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1.  Flight calls signal group and individual identity but not kinship in a cooperatively breeding bird 
Behavioral Ecology  2013;24(6):1279-1285.
Lay Summary
Ants are models of conflict, generally working together but at the same time competing over individual fitness. We show that ant larvae compete by cannibalizing eggs, which increases their survival. Male larvae are particularly selfish, and eat eggs three times more often than females. Larvae also discriminate between sibling and alien eggs, which suggests that they can react to chemical recognition cues. Remarkably, ant larvae thus possess the power to act in social conflict.
In many complex societies, intricate communication and recognition systems may evolve to help support both direct and indirect benefits of group membership. In cooperatively breeding species where groups typically comprise relatives, both learned and innate vocal signals may serve as reliable cues for kin recognition. Here, we investigated vocal communication in the plural cooperatively breeding superb starling, Lamprotornis superbus, where flight calls—short, stereotyped vocalizations used when approaching conspecifics—may communicate kin relationships, group membership, and/or individual identity. We found that flight calls were most similar within individual repertoires but were also more similar within groups than within the larger population. Although starlings responded differently to playback of calls from their own versus other neighboring and distant social groups, call similarity was uncorrelated with genetic relatedness. Additionally, immigrant females showed similar patterns to birds born in the study population. Together, these results suggest that flight calls are learned signals that reflect social association but may also carry a signal of individuality. Flight calls, therefore, provide a reliable recognition mechanism for groups and may also be used to recognize individuals. In complex societies comprising related and unrelated individuals, signaling individuality and group association, rather than kinship, may be a route to cooperation.
PMCID: PMC3796708  PMID: 24137044
cooperative breeding; flight call; individual recognition; kin recognition; Lamprotornis superbus; vocal communication.
2.  The role of beginner’s luck in learning to prefer risky patches by socially foraging house sparrows 
Behavioral Ecology  2013;24(6):1398-1406.
Lay summary
Experiments with foraging house sparrows show that chance events during learning can explain contrasting individual preferences for safe versus risky alternatives, even when the expected benefit of the risky alternativeis 8-fold higher than that of the safe one. However, in social groups, learning to prefer the safe but less rewarding alternative mayoccasionally be compensated by scrounging on the food findings of individuals that havelearned to prefer the high risk-high reward option.
Although there has been extensive research on the evolution of individual decision making under risk (when facing variable outcomes), little is known on how the evolution of such decision-making mechanisms has been shaped by social learning and exploitation. We presented socially foraging house sparrows with a choice between scattered feeding wells in which millet seeds were hidden under 2 types of colored sand: green sand offering ~80 seeds with a probability of 0.1 (high risk–high reward) and yellow sand offering 1 seed with certainty (low risk–low reward). Although the expected benefit of choosing variable wells was 8 times higher than that of choosing constant wells, only some sparrows developed a preference for variable wells, whereas others developed a significant preference for constant wells. We found that this dichotomy could be explained by stochastic individual differences in sampling success during foraging, rather than by social foraging strategies (active searching vs. joining others). Moreover, preference for variable or constant wells was related to the sparrows’ success during searching, rather than during joining others or when picking exposed seeds (i.e., they learn when actively searching in the sand). Finally, although for many sparrows learning resulted in an apparently maladaptive risk aversion, group living still allowed them to enjoy profitable variable wells by occasionally joining variable-preferring sparrows.
PMCID: PMC3796710  PMID: 24137046
decision making; producer; risk sensitivity; scrounger; social foraging; social learning.
3.  Predator and prey activity levels jointly influence the outcome of long-term foraging bouts 
Behavioral Ecology  2013;24(5):1205-1210.
Lay summary
Animals exhibit “behavioral types” (akin to human personalities) where individuals differ consistently on traits like activity which may influence the predators it encounters and the prey it captures. Here we demonstrate that active jumping spiders are more likely to encounter and consume inactive crickets and vice versa. This presents a potential explanation for the persistence of behavioral types in natural populations, as behavioral variation in one trophic level maintains variation in the associated level.
Consistent interindividual differences in behavior (i.e., “behavioral types”) may be a key factor in determining the outcome of species interactions. Studies that simultaneously account for the behavioral types of individuals in multiple interacting species, such as predator–prey systems, may be particularly strong predictors of ecological outcomes. Here, we test the predator–prey locomotor crossover hypothesis, which predicts that active predators are more likely to encounter and consume prey with the opposing locomotor tendency. We test this hypothesis using intraspecific behavioral variation in both a predator and prey species as predictors of foraging outcomes. We use the old field jumping spider, Phidippus clarus (Araneae, Salticidae), and the house cricket, Acheta domesticus (Orthoptera, Gryllidae), as a model predator–prey system in laboratory mesocosm trials. Stable individual differences in locomotor tendencies were identified in both P. clarus and A. domesticus, and the outcome of foraging bouts depended neither on the average activity level of the predator nor on the average activity level of prey. Instead, an interaction between the activity level of spiders and crickets predicted spider foraging success and prey survivorship. Consistent with the locomotor crossover hypothesis, predators exhibiting higher activity levels consumed more prey when in an environment containing low-activity prey items and vice versa. This study highlights 1) the importance of intraspecific variation in determining the outcome of predator–prey interactions and 2) that acknowledging behavioral variation in only a single species may be insufficient to characterize the performance consequences of intraspecific trait variants.
PMCID: PMC3739417  PMID: 23935257
behavioral syndrome; foraging mode; intraspecific variation; personality; predator–prey interaction.
4.  Socially mediated polyandry: a new benefit of communal nesting in mammals 
Behavioral Ecology  2014;25(6):1467-1473.
In many species, females have evolved behavioral strategies to reduce the risk of infanticide. For instance, polyandry can create paternity confusion that inhibits males from killing offspring they could have sired. Here, the authors propose that females could socially obtain the same benefits by nesting communally. Singly sired litters could be perceived as a large multiply sired litter once pooled together in a single nest. Long-term data from a wild house mouse population showed that monandrous litters (singly sired) were more common in communal than in solitary nests and 85% of them were raised with litters sired by different males hence becoming effectively polyandrous (multiply sired). These socially polyandrous litters had significantly higher offspring survival than genetically or socially monandrous litters and reached a similar survival to that of multiply sired litters raised in solitary or communal nests. Furthermore, the number of sires within nests significantly improved offspring survival whereas the number of mothers did not. These results suggest that the survival benefits associated with communal nesting are driven by polyandry and not communal defense. This socially mediated polyandry was as efficient as multiple paternity in preventing infanticide, and may also occur in other infanticidal and polytocous species where the caring parent exhibits social behavior.
Lay Summary
Communal nesting allows social females to avoid infanticide in much the same way as multiple mating: through paternity confusion. Litters sired by a single male can be perceived as a large multiply-sired litter once pooled together in a communal nest. This socially mediated polyandry was as efficient as multiple paternity in preventing infanticide. The number of mothers in communal nests did not explain offspring survival hence rejecting the communal defense hypothesis.
PMCID: PMC4235584  PMID: 25419087
cooperation; mammals; maternal care; maternal defense; multiple mating; Mus musculus domesticus.
5.  Behavioral responses of wolves to roads: scale-dependent ambivalence 
Behavioral Ecology  2014;25(6):1353-1364.
Throughout their recent recovery in several industrialized countries, large carnivores have had to cope with a changed landscape dominated by human infrastructure. Population growth depends on the ability of individuals to adapt to these changes by making use of new habitat features and at the same time to avoid increased risks of mortality associated with human infrastructure. We analyzed the summer movements of 19 GPS-collared resident wolves (Canis lupus L.) from 14 territories in Scandinavia in relation to roads. We used resource and step selection functions, including >12000 field-checked GPS-positions and 315 kill sites. Wolves displayed ambivalent responses to roads depending on the spatial scale, road type, time of day, behavioral state, and reproductive status. At the site scale (approximately 0.1 km2), they selected for roads when traveling, nearly doubling their travel speed. Breeding wolves moved the fastest. At the patch scale (10 km2), house density rather than road density was a significant negative predictor of wolf patch selection. At the home range scale (approximately 1000 km2), breeding wolves increased gravel road use with increasing road availability, although at a lower rate than expected. Wolves have adapted to use roads for ease of travel, but at the same time developed a cryptic behavior to avoid human encounters. This behavioral plasticity may have been important in allowing the successful recovery of wolf populations in industrialized countries. However, we emphasize the role of roads as a potential cause of increased human-caused mortality.
Lay Summary
We studied how wolves in Scandinavia respond to roads built to ease human travel but degrading habitat quality for many wildlife species. Wolves responded with ambivalence: They both selected and avoided roads, all depending on the spatial and temporal scale and their behavioral status. To understand the multi-scale effects of human infrastructure on animal behavior is important with regard to the recent come-back of many wildlife species to now industrialized countries.
PMCID: PMC4235582  PMID: 25419085
Canis lupus; functional response; movement; resource selection; road; step selection function; travel speed.
6.  Thrips domiciles protect larvae from desiccation in an arid environment 
Behavioral Ecology  2014;25(6):1338-1346.
Desiccation is a particular risk for small animals in arid environments. In response, many organisms “construct niches,” favorable microenvironments where they spend part or all of their life cycle. Some maintain such environments for their offspring via parental care. Insect eggs are often protected from desiccation by parentally derived gels, casings, or cocoons, but active parental protection of offspring from desiccation has never been demonstrated. Most free-living thrips (Thysanoptera) alleviate water loss via thigmotaxis (crevice seeking). In arid Australia, Acacia thrips (Phlaeothripidae) construct many kinds of niche. Some thrips induce galls; others, like Dunatothrips aneurae, live and breed within “domiciles” made from loosely glued phyllodes. The function of domiciles is unknown; like other constructed niches, they may 1) create favorable microenvironments, 2) facilitate feeding, 3) protect from enemies, or a combination. To test the first 2 alternatives experimentally, field-collected domiciles were destroyed or left intact. Seven-day survival of feeding and nonfeeding larval stages was monitored at high (70–80%) or low (8–10%, approximately ambient) humidity. Regardless of humidity, most individuals survived in intact domiciles, whereas for destroyed domiciles, survival depended on humidity, suggesting parents construct and maintain domiciles to prevent offspring desiccating. Feeding and nonfeeding larvae had similar survival patterns, suggesting the domicile’s role is not nutritional. Outside domiciles, survival at “high” humidity was intermediate, suggesting very high humidity requirements, or energetic costs of wandering outside domiciles. D. aneurae commonly cofound domiciles; cofoundresses may benefit both from shared nestbuilding costs, and from “deferred byproduct mutualism,” that is, backup parental care in case of mortality.
Lay Summary
Tiny Acacia thrips build communal “domiciles” in arid Australia. Here I show that domiciles prevent desiccation, ensuring offspring survival—a novel kind of parental care in insects. We suspect many insect parents perform this function for offspring, but it has never been demonstrated experimentally. If larvae require parental care, this suggests one reason thrips are sometimes communal: if a female dies, her nestmates can ensure her offspring survive.
PMCID: PMC4235581  PMID: 25419084
cooperative breeding; humidity; moisture; nestbuilding; niche construction; parental investment; sociality; water balance.
7.  Wall lizards display conspicuous signals to conspecifics and reduce detection by avian predators 
Behavioral Ecology  2014;25(6):1325-1337.
Visual signals are often under conflicting selection to be hidden from predators while being conspicuous to mates and rivals. Here, we investigated whether 3 different island populations of Aegean wall lizards (Podarcis erhardii) with variable coloration among diverse island habitats exhibit simultaneous camouflage and sexual signals. We examined whether signals appear better tuned to conspecific vision as opposed to that of avian predators, and whether background-matching camouflage and sexual signals are partitioned to specific body regions. This could facilitate both covert sexual signaling and camouflage according to the viewing perspectives of predators and conspecifics. We found that lizards typically appeared twice as conspicuous to conspecifics than to avian predators against the same visual background, largely due to lizards’ enhanced sensitivity to ultraviolet, suggesting that P. erhardii signals are tuned to conspecific vision to reduce detection by predators. Males were more conspicuous than females to both predators and conspecifics. In 2 populations, male backs were relatively more camouflaged to predators compared to signaling flanks, whereas in females, exposed and concealed surfaces were camouflaged to predators and generally did not differ in background matching. These findings indicate that lizard coloration evolves under the competing demands of natural and sexual selection to promote signals that are visible to conspecifics while being less perceptible to avian predators. They also elucidate how interactions between natural and sexual selection influence signal detectability and partitioning to different body regions, highlighting the importance of considering receiver vision, viewing perspectives, and signaling environments in studies of signal evolution.
Lay Summary
Lizards and their predators see the world differently, allowing lizards (Podarcis erhardii) to display bright sexual signals that are less visible to hunting birds. Males are more conspicuous than females, but reduce their visibility to predators by having camouflaged backs and restricting brighter signals to their sides, which makes them less visible to birds hunting from above while still being highly visible to mates and rivals on the ground.
PMCID: PMC4235580  PMID: 25419083
camouflage; color variation; communication; signal partitioning; trade-offs; vision.
8.  Resource redistribution in polydomous ant nest networks: local or global? 
Behavioral Ecology  2014;25(5):1183-1191.
Lay Summary
Wood ants nests share resources with neighboring nests, not the whole colony. A single ant colony can either live all in one nest, or split into several separate, but communicating, nests. How and why ant colonies do this is unknown. By treating these separated colonies as networks we show that wood ants exchange food locally, with neighboring nests, without a colony-level plan.
An important problem facing organisms in a heterogeneous environment is how to redistribute resources to where they are required. This is particularly complex in social insect societies as resources have to be moved both from the environment into the nest and between individuals within the nest. Polydomous ant colonies are split between multiple spatially separated, but socially connected, nests. Whether, and how, resources are redistributed between nests in polydomous colonies is unknown. We analyzed the nest networks of the facultatively polydomous wood ant Formica lugubris. Our results indicate that resource redistribution in polydomous F. lugubris colonies is organized at the local level between neighboring nests and not at the colony level. We found that internest trails connecting nests that differed more in their amount of foraging were stronger than trails between nests with more equal foraging activity. This indicates that resources are being exchanged directly from nests with a foraging excess to nests that require resources. In contrast, we found no significant relationships between nest properties, such as size and amount of foraging, and network measures such as centrality and connectedness. This indicates an absence of a colony-level resource exchange. This is a clear example of a complex behavior emerging as a result of local interactions between parts of a system.
PMCID: PMC4160112  PMID: 25214755
Formica lugubris; levels of selection; network analysis; polydomy; self-organization; wood ants.
9.  Social and ecological factors influencing offspring survival in wild macaques 
Behavioral Ecology  2014;25(5):1164-1172.
Lay summary
Better to live in a big group if you want your offspring to survive! Using a multivariate approach, we show how the interplay of ecological and social factors influences fetus and infant survival in wild crested macaques. Offspring are more likely to survive in bigger groups, but seasonality also influences their survival. Fetus survival is higher for higher ranking mothers, whereas the main determinant of infants’ death is an alpha-male takeover by an immigrant male.
Premature loss of offspring decreases direct fitness of parents. In gregarious mammals, both ecological and social variables impact offspring survival and may interact with each other in this regard. Although a number of studies have investigated factors influencing offspring loss in mammals, we still know very little on how different factors interact with one another. We therefore investigated fetal and infant mortality in 3 large groups of wild crested macaques (Macaca nigra) over a period of up to 5 years by including potential social causes such as maternal dominance rank, male immigration, between group encounters, and ecological conditions such as rainfall in a multivariate survival analysis using Cox proportional hazards model. Infant but not fetal survival was most impaired after a recent takeover of the alpha-male position by an immigrant male. Furthermore, infant survival probability increased when there was an increase in number of group adult females and rainfall. Fetal survival probability also increased with an increase of these 2 factors, but more in high-ranking than low-ranking females. Fetal survival, unlike that of infants, was also improved by an increase of intergroup encounter rates. Our study thus stresses the importance of survival analyses using a multivariate approach and encompassing more than a single offspring stage to investigate the determinants of female direct fitness. We further provide evidence for fitness costs and benefits of group living, possibly deriving from high pressures of both within- and between-group competition, in a wild primate population.
PMCID: PMC4160111  PMID: 25214754
between-group encounters; female reproductive success; Macaca nigra; offspring loss; proportional hazards model; socioecology.
10.  Foraging for carotenoids: do colorful male hihi target carotenoid-rich foods in the wild? 
Behavioral Ecology  2014;25(5):1048-1057.
Lay Summary
Birds that color their feathers with dietary carotenoid pigments are expected to seek out these pigments when they are molting. We show that molting male hihi, who express carotenoid-based plumage, seek out naturally occurring foods that are rich in carotenoid pigments. Female hihi, who do not express carotenoid-based plumage, do not seek out carotenoid-rich foods. This lends strength to the idea that carotenoid-based plumage reveals an individual’s foraging ability.
Dietary access to carotenoids is expected to determine the strength of carotenoid-based signal expression and potentially to maintain signal honesty. Species that display carotenoid-based yellow, orange, or red plumage are therefore expected to forage selectively for carotenoid-rich foods when they are depositing these pigments during molt, but whether they actually do so is unknown. We set out to address this in the hihi (Notiomystis cincta), a New Zealand passerine where males, but not females, display yellow carotenoid-based plumage. We measured circulating carotenoid concentrations in male and female hihi during breeding and molt, determined the nutritional content of common foods in the hihi diet, and conducted feeding observations of male and female hihi during molt. We found that although male and female hihi do not differ significantly in plasma carotenoid concentration, male hihi have a greater proportion of carotenoid-rich foods in their diet than do females. This is a consequence of a greater fruit and lower invertebrate intake than females and an avoidance of low-carotenoid content fruit. By combining behavioral observations with quantification of circulating carotenoids, we present evidence that colorful birds forage to maximize carotenoid intake, a conclusion we would not have drawn had we examined plasma carotenoids alone.
PMCID: PMC4160110  PMID: 25214753
carotenoids; foraging; hihi; nutrition; plumage.
11.  Sequential male mate choice under sperm competition risk 
Behavioral Ecology  2014;25(3):660-667.
Lay Summary
New research shows that male house mice can be coy too. Male eagerness to mate is a central tenet of sexual selection theory, based on the expectation that male reproductive success is limited mainly by access to females. Here, we show that where sperm supplies are limited, males too can display considerable restraint in mating, targeting reproductive effort toward particular females.
Male eagerness to mate is a central paradigm of sexual selection theory. However, limited sperm supplies mean that male sexual restraint might sometimes be favored under promiscuous mating. Here, we demonstrate dynamic plasticity in male mating effort when females are encountered sequentially under varying sperm competition risk. Rather than showing consistent eagerness to mate, male house mice (Mus musculus domesticus) instead tailor their mating effort according to likely reproductive payoffs. They are significantly less likely to mate when sperm competition is certain and potential reproductive payoffs low, but dramatically increase investment if they do choose to mate under such circumstances. By contrast, male mice are significantly more likely to mate in situations simulating extra-territorial copulations, where future risk of competition is high but so too are potential reproductive rewards. Differential mating propensity appears to be the primary mechanism by which male house mice allocate sperm adaptively under sperm competition risk because we find no evidence for facultative adjustment of sperm numbers per ejaculate or ejaculation frequency in response to female-related cues. We conclude that sequential male mate choice under sperm competition risk could be a widespread but often unappreciated mechanism of strategic sperm allocation.
PMCID: PMC4014308  PMID: 24822023
copulatory behavior; mate choice; mating effort; sex roles; sexual conflict; sexual selection; sperm allocation; sperm competition.
12.  Experimental evidence of impacts of an invasive parakeet on foraging behavior of native birds 
Behavioral Ecology  2014;25(3):582-590.
Lay Summary
Invasive rose-ringed parakeets caused behavioral changes in native garden birds that reduced their feeding rates. Understanding how invasive species impact native species can be complex, especially in urban environments where many other factors are also at play. We therefore used an experiment to disentangle these factors and demonstrate that parakeets are more disruptive than a dominant native competitor.
Resource competition is one potential behavioral mechanism by which invasive species can impact native species, but detecting this competition can be difficult due to the interactions that variable environmental conditions can have on species behavior. This is particularly the case in urban habitats where the disturbed environment can alter natural behavior from that in undisturbed habitats. The rose-ringed parakeet (Psittacula krameri), is an increasingly common invasive species, predominantly associated with large urban centers. Using an experimental approach, we tested the behavioral responses of native garden birds in response to the presence of a rose-ringed parakeet versus the presence of a similarly sized and dominant native bird, the great spotted woodpecker (Dendrocopos major). Parakeet presence significantly reduced feeding rates and increased vigilance among native birds compared with our control treatments. Of visits made by native birds in the presence of a parakeet, feeding was more likely to occur in sites within the parakeet range compared with sites outside, suggesting some habituation of native birds has occurred following prior exposure to parakeets but overall foraging behavior is still disrupted. The results of our study suggest that nonnative species can have complex and subtle impacts on native fauna and show that a nonnative competitor can impact native species simply through their presence near resources.
PMCID: PMC4014307  PMID: 24822022
alien; ecological impacts; foraging behavior; interspecific interference competition; parrot; ringnecked parakeet.
13.  Size and competitive mating success in the yeast Saccharomyces cerevisiae  
Behavioral Ecology  2013;25(2):320-327.
Lay Summary
Yeast cells that are too big or too small are more likely to remain virgins. Big yeast cells are fitter than small cells when food is plentiful, but smaller cells are fitter when food is scarce. When there is a choice of different size potential mates, the best size partner for the conditions is more likely to be chosen for sex, ensuring that the resulting offspring are of a fit size.
In unicellular organisms like yeast, mating with the right partner is critical to future fitness because each individual can only mate once. Because cell size is important for viability, mating with a partner of the right size could be a significant advantage. To investigate this idea, we manipulated the size of unmated yeast cells and showed that their viability depended on environmental conditions; large cells do better on rich medium and small cells do better on poor medium. We also found that the fitness of offspring is determined by the size of their parents. Finally, we demonstrated that when a focal cell of one mating type was placed with a large and a small cell of the opposite mating type, it was more likely to mate with the cell that was closer to the optimum size for growth in a given environment. This pattern was not generated by differences in passive mating efficiency of large and small cells across environments but by competitive mating behavior, mate preference, or both. We conclude that the most likely mechanism underlying this interesting behavior is that yeast cells compete for mates by producing pheromone signals advertising their viability, and cells with the opportunity to choose prefer to mate with stronger signalers because such matings produce more viable offspring.
PMCID: PMC3945744  PMID: 24616602
body size; cell size; mate choice; mating; Saccharomyces cerevisiae; sexual selection.
14.  Effects of age and experience on contest behavior in the burying beetle, Nicrophorus vespilloides  
Behavioral Ecology  2013;25(1):172-179.
Lay summary:
Aggression and likelihood of winning contests are expected to change as a male ages. We test this idea in burying beetles, a species which competes over small mammal carcasses as a breeding resource. We find that male size relative to his opponent is far more important in determining contest outcome than any effects of age or social experience.
Contest behavior forms an important part of reproductive investment. Life-history theory predicts that as individuals age and their residual reproductive value decreases, they should increase investment in contest behavior. However, other factors such as social experience may also be important in determining age-related variation in contest behavior. To understand how selection acts on contest behavior over an individual’s lifetime, it is therefore important to tease apart the effects of age per se from other factors that may vary with age. Here, we independently manipulate male age and social experience to examine their effects on male contest behavior in the burying beetle Nicrophorus vespilloides. We found that social experience, but not age, influenced male contest behavior but that these changes in behavior did not alter contest outcomes. Male size (relative to his opponent) was overwhelmingly the most important factor determining contest outcome. Our results suggest that in systems with high variation in fighting ability among males, there may be little opportunity for selection to act on factors that influence contest outcomes by altering motivation to win.
PMCID: PMC3860834  PMID: 24347998
age; contest behavior; fighting; male competition; Nicrophorus vespilloides; social experience; terminal investment; winner–loser effect.
15.  Biparental incubation patterns in a high-Arctic breeding shorebird: how do pairs divide their duties? 
Behavioral Ecology  2013;25(1):152-164.
Lay summary:
Parents may be in conflict over the care they provide to their offspring. To understand this conflict, an accurate description of who does what and when is necessary. We used an automated system to continuously monitor which parent incubated the eggs in an arctic breeding shorebird. Birds sat on the eggs around 11 h at a time, but females sat longer than males. In compensation, females were off-duty more when feeding was easier.
In biparental species, parents may be in conflict over how much they invest into their offspring. To understand this conflict, parental care needs to be accurately measured, something rarely done. Here, we quantitatively describe the outcome of parental conflict in terms of quality, amount, and timing of incubation throughout the 21-day incubation period in a population of semipalmated sandpipers (Calidris pusilla) breeding under continuous daylight in the high Arctic. Incubation quality, measured by egg temperature and incubation constancy, showed no marked difference between the sexes. The amount of incubation, measured as length of incubation bouts, was on average 51min longer per bout for females (11.5h) than for males (10.7h), at first glance suggesting that females invested more than males. However, this difference may have been offset by sex differences in the timing of incubation; females were more often off nest during the warmer period of the day, when foraging conditions were presumably better. Overall, the daily timing of incubation shifted over the incubation period (e.g., for female incubation from evening–night to night–morning) and over the season, but varied considerably among pairs. At one extreme, pairs shared the amount of incubation equally, but one parent always incubated during the colder part of the day; at the other extreme, pairs shifted the start of incubation bouts between days so that each parent experienced similar conditions across the incubation period. Our results highlight how the simultaneous consideration of different aspects of care across time allows sex-specific investment to be more accurately quantified.
PMCID: PMC3860833  PMID: 24347997
Arctic; Calidris pusilla; continuous daylight; incubation pattern; incubation timing; negotiation; nest attendance; parental care division; semipalmated sandpiper; sexual conflict.
16.  Boldness behavior and stress physiology in a novel urban environment suggest rapid correlated evolutionary adaptation 
Behavioral Ecology  2012;23(5):960-969 .
Novel or changing environments expose animals to diverse stressors that likely require coordinated hormonal and behavioral adaptations. Predicted adaptations to urban environments include attenuated physiological responses to stressors and bolder exploratory behaviors, but few studies to date have evaluated the impact of urban life on codivergence of these hormonal and behavioral traits in natural systems. Here, we demonstrate rapid adaptive shifts in both stress physiology and correlated boldness behaviors in a songbird, the dark-eyed junco, following its colonization of a novel urban environment. We compared elevation in corticosterone (CORT) in response to handling and flight initiation distances in birds from a recently established urban population in San Diego, California to birds from a nearby wildland population in the species' ancestral montane breeding range. We also measured CORT and exploratory behavior in birds raised from early life in a captive common garden study. We found persistent population differences for both reduced CORT responses and bolder exploratory behavior in birds from the colonist population, as well as significant negative covariation between maximum CORT and exploratory behavior. Although early developmental effects cannot be ruled out, these results suggest contemporary adaptive evolution of correlated hormonal and behavioral traits associated with colonization of an urban habitat.
PMCID: PMC3431113  PMID: 22936840
adaptation; boldness; corticosterone; evolution; junco; urbanization
17.  Nest site and weather affect the personality of harvester ant colonies 
Behavioral Ecology  2012;23(5):1022-1029.
Environmental conditions and physical constraints both influence an animal's behavior. We investigate whether behavioral variation among colonies of the black harvester ant, Messor andrei, remains consistent across foraging and disturbance situations and ask whether consistent colony behavior is affected by nest site and weather. We examined variation among colonies in responsiveness to food baits and to disturbance, measured as a change in numbers of active ants, and in the speed with which colonies retrieved food and removed debris. Colonies differed consistently, across foraging and disturbance situations, in both responsiveness and speed. Increased activity in response to food was associated with a smaller decrease in response to alarm. Speed of retrieving food was correlated with speed of removing debris. In all colonies, speed was greater in dry conditions, reducing the amount of time ants spent outside the nest. While a colony occupied a certain nest site, its responsiveness was consistent in both foraging and disturbance situations, suggesting that nest structure influences colony personality.
PMCID: PMC3431114  PMID: 22936841
behavioral syndromes; collective behavior; harvester ant; Messor andrei; nest structure; personality; plasticity; social insects; temperament
18.  Photorefractoriness and energy availability interact to permit facultative timing of spring breeding 
Behavioral Ecology  2012;23(5):1049-1058.
In seasonally breeding mammals, vernal reproductive development is not directly triggered by increases in day length, rather, an endogenous program of photorefractoriness to short winter days initiates spontaneous development in advance of spring. The transition to the reproductive phenotype is energetically demanding. How food availability in late winter and early spring impacts the onset and expression of photorefractoriness is not known. In this study, male Siberian hamsters were born into a simulated natural photoperiod, and at the winter solstice, they were subjected to a restricted feeding protocol in which a daily food ration was provided in an amount equal to ad libitum (AL) intake during the weeks preceding the solstice. Over the next several months, AL–fed control hamsters exhibited spontaneous recrudescence or spontaneous development. In contrast, vernal reproductive development was abolished in most food-rationed hamsters. In food-rationed hamsters that did exhibit recrudescence, conspicuous delays in the onset of gonadal development and decreases in the magnitude of growth were evident. In all hamsters, the termination of food rationing triggered rapid gonadal development. The data indicate that late winter/early spring increases in environmental food availability are required for the normal manifestation of photorefractoriness-induced reproductive development and suggest that a function of photorefractoriness may be merely to disinhibit the reproductive axis from photoperiodic suppression. Vernal gonadal development or recrudescence appears to be strongly affected by proximate energy availability.
PMCID: PMC3431115  PMID: 22936842
energy balance; food availability; photoperiodism; seasonality; Siberian hamster
19.  Rates of agonism among female primates: a cross-taxon perspective 
Behavioral Ecology  2013;24(6):1369-1380.
Lay summary:
It has long been thought that female-female aggression in primates is higher in species that primarily eat fruits than in those that feed more on leaves or insects. Here we test this hypothesis with data from 23 primate species, and show that primates that eat more fruits do not engage in more aggression. Instead, rates of aggression increase with group size and time spent on the ground. Thus, female aggression depends on the density of competitors and the ease or costs of aggression.
Agonism is common in group-living animals, shaping dominance relationships and ultimately impacting individual fitness. Rates of agonism vary considerably among taxa, however, and explaining this variation has been central in ecological models of female social relationships in primates. Early iterations of these models posited a link to diet, with more frequent agonism predicted in frugivorous species due to the presumed greater contestability of fruits relative to other food types. Although some more recent studies have suggested that dietary categories may be poor predictors of contest competition among primates, to date there have been no broad, cross-taxa comparisons of rates of female–female agonism in relation to diet. This study tests whether dietary variables do indeed predict rates of female agonism and further investigates the role of group size (i.e., number of competitors) and substrate use (i.e., degree of arboreality) on the frequency of agonism. Data from 44 wild, unprovisioned groups, including 3 strepsirhine species, 3 platyrrhines, 5 colobines, 10 cercopithecines, and 2 hominoids were analyzed using phylogenetically controlled and uncontrolled methods. Results indicate that diet does not predict agonistic rates, with trends actually being in the opposite direction than predicted for all taxa except cercopithecines. In contrast, agonistic rates are positively associated with group size and possibly degree of terrestriality. Competitor density and perhaps the risk of fighting, thus, appear more important than general diet in predicting agonism among female primates. We discuss the implications of these results for socio-ecological hypotheses.
PMCID: PMC3796709  PMID: 24137045
aggression; feeding competition; folivory; frugivory; group size; terrestriality.
20.  Paternal care and the evolution of exaggerated sexual swellings in primates 
Behavioral Ecology  2012;23(4):699-706.
The exaggerated sexual swellings exhibited by females of some primate species have been of interest to evolutionary biologists since the time of Darwin. We summarize existing hypotheses for their function and evolution and categorize these hypotheses within the context of 3 types of variation in sexual swelling size: 1) variation within a single sexual cycle, 2) variation between the sexual cycles of a single female, and 3) differences between females. We then propose the Paternal Care Hypothesis for the function of sexual swellings, which posits that exaggerated sexual swellings function to elicit the right quantity and quality of male care for a female's infant. As others have noted, swellings may allow females to engender paternity confusion, or they may allow females to confer relative paternal certainty on one male. Key to our hypothesis is that both of these scenarios create an incentive for one or more males to provide care. This hypothesis builds on previous hypotheses but differs from them by highlighting the elicitation of paternal care as a key function of swellings. Our hypothesis predicts that true paternal care (in which males accurately differentiate and provide assistance to their own offspring) will be most common in species in which exaggerated swellings accurately signal the probability of conception, and males can monopolize females during the window of highest conception probability. Our hypothesis also predicts that females will experience selection to behave in ways that either augment paternity confusion or enhance paternal certainty depending on their social and demographic contexts.
PMCID: PMC3999376  PMID: 24771988
infanticide; parental care; primates; sexual swellings
21.  Spatial movements and social networks in juvenile male song sparrows 
Behavioral Ecology  2011;23(1):141-152.
The time between fledging and breeding is a critical period in songbird ontogeny, but the behavior of young songbirds in the wild is relatively unstudied. The types of social relationships juveniles form with other individuals can provide insight into the process through which they learn complex behaviors crucial for survival, territory establishment, and mate attraction. We used radio telemetry to observe social associations of young male song sparrows (Melospiza melodia) from May to November. Juvenile song sparrows were frequently observed in social flocks and generally associated with more birds in the summer than in the autumn months. Most juvenile subjects formed stable social relationships with other birds and were seen with the same individual on up to 60% of the days observed. The strongest associations occurred with other juvenile males, and these individuals were often seen <1 m from the subject, even when the subject moved large distances between tracking observations. Associations also had long-term behavioral consequences as subjects were more likely to establish territories near their associates and learn shared song types. Our results indicate that male song sparrows spend a large percentage of the juvenile life stage forming social relationships and suggest that these associations may be important for the ecology of young birds and the ontogeny of their behaviors.
PMCID: PMC3242974  PMID: 22479140
22.  Eyespot display in the peacock butterfly triggers antipredator behaviors in naïve adult fowl 
Behavioral Ecology  2012;24(1):305-310.
Large conspicuous eyespots have evolved in multiple taxa and presumably function to thwart predator attacks. Traditionally, large eyespots were thought to discourage predator attacks because they mimicked eyes of the predators’ own predators. However, this idea is controversial and the intimidating properties of eyespots have recently been suggested to simply be a consequence of their conspicuousness. Some lepidopteran species include large eyespots in their antipredation repertoire. In the peacock butterfly, Inachis io, eyespots are typically hidden during rest and suddenly exposed by the butterfly when disturbed. Previous experiments have shown that small wild passerines are intimidated by this display. Here, we test whether eyespots also intimidate a considerably larger bird, domestic fowl, Gallus gallus domesticus, by staging interactions between birds and peacock butterflies that were sham-painted or had their eyespots painted over. Our results show that birds typically fled when peacock butterflies performed their display regardless of whether eyespots were visible or painted over. However, birds confronting butterflies with visible eyespots delayed their return to the butterfly, were more vigilant, and more likely to utter alarm calls associated with detection of ground-based predators, compared with birds confronting butterflies with eyespots painted over. Because production of alarm calls and increased vigilance are antipredation behaviors in the fowl, their reaction suggests that eyespots may elicit fear rather than just an aversion to conspicuous patterns. Our results, therefore, suggest that predators perceive large lepidopteran eyespots as belonging to the eyes of a potential predator.
PMCID: PMC3518204  PMID: 23243378
chicken; predator–prey interactions; startle display
23.  Geometric analysis of macronutrient selection in breeds of the domestic dog, Canis lupus familiaris  
Behavioral Ecology  2012;24(1):293-304.
Although many herbivores and omnivores have been shown to balance their intake of macronutrients when faced with nutritionally variable foods, study of this ability has been relatively neglected in carnivores, largely on the assumption that prey are less variable in nutrient composition than the foods of herbivores and omnivores and such mechanisms therefore unnecessary. We performed diet selection studies in 5 breeds of adult dog (Canis lupus familiaris) to determine whether these domesticated carnivores regulate macronutrient intake. Using nutritional geometry, we show that the macronutrient content of the diet was regulated to a protein:fat:carbohydrate ratio of approximately 30%:63%:7% by energy, a value that was remarkably similar across breeds. These values, which the analysis suggests are dietary target values, are based on intakes of dogs with prior experience of the respective experimental food combinations. On initial exposure to the diets (i.e., when naive), the same dogs self-selected a diet that was marginally but significantly lower in fat, suggesting that learning played a role in macronutrient regulation. In contrast with the tight regulation of macronutrient ratios, the total amount of food and energy eaten was far higher than expected based on calculated maintenance energy requirements. We interpret these results in relation to the evolutionary history of domestic dogs and compare them to equivalent studies on domestic cats.
PMCID: PMC3518205  PMID: 23243377
Canis lupus; carnivore nutrition; domestication; domestic dog; geometric framework; macronutrient regulation; predation; right-angled mixture triangles
24.  Green symphonies: a call for studies on acoustic communication in plants 
Behavioral Ecology  2012;24(4):789-796.
Sound and its use in communication have significantly contributed to shaping the ecology, evolution, behavior, and ultimately the success of many animal species. Yet, the ability to use sound is not a prerogative of animals. Plants may also use sound, but we have been unable to effectively research what the ecological and evolutionary implications might be in a plant’s life. Why should plants emit and receive sound and is there information contained in those sounds? I hypothesize that it would be particularly advantageous for plants to learn about the surrounding environment using sound, as acoustic signals propagate rapidly and with minimal energetic or fitness costs. In fact, both emission and detection of sound may have adaptive value in plants by affecting responses in other organisms, plants, and animals alike. The systematic exploration of the functional, ecological, and evolutionary significance of sound in the life of plants is expected to prompt a reinterpretation of our understanding of these organisms and galvanize the emergence of novel concepts and perspectives on their communicative complexity.
PMCID: PMC3677178  PMID: 23754865
behavior; bioacoustics; communication; frequencies; plants signaling; sound.
25.  Intrasexual competition in females: evidence for sexual selection? 
Behavioral Ecology  2011;22(6):1131-1140.
In spite of recent interest in sexual selection in females, debate exists over whether traits that influence female–female competition are sexually selected. This review uses female–female aggressive behavior as a model behavioral trait for understanding the evolutionary mechanisms promoting intrasexual competition, focusing especially on sexual selection. I employ a broad definition of sexual selection, whereby traits that influence competition for mates are sexually selected, whereas those that directly influence fecundity or offspring survival are naturally selected. Drawing examples from across animal taxa, including humans, I examine 4 predictions about female intrasexual competition based on the abundance of resources, the availability of males, and the direct or indirect benefits those males provide. These patterns reveal a key sex difference in sexual selection: Although females may compete for the number of mates, they appear to compete more so for access to high-quality mates that provide direct and indirect (genetic) benefits. As is the case in males, intrasexual selection in females also includes competition for essential resources required for access to mates. If mate quality affects the magnitude of mating success, then restricting sexual selection to competition for quantity of mates may ignore important components of fitness in females and underestimate the role of sexual selection in shaping female phenotype. In the future, understanding sex differences in sexual selection will require further exploration of the extent of mutual intrasexual competition and the incorporation of quality of mating success into the study of sexual selection in both sexes.
PMCID: PMC3199163  PMID: 22479137
aggression; female competition; intrasexual selection; mating success; sexual selection

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