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1.  The deterrent effect of bird song in territory defense 
Behavioral Ecology  2008;20(1):200-206.
Using the responses of territory owners to playback to infer the territorial function of acoustic signals is common practice. However, difficulties with interpreting the results of such experiments have obscured our understanding of territorial signalling. For instance, a stronger response to playback is often interpreted as more aggressive, but there is no consensus as to whether this should be in response to the least or most threatening simulated intruder. Rather than following a gradual increase or decrease, the relationship between signal intensity and response strength may instead describe a peaked curve. We manipulated banded wren (Thryophilus pleurostictus) songs to simulate low-, median-, and high-performance singers and used these songs as stimuli in playback experiments. Banded wrens were less likely to approach the high-performance stimulus compared with the low- and median-performance stimuli. However, the birds that did approach the high-performance stimulus sang more than those that approached the low-performance stimulus. In addition, birds were more likely to match the songs when exposed to the median- and high-performance stimuli compared with the low-performance stimuli, and song matching predicted approach behavior. These results are in accordance with theoretical models of aggressive encounters in which low-performance opponents are challenged without further assessment. Median- and high-performance opponents, however, may require further assessment, and the latter may be perceived as too intimidating for approach.
doi:10.1093/beheco/arn135
PMCID: PMC2662740  PMID: 19337589
assessment; playback; sexual selection; song; territory defense
2.  Courtship attention in sagebrush lizards varies with male identity and female reproductive state 
Behavioral Ecology  2008;19(6):1326-1332.
Previous experiments suggest that males spend more time with the more receptive of 2 novel females or the one with the higher fitness potential. However, males often court individual females repeatedly over a season; for example, male lizards sequentially visit familiar females as they patrol territorial boundaries. It may benefit males to vary display intensity as they move between multiple females. In this study, we explored the factors influencing amount of male courtship to familiar females in the sagebrush lizard, Sceloporus graciosus. We tested whether males vary the amount of courtship exhibited due to individual differences among males, female reproductive state, or female fitness potential. Each male was allowed to interact separately, but repeatedly, with 2 females until both females laid eggs. Male courtship behavior with each of the 2 females was assayed at an intermediate point, after 3 weeks of interaction. We found that individual differences among males were considerable. The number of male courtship displays was also positively correlated with female latency to lay eggs, with males displaying more often toward females with eggs that had not yet been fertilized. Courtship behavior was not well predicted by the number of eggs laid or by female width, both measures of female quality. Thus, male S. graciosus appear to alter courtship intensity more in response to signals of female reproductive state than in response to variation in potential female fitness.
doi:10.1093/beheco/arn072
PMCID: PMC2583109  PMID: 19458780
courtship; male choice; mate choice; reproductive state; Sceloporus graciosus; sexual selection
3.  The deterrent effect of bird song in territory defense 
Using the responses of territory owners to playback to infer the territorial function of acoustic signals is common practice. However, difficulties with interpreting the results of such experiments have obscured our understanding of territorial signaling. For instance, a stronger response to playback is often interpreted as more aggressive, but there is no consensus as to whether this should be in response to the least or most threatening simulated intruder. Rather than following a gradual increase or decrease, the relationship between signal intensity and response strength may instead describe a peaked curve. We manipulated banded wren (Thryophilus pleurostictus) songs to simulate low, median and high performance singers and used these songs as stimuli in playback experiments. Banded wrens were less likely to approach the high performance stimulus compared to the low and median performance stimuli. However, the birds that did approach the high performance stimulus sang more than those that approached the low performance stimulus. In addition, birds were more likely to match the songs when exposed to the median and high performance stimuli compared to the low performance stimuli and song matching predicted approach behavior. These results are in accordance with theoretical models of aggressive encounters in which low performance opponents are challenged without further assessment. Median and high performance opponents however, may require further assessment and the latter may be perceived as too intimidating for approach.
doi:10.1093/beheco/arn135
PMCID: PMC2662740  PMID: 19337589
playback; song; territory defense; sexual selection; assessment
4.  Courtship attention in sagebrush lizards varies with male identity and female reproductive state 
Previous experiments suggest that males spend more time with the more receptive of two novel females or the one with the higher fitness potential. However, males often court individual females repeatedly over a season; for example, male lizards sequentially visit familiar females as they patrol territorial boundaries. It may benefit males to vary display intensity as they move between multiple females. In this study, we explored the factors influencing amount of male courtship to familiar females in the Sagebrush lizard, Sceloporus graciosus. We tested whether males vary the amount of courtship exhibited due to individual differences among males, female reproductive state, or female fitness potential. Each male was allowed to interact separately, but repeatedly, with two females until both females laid eggs. Male courtship behavior with each of the two females was assayed at an intermediate point, after three weeks of interaction. We found that individual differences among males were considerable. The number of male courtship displays was also positively correlated with female latency to lay eggs, with males displaying more often towards females with eggs that had not yet been fertilized. Courtship behavior was not well predicted by the number of eggs laid or by female width, both measures of female quality. Thus, male S. graciosus appear to alter courtship intensity more in response to signals of female reproductive state than in response to variation in potential female fitness.
