Sociality in New World hystricognath rodents is linked to predators and burrow digging

The importance of predation and burrow digging in explainingthe evolution of sociality is generally unclear. We focusedon New World hystricognath rodents to evaluate three key predictionsof the predation hypothesis. First, large-bodied surface-dwellingspecies will be more vulnerable because they are more detectable;thus sociality should be associated with body size. Second,surface-dwelling, diurnal species would be more vulnerable topredators than nocturnal species; thus sociality should be associatedwith the evolution of diurnality. Third, species living in openhabitats will be more vulnerable; thus sociality should evolvein species living in open habitats. Regarding the importanceof burrows, we tested if species that dig burrows can benefitfrom communal labor; thus, sociality should be associated withburrow digging. All traits had significant phylogenetic signal,thus comparative analyses should explicitly address this. Ina comparative analysis on independent contrasts we found thatsociality was correlated with body size (larger species weremore social), diurnality (diurnal species were more social),and burrowing (burrowing species were more social), but we foundno effect of overhead plant cover of habitat on sociality inhystricognath rodents. Somewhat different results were foundwhen we analyzed the raw data. Taken together, our results providesupport for a link between predation risk, burrow digging, andsociality in this group.     

Premating Behavior in the Subgenus Limia (Pisces: Poeciliidae): Sexual Selection and the Evolution of Courtship

A three-year field-study of Richardson's ground squirrels was conducted to assess whether alarm calling functions to warn close relatives (“kin selection” hypothesis) or manipulate conspecifics (a “selfish” hypothesis). S. richardsonii had distinct calls for terrestrial and aerial predators, and the responses of squirrels varied appropriately according to the context of calls, implying that calling conveyed correct information concerning the nature of the danger. Alarm calling elicited by naturally occurring encounters with potential predators during 454 h of observation, and by a thrown frisbee in 70 experimental trials, was not equally probable for all age/sex classes. Squirrels were most likely to call when they had offspring or siblings nearby, which is supportive of the hypothesis that alarm calling is maintained by kin selection. Adult males, residing in the vicinity of either their probable progeny or their nonlittermate half-siblings, were the most likely age/sex class to call during the lactation period when young were below ground and were most vulnerable. I conclude that alarm calling by Richardson's ground squirrels is nepotistic rather than manipulative.     

ECOLOGICAL DRIVERS OF ANTIPREDATOR DEFENSES IN CARNIVORES

Mammals have evolved several morphological and behavioral adaptations to reduce the risk of predation, but we know little about the ecological factors that favor their evolution. For example, some mammalian carnivores have the ability to spray noxious anal secretions in defense, whereas other species lack such weaponry but may instead rely on collective vigilance characteristic of cohesive social groups. Using extensive natural history data on 181 species in the order Carnivora, we created a new estimate of potential predation risk from mammals and birds of prey and used comparative phylogenetic methods to assess how different sources of predation risk and other ecological variables influence the evolution of either noxious weaponry or sociality in this taxon. We demonstrate that the evolution of enhanced spraying ability is favored by increased predation risk from other mammals and by nocturnality, but the evolution of sociality is favored by increased predation risk from birds of prey and by diurnality, which may allow for enhanced early visual detection. These results suggest that noxious defenses and sociality are alternative antipredator strategies targeting different predator guilds under different lighting conditions.     

Does sociality drive the evolution of communicative complexity? A comparative test with ground-dwelling sciurid alarm calls

While sociality has been hypothesized to drive the evolution of communicative complexity, the relationship remains to be formally tested. We derive a continuous measure of social complexity from demographic data and use this variable to explain variation in alarm repertoire size in ground-dwelling sciurid rodents (marmots, Marmota spp.; prairie dogs, Cynomys spp.; and ground squirrels, Spermophilus spp.). About 40% of the variation in alarm call repertoire size was explained by social complexity in the raw data set. To determine the degree to which this relationship may have been influenced by historical relationships between species, we used five different phylogenetic hypotheses to calculate phylogenetically independent contrasts. Less variation was significantly explained in contrast-based analyses, but a general positive relationship remained. Social complexity explained more variation in alarm call repertoire size in marmots, while sociality explained no variation in repertoire size in prairie dogs and no variation in phylogenetically based analyses of squirrels. In most cases, substantial variation remained unexplained by social complexity. We acknowledge that factors other than social complexity, per se, may contribute to the evolution of alarm call repertoire size in sciurid rodents, and we discuss alternative hypotheses. Our measure of social complexity could be used by other researchers to test explicit evolutionary hypotheses that involve social complexity.     

Anti‐Predator Signals in the Chaffinch Fringilla coelebs in Response to Habitat Structure and Different Predator Types

Many animals respond to the presence of predators with conspicuous signals such as alarm calling. These signals may aid the detection of the predator by conspecifics or may deter the predator from attack. The advantages of such signals may be dependent upon predator type and habitat type. We measured signalling behaviours (alarm calling and tail flicking) in foraging chaffinches in response to different predator models (hawk and pigeon control, cat and plastic box as control). In addition we measured responses to a cat model when chaffinches were foraging in different habitat structures (obstructed vs. open). There was no difference in the number of individual chaffinches alarm calling in obstructed vs. open habitat, but birds tail flicked more in open habitat, suggesting that tail flicking acts as a visual signal to the predator or conspecifics and therefore unlike auditory cues is influenced by habitat structure. Chaffinches were also more likely to tail flick in response to the cat model than the other three models. Our results are consistent with the idea that animals may respond to ground predators, which spend a large amount of time observing prey before attack, by using signalling behaviours, such as tail flicking and alarm calling. Further work on prey selection by predators is needed to separate the functions of signalling behaviour in response to predators.     

Effect of alarm calling by male Red‐winged Blackbirds on nestling begging and female provisioning behavior

ABSTRACT Nestling begging and parental provisioning can attract nest predators and reduce reproductive success, so parents and their offspring might be expected to respond adaptively by minimizing predator‐attracting cues when predators threaten nests. Male Red‐winged Blackbirds (Agelaius phoeniceus) are well known for their antipredator alarm calls that contain information about the approach of potential nest predators. We examined the begging behavior of nestlings and the provisioning behavior of females in response to antipredator alarm calls of males to test the adaptive response hypothesis. Playback experiments provided no evidence that alarm calls function to switch off vocal begging; nestlings were equally likely to beg vocally during playback and control periods. Video recordings showed that male alarm calling had no significant effect on inappropriate vocal begging (in the absence of an adult), but significantly reduced the incidence of spontaneous calling (in the absence of begging). Adult females responded to male antipredator alarm calls by delaying their provisioning visits. In addition, although having no significant effect on use of nest‐arriving calls by females, male alarm calling significantly reduced their use of nest‐leaving calls. We conclude that nestling and female Red‐winged Blackbirds respond to male alarm calls in ways that might reduce the risk of predation, but nestlings beg vocally when females arrive to feed them, regardless of male alarm calling, perhaps to avoid a competitive disadvantage with broodmates.     

Predator‐Associated Vocalizations in North American Red Squirrels (Tamiasciurus hudsonicus): To Whom are Alarm Calls Addressed and How do They Function?

Alarm vocalizations produced by prey species encountering predators can serve a variety of functions. North American red squirrels are a small-bodied mammal popularly known for producing loud, conspicuous alarm calls, but functional accounts of calling in this species are few and contradictory. We conducted research over a 3-yr period on a sample of 47 marked red squirrels in the foothills of the Canadian Rockies. We recorded the production of alarm calls during encounters with natural predators and in a series of simulated predator experiments. We tested for variation in call production patterns consistent with three traditional hypotheses concerning the conspecific warning functions of alarm calling: namely that they serve as warnings to kin, to potential mates, or to territorial neighbors with which callers have an established relationship. Patterns of calling did not provide clear support for any of these hypothesized functions. We consider several possible qualifications to our results. We also consider the possibility that conspicuous calls given by red squirrels during encounters with predators are directed at the predators themselves and function to announce their detection and possibly deter them. This possibility is consistent with additional life-history features of red squirrels including that they are a relatively solitary and territorial, food-hoarding species that produces the same conspicuous vocalizations in response to other squirrels intruding on their territory to steal cones. An important corollary of this account is that red squirrel alarm calls probably do not entail referentially specific messages about different types of predator, as proposed previously.     

Observed instances of alarm calling in the Cape Rockjumper

Here I give an account of alarm calls recorded during behavioural observations on Cape Rockjumpers (CRJs) and the potential predators observed nearby. I found CRJs did not produce alarm calls in the presence of Boomslang (a previously known predator of CRJ nestlings), whereas they did produce alarm calls in the presence of Rock Kestrels, which was unexpected as previous literature suggested Rock Kestrels do not prey upon CRJ. However, during field observations I witnessed a Rock Kestrel attack an adult CRJ, suggesting that Rock Kestrels may opportunistically prey upon CRJs. Further studies on site- and temporal-specificity in CRJs may lead to additional understanding of the flexibility of alarm calling in group-living species.     

Nepotistic alarm calling in the Siberian jay, Perisoreus infaustus

From a life history perspective, parents have an incentive to protect their reproductive investment, and so may provide care even after their offspring are independent. Such prolonged parental care could lead to postponed dispersal of the offspring and thereby facilitate the formation of kin groups. We tested whether alpha birds in Siberian jays protected their independent, retained offspring by giving alarm calls during simulated predator attacks. We compared the responses to predator attacks simulated by flying a hawk model over a dyad of birds on a feeder for dyads composed of an alpha bird and either a relative or a nonrelative. Alpha females were nepotistic in their alarm-calling behaviour, in that they called more frequently when accompanied by their retained offspring than by unrelated immigrants, but alpha males called indiscriminately. This difference in alarm calling could reflect dominance relationships in Siberian jay groups, because the presence of immigrants may be less costly to alpha males, but alpha females are more vulnerable to competition from immigrants. Alarm calls were usually given during escape, when both individuals in the dyad had left the feeding site. However, results of a playback experiment suggest that alarm calls conveyed information about danger and incited an immediate escape reaction. Our results indicate that alarm calling can be nepotistic, and that factors other than kinship influence alarm-calling behaviour. Nepotistic antipredator behaviours are benefits that offspring can gain only in their natal territory. Hence, in the absence of preferential treatment by their parents, offspring may be more likely to disperse and kin groups are prevented from forming.     

Night and day: the comparative study of strepsirrhine primates reveals socioecological and phylogenetic patterns in olfactory signals

Studies of chemical signals in vertebrates typically target single species; however, a broader understanding of olfactory communication may derive from comparative studies. We collected urine from 12 species representing most families of strepsirrhine primates--an excellent model clade because of variation in scent marking and socioecology. Using SPDE/GC-MS, we identified the volatile chemical composition of male and female urine from six 'urine marking' species and six glandular or 'non-urine marking' species. We found no sex differences, but as predicted, urine markers expressed the most chemically complex and distinctive urine. More distantly related species had more dissimilar urinary profiles, suggesting gradual signal evolution. Reconstructing ancestral chemical profiles revealed different evolutionary trajectories for urine and non-urine markers. We suggest that urine marking is an ancestral behaviour related to solitary, nocturnal living and that parallel evolutionary shifts towards greater reliance on derived glandular marking occurred in a family (Lemuridae) characterized by diurnality and sociality.     

Is Alarm Calling Risky? Marmots Avoid Calling from Risky Places

Alarm calling is common in many species. A prevalent assumption is that calling puts the vocalizing individual at increased risk of predation. If calling is indeed costly, we need special explanations for its evolution and maintenance. In some, but not all species, callers vocalize away from safety and thus may be exposed to an increased risk of predation. However, for species that emit bouts with one or a few calls, it is often difficult to identify the caller and find the precise location where a call was produced. We analyzed the spatial dynamics of yellow-bellied marmot (Marmota flaviventris) alarm calling using an acoustic localization system to determine the location from which calls were emitted. Marmots almost always called from positions close to the safety of their burrows, and, if they produced more than one alarm call, tended to end their calling bouts closer to safety than they started them. These results suggest that for this species, potential increased predation risk from alarm calling is greatly mitigated and indeed calling may have limited predation costs.     

Are Blackcaps (Sylvia atricapilla) defending their nests also calling for help from their neighbours?

One hypothesized function of conspicuous mobbing of intruders by bird nest owners is to attract neighbouring birds (“calling for help” hypothesis) or third-party predators (“attract the mightier” hypothesis). These may help the nest owners by distracting and/or attacking the mobbed intruder. To date, these hypotheses have been studied solely during the mobbing of predators. Here, for the first time, I have studied mobbing attraction in the context of brood parasitism. I experimentally tested the Blackcap (Sylvia atricapilla), a small passerine with a highly aggressive and conspicuous nest defence behaviour. I elicited the aggressive responses of Blackcaps by presenting stuffed dummies of the brood parasitic Common Cuckoo (Cuculus canorus) and controls near their nests. At 32% of the nests (n = 75), the responses of the Blackcaps to dummies attracted up to 15 birds per trial from 21 passerine species. Most of the attracted birds were heterospecifics and rarely participated in mobbing; thus the “calling for help” hypothesis was not supported. No potential predators of the Cuckoo were attracted despite them living in the study area and despite prolonged mobbing by Blackcaps; thus rejecting the “attract the mightier” hypothesis. I argue that this hypothesis is unlikely to apply to typical avian predators during nest predation acts because these only last for several seconds. The number of attracted birds was a positive function of the owner’s intensity of nest defence as measured by the rates of alarm calling but not visual cues (rates of attacks). Suitable and unsuitable Cuckoo hosts did not differ in their behaviour in the vicinity of defended nests. The observed pattern of the positive correlation between the intensity of nest defence and the number of attracted birds is most likely a proximate by-product of the conspicuous nest defence by Blackcaps (but may well be adaptive for recruiting neighbours themselves). Thus, the mobbing behaviour of the Blackcap is directed towards the brood parasite and not towards other audience predators or potential recruits to the mob.     

Male monkeys remember which group members have given alarm calls

Primates give alarm calls in response to the presence of predators. In some species, such as the Thomas langur (Presbytis thomasi), males only emit alarm calls if there is an audience. An unanswered question is whether the audience's behaviour influences how long the male will continue his alarm calling. We tested three hypotheses that might explain the alarm calling duration of male Thomas langurs: the fatigue, group size and group member behaviour hypotheses. Fatigue and group size did not influence male alarm calling duration. We found that males only ceased calling shortly after all individuals in his group had given at least one alarm call. This shows that males keep track of and thus remember which group members have called.     

Essay on Contemporary Issues in Ethology: Variation among Mammalian Alarm Call Systems and the Problem of Meaning in Animal Signals

Understanding the information conveyed by animal signals requires studies of both production and perception. It is important to determine the relationship between signal morphology and the circumstances of production, the way signaller behavior varies with motivational state and the role of context in mediating responses to signals. Alarm calls are well-suited to research of this type because they are widespread in birds and mammals and typically evoke unambiguous responses. We review studies of alarm calling in primates and ground-dwelling sciurid rodents, concentrating especially on whether these signal systems may be viewed as ‘functionally referential’, that is, as conveying sufficient information about an event for receivers to select appropriate responses. Comparisons of the physical, behavioral and habitat characteristics of these species suggest that incompatibility of the escape responses required to avoid different classes of predators may have been an important factor in the evolution of functionally referential alarm calls.     

To call or not to call: parents assess the vulnerability of their young before warning them about predators

Communication about predators can reveal the effects of both conspecific and heterospecific audiences on signalling strategy, providing insight into signal function and animal cognition. In species that alarm call to their young, parents face a fundamental dilemma: calling can silence noisy offspring and so make them less likely to be overheard, but can also alert predators that young are nearby. Parents could resolve this dilemma by being sensitive to the current vulnerability of offspring, and calling only when young are most at risk. Testing whether offspring vulnerability affects parental strategy has proved difficult, however, because more vulnerable broods are often also more valuable. We tested experimentally whether parent white-browed scrubwren, Sericornis frontalis, assessed brood noisiness when alarm calling near nests. When a model predator was nearby, parents gave more alarm calls when playbacks simulated noisy broods, yet brood noisiness did not affect adult calling when only a control model was present. Parents were therefore sensitive to the tradeoff between silencing young and alerting predators to the presence of nests. Our study demonstrates that receiver vulnerability can affect signalling decisions in species other than primates.     

Experimental study of alarm calls of the oriental tit (Parus minor) toward different predators and reactions they induce in nestlings

Anti-predatory strategies of birds are diverse and may include predator-specific alarm calls. For example, oriental tit (Parus minor) parents can distinguish snakes from other predators and produce snake-specific referential vocalizations ("jar" call) when a snake poses a threat to their nest. The “jar” call has a very specific function to induce fledging of nestlings close to fledging age. This reaction ensures nestlings' survival in natural encounters with snakes that are capable of entering nest cavities and kill entire broods. Sciurid rodents, like chipmunks, may pose a similar threat to cavity-nesting birds. We explored the hypothesis that parents use the fledging-inducing alarm vocalizations in this situation, because chipmunks, like snakes, can kill the brood upon entering the nest cavity. We compared alarm calls of parents toward two predators (chipmunk and snake) who pose a similar threat to the nestlings in a nest cavity, and toward an avian predator (Eurasian jay) who cannot enter nest cavities and poses no threat to the nestlings in a nest. Our results show that the vocal responses of oriental tits were different among the three predators. This suggests that the acoustic properties of vocal responses to predators are different between predators of a similar hunting strategy (nest-cavity entering). The playback of recorded vocal responses of parents to chipmunks did not trigger the fledging of old nestlings, whereas the vocalizations toward a snake did, as shown by earlier studies. Our study suggests that the vocal response of parents does not carry information about the ability of predators to enter the nest cavity and confirms the special status of alarm calls triggered by snakes.     

Ecological constraints drive social evolution in the African mole-rats.

The African mole-rats (family Bathyergidae) are subterranean hystricomorph rodents occurring in a variety of habitats and displaying levels of sociality which range from solitary to eusocial, making them a unique mammalian taxonomic group to test ecological influences on sociality. Here, we use an extensive DNA-based phylogeny and comparative analysis to investigate the relationship between ecology, sociality and evolution within the family. Mitochondrial cytochrome-b and 12s rRNA trees reveal that the solitary species are monophyletic when compared to the social species. The naked mole-rat (Heterocephalus glaber) is ancestral and divergent from the Damaraland mole-rat (Cryptomys damarensis), supporting previous findings that have suggested the multiple evolution of eusociality within the family. The Cryptomys genus is species-rich and contains taxa exhibiting different levels of sociality, which can be divided into two distinct clades. A total of seven independent comparisons were generated within the phylogeny, and three ecological variables were significantly correlated with social group size: geophyte density (p < 0.05), mean months per year of rainfall greater than 25 mm (p < 0.001), and the coefficient of rainfall variation (p = 0.001). These results support the food-aridity hypothesis for the evolution of highly social cooperative behaviour in the Bathyergidae, and are consistent with the current theoretical framework for skew theory.     

Biophysical modeling of the temporal niche: from first principles to the evolution of activity patterns

Most mammals can be characterized as nocturnal or diurnal. However infrequently, species may overcome evolutionary constraints and alter their activity patterns. We modeled the fundamental temporal niche of a diurnal desert rodent, the golden spiny mouse, Acomys russatus. This species can shift into nocturnal activity in the absence of its congener, the common spiny mouse, Acomys cahirinus, suggesting that it was competitively driven into diurnality and that this shift in a small desert rodent may involve physiological costs. Therefore, we compared metabolic costs of diurnal versus nocturnal activity using a biophysical model to evaluate the preferred temporal niche of this species. The model predicted that energy expenditure during foraging is almost always lower during the day except during midday in summer at the less sheltered microhabitat. We also found that a shift in summer to foraging in less sheltered microhabitats in response to predation pressure and food availability involves a significant physiological cost moderated by midday reduction in activity. Thus, adaptation to diurnality may reflect the "ghost of competition past"; climate-driven diurnality is an alternative but less likely hypothesis. While climate is considered to play a major role in the physiology and evolution of mammals, this is the first study to model its potential to affect the evolution of activity patterns of mammals.     

The Predator Deterrence Function of Primate Alarm Calls

It is generally assumed that alarm calls function in intraspecific communication, for example to warn close relatives about the presence of a predator. However, an alternative hypothesis suggests that, in some cases, signallers may also gain fitness benefits in directly communicating to the predator, for example by advertising perception and unprofitability to predators that depend on unprepared prey. In this study, we show that six monkey species in Taï forest, Ivory Coast, produce significantly more alarm calls to leopards than to chimpanzees, although both are notorious monkey predators. The conspicuously high vocalization rates to leopards had adaptive consequences for the monkeys. By following a radio-collared leopard, we found that after detection and high alarm call rates the leopard gave up its hiding location and left the group significantly faster than would be expected by chance. We discuss these data with respect to the various functional hypothesis of alarm call behaviour and conclude that the high alarm call rates to leopards are part of an anti-predator strategy in primates that may have evolved to deter predators that depend on surprise.     

Maternal care, defensive behavior, and sociality in neotropical Goniosoma harvestmen (Arachnida, Opiliones)

Summary: Goniosoma includes large and conspicuous species of harvestmen that occur exclusively in the Brazilian Atlantic forest. This paper reports on the parental activities, defensive behavior, and gregariousness of five species of Goniosoma, and also summarizes the published biological data for the genus. The behavioral patterns within the genus are discussed and a hypothesis for the emergence of gregariousness in the group is presented. Several Goniosoma live inside caves, mainly as trogloxenes. Although species of the genus comprise only 5% of the harvestmen fauna in Brazil, they account for 20.6% of all harvestmen species recorded in Brazilian caves. In addition to several morphological and physiological features that may favor the occupation of caves, species of Goniosoma also present subsocial behavior, which may confer a special advantage in this particular environment. Female protection is crucial for egg survival since predators may consume entire batches in a single night. Most species of Goniosoma form dense diurnal aggregations ranging from three to 200 individuals (mainly subadults and adults of both sexes). In a hypothetical scenario for the evolution of sociality in the Goniosoma, physiological constraints acting on individual harvestmen would lead to a behavioral response for the selection of sites with appropriate microclimatic conditions. The lack of cannibalism among adults and subadults may favor tolerance towards conspecifics, and may represent a pre-adaptation to gregariousness. The derived functions of gregarious behavior may include strengthening of the defensive signal through the collective release of a repugnant secretion, the dilution effect, and promptness in fleeing a predator attack as a consequence of the additional alarm role of scent gland secretions. These defensive functions may overcome the costs of group living and may be responsible for the maintenance of gregariousness in Goniosoma.