conflicts over which individual will have priority of access to the next delivered food item. Siblings challenge each other vocally to confirm that the level of signalling accurately reflects motivation.

Queen acceptance in a socially polymorphic ant

A central question in social evolution is what processes regulate the number of breeders in each social group. Here, we tested whether differences in the rate of acceptance of new queens by resident workers could be a proximate cause explaining the coexistence of single- and multiple-queen colonies in an ant population. We found that Formica selysi workers discriminated against foreign (non-nestmate) queens, which contributes to maintaining the genetic integrity of the social group essential to kin selection. All the young and newly mated foreign queens introduced into experimental groups of workers died within 48 h. In contrast, workers frequently accepted young newly mated nestmate queens. The survival of nestmate queens was not significantly lower in groups of workers originating from single- queen colonies than in groups of workers originating from multiple-queen colonies. Finally, virgin queens had significantly higher survival than mated queens. Together, these results show that the maintenance of single-queen and multiple-queen colonies in the same population is unlikely to be caused by strong differences between the two types of colonies in their rate of acceptance of new queens by workers. They also suggest that the discrimination of queens by resident workers restricts the dispersal of foreign queens among colonies, but not the acceptance of additional nestmate queens.

Sibling competition and the risk of falling out of the nest

In birds, sibling competition encompasses several activities, one of which is jostling for position, that is, competing for the location in the nest where parents predictably deliver food items. We hypothesized that nestlings that compete by jostling for position may fall out of the nest either accidentally or because siblings push each other to reduce brood size. This hypothesis predicts that in a competitive environment needy nestlings trade-off the benefit of being fed against the cost of falling out of the nest. As a first attempt to evaluate this hypothesis, we experimentally manipulated the number of young per brood in the colonial Alpine swift, Apus melba. Nestlings fell out of their colony more frequently when reared in enlarged than in reduced broods. Because brood size manipulation affects not only the number of young per nest but also their body condition, we analysed an extended data set to disentangle these two factors. This analysis showed that, independently of brood size, nestlings in poor condition and those reared in broods where sibling differed markedly in weight were more likely to disappear from the colony. Nestling disappearance also occurred predominantly in nests close to the colony entrances. Although nestling swifts can wander in the colony and become adopted in neighbouring nests, we found no evidence that wandering per se increased the risk of falling out of the colony. Our study therefore highlights a novel cost of scramble competition.

Ectoparasite affects choice and use of roost sites in the great tit, Parus major

Many diurnal bird species roost at night in holes. As a regular visitor of a hole they are therefore a welcome host for several species of ectoparasites. The interactions of ectoparasites with the behaviour, life-history traits and population demography of their hosts are largely unknown. In the present study the effects of the haematophagous hen flea, Ceratophyllus gallinae , on the great tit's choice of winter roost site were investigated experimentally. Three experiments tested (1) whether great tits prefer a clean nestbox to one containing an old, but parasite-free nest, (2) whether they prefer a parasite-free nestbox to one infested with the haematophagous hen flea, and (3) whether they prefer not to use a nestbox when there is only an infested box available in their territory. In the first experiment there was no discrimination and both kinds of boxes were used equally often. In the second experiment the great tits clearly preferred to roost in the box without ectoparasites. In the third experiment a significantly higher proportion of the infested nestboxes were not used for roosting compared with the parasite-free boxes. Recently the validity of the conclusions drawn from nestbox studies where the naturally occurring detrimental ectoparasites are eliminated by the routine removal of old nests between breeding seasons has been questioned. This study shows that ectoparasites affect host behaviour and therefore lends support to that criticism.

Signalling by the cleaner shrimp Periclimenes longicarpus

Signals increase the fitness of a sender by altering the behaviour of receivers. For cooperative interactions biological market theory proposes that signalling strength may be linked to supply and demand. In this context, a recent laboratory experiment demonstrated that cleaner shrimps may advertise their service to client reef fish and that the advertisement is linked to hunger levels. We investigated signalling by the cleaner shrimp Periclimenes longicarpus in the field to test more detailed predictions of biological market theory. Shrimps often clapped with their pair of claws in response to approaching clients. In line with both theory and the previous study, the probability of clapping increased when the shrimps had been food deprived and clapping shrimps were more likely to clean than nonclapping individuals. However, we found no evidence for the market theory prediction that signalling was targeted specifically to visiting client species with the option to choose other cleaning stations. Instead, shrimps signalled more frequently towards predatory clients than towards nonpredatory clients. We conclude that the signal does not serve primarily to attract the choosy clients but to convey information about identity as preconflict management to avoid predation.