doi:10.1093/beheco/arn072
PMCID: PMC2583109  PMID: 19458780
Sceloporus graciosus; male choice; mate choice; sexual selection; reproductive state; courtship
5.  Variance in male lifetime reproductive success and estimation of the degree of polygyny in a primate 
Behavioral Ecology  2014;25(4):878-889.
The degree of polygyny is predicted to influence the strength of direct male–male competition, leading to a high variance in male lifetime reproductive success and to reproduction limited to the prime period of adulthood. Here, we explore the variance in male lifetime reproductive success and reproductive time in an anthropoid primate forming multimale–multifemale groups. Males of this species form dominance hierarchies, which are expected to skew reproduction toward few high-ranking males. At the same time, however, females mate with multiple males (polygynandry), which should limit the degree of polygyny. Using 20 years of genetic and demographic data, we calculated lifetime reproductive success for the free-ranging rhesus macaque (Macaca mulatta) population of Cayo Santiago for subjects that died naturally or reached senescence. Our results show that 1) male lifetime reproductive success was significantly skewed (range: 0–47 offspring; males reproducing below average: 62.8%; nonbreeders: 17.4%), 2) variance in male lifetime reproductive success was 5 times larger than in females, and 3) male lifetime reproductive success was more influenced by variation in fecundity (60%) than longevity (25%), suggesting that some direct male–male competition takes place. However, the opportunity for selection (i.e., standardized variance in male lifetime reproductive success) is low compared with that in other large mammal species characterized by a high degree of polygyny. Moreover, male reproductive life extended much beyond the prime period, showing that physical strength was not required to acquire mates. We conclude that rhesus macaques exhibit a moderate degree of polygyny and, therefore, low levels of direct male–male competition for fertile females, despite the fact that males form linear dominance hierarchies.
Lay summary
Male rhesus macaques face moderate strength of direct competition for fertile mates, creating opportunity for indirect forms of competition. Using 20 years of genetic and demographic data, we show that variance in lifetime reproductive success is more pronounced in males than in females. Yet, most males reproduce in their lifetime, that surviving as long as possible increases males’ success, and that males reach high fecundity before the full development of secondary sex characteristics.
doi:10.1093/beheco/aru052
PMCID: PMC4095946  PMID: 25024637
lifetime reproductive success; male–male competition; mammals; opportunity for selection; reproductive skew; reproductive timing; rhesus macaques.
6.  Vocal fundamental and formant frequencies are honest signals of threat potential in peripubertal males 
Behavioral Ecology  2014;25(4):984-988.
Lay Summary
Men with lower voices are perceived as more physically dominant; however, it is unclear why, and whether this perception is accurate. We examine whether vocal frequencies are more strongly related to measures of threat potential (size or strength) among adolescents. Results show that vocal frequencies are more informative about strength than about size. These findings suggest that listeners ascribe greater dominance to low male voices because low voices are reliably associated with strength.
Fundamental and formant frequencies influence perceived pitch and are sexually dimorphic in humans. The information content of these acoustic parameters can illuminate the forces of sexual selection shaping vocal sex differences as well as the mechanisms that ensure signal reliability. We use multiple regression to examine the relationships between somatic (height, adiposity, and strength) and acoustic (fundamental frequency [F 0], formant position [P f], and fundamental frequency variation [F 0-SD]) characteristics in a sample of peripubertal Bolivian Tsimane. Results indicate that among males—but not females—strength is the strongest predictor of F 0 and P f and that F 0 and P f are independent predictors of strength when height and adiposity are controlled. These findings suggest that listeners may attend to vocal frequencies because they signal honest, nonredundant information about male strength and threat potential, which are strongly related to physical maturity and which cannot be ascertained from visual or other indicators of height or adiposity alone.
doi:10.1093/beheco/aru081
PMCID: PMC4095947  PMID: 25024638
costly signaling; formants; fundamental frequency; pitch; voice.
7.  Flexible compensation of uniparental care: female poison frogs take over when males disappear 
Behavioral Ecology  2015;26(4):1219-1225.
Lay Summary
Caring mothers step in for deadbeat dads. Flexible compensation has evolved as a countermeasure against reduced or lost parental care and is commonly found in biparental species. In the poison frog Allobates femoralis with obligatory male-only care, we show that females flexibly perform tadpole transport when males disappear. This demonstrates that compensatory flexibility also evolved in species with unisexual care, suggesting that parental care systems are more flexible than previously thought.
Parental care systems are shaped by costs and benefits to each sex of investing into current versus future progeny. Flexible compensatory parental care is mainly known in biparental species, particularly where parental desertion or reduction of care by 1 parent is common. The other parent can then compensate this loss by either switching parental roles and/or by increasing its own parental effort. In uniparental species, desertion of the caregiver usually leads to total brood loss. In the poison frog, Allobates femoralis, obligatory tadpole transport (TT) is generally performed by males, whereas females abandon their clutches after oviposition. Nevertheless, in a natural population we previously observed 7.8% of TT performed by females, which we could link to the absence of the respective fathers. In the following experiment, under laboratory conditions, all tested A. femoralis females flexibly took over parental duties, but only when their mates were removed. Our findings provide clear evidence for compensatory flexibility in a species with unisexual parental care. Contrary to the view of amphibian parental care as being stereotypical and fixed, these results demonstrate behavioral flexibility as an adaptive response to environmental and social uncertainty. Behavioral flexibility might actually represent a crucial step in the evolutionary transition from uniparental to biparental care in poison frogs. We suspect that across animal species flexible parental roles are much more common than previously thought and suggest the idea of a 3-dimensional continuum regarding flexibility, parental involvement, and timing, when thinking about the evolution of parental care.
doi:10.1093/beheco/arv069
PMCID: PMC4495760  PMID: 26167099
behavioral flexibility; compensation; partner removal; poison frog; tadpole transport; uniparental care.
8.  An arms race between producers and scroungers can drive the evolution of social cognition 
Behavioral Ecology  2014;25(3):487-495.
Lay Summary
Many cognitively advanced species live in groups, suggesting that this could have been important in the evolution of their high intelligence. We use theoretical analyses to show how the widespread behavior of foraging for food in groups can fuel an evolutionary arms race of intelligence. Strategies to outsmart others, stealing their food, and strategies to avoid being stolen from will continue to evolve so long as both sides use the same cognitive capacity in implementing these.
The “social intelligence hypothesis” states that the need to cope with complexities of social life has driven the evolution of advanced cognitive abilities. It is usually invoked in the context of challenges arising from complex intragroup structures, hierarchies, and alliances. However, a fundamental aspect of group living remains largely unexplored as a driving force in cognitive evolution: the competition between individuals searching for resources (producers) and conspecifics that parasitize their findings (scroungers). In populations of social foragers, abilities that enable scroungers to steal by outsmarting producers, and those allowing producers to prevent theft by outsmarting scroungers, are likely to be beneficial and may fuel a cognitive arms race. Using analytical theory and agent-based simulations, we present a general model for such a race that is driven by the producer–scrounger game and show that the race’s plausibility is dramatically affected by the nature of the evolving abilities. If scrounging and scrounging avoidance rely on separate, strategy-specific cognitive abilities, arms races are short-lived and have a limited effect on cognition. However, general cognitive abilities that facilitate both scrounging and scrounging avoidance undergo stable, long-lasting arms races. Thus, ubiquitous foraging interactions may lead to the evolution of general cognitive abilities in social animals, without the requirement of complex intragroup structures.
doi:10.1093/beheco/aru002
PMCID: PMC4014306  PMID: 24822021
game theory; intraspecific arms race; social foraging; social intelligence hypothesis.
9.  Rival male chemical cues evoke changes in male pre- and post-copulatory investment in a flour beetle 
Behavioral Ecology  2015;26(4):1021-1029.
Lay Summary
Males adjust both courtship effort and ejaculate expenditure when mating with females that are coated in the chemical cues of other males. Using a manipulative approach, we show that male flour beetles use the chemical cues of rival males left behind on virgin female cuticles to assess sperm competition risk. These cues do not make virgin females more chemically similar to mated females but appear to allow males to indirectly assess competition within the population.
Males can gather information on the risk and intensity of sperm competition from their social environment. Recent studies have implicated chemosensory cues, for instance cuticular hydrocarbons (CHCs) in insects, as a key source of this information. Here, using the broad-horned flour beetle (Gnatocerus cornutus), we investigated the importance of contact-derived rival male CHCs in informing male perception of sperm competition risk and intensity. We experimentally perfumed virgin females with male CHCs via direct intersexual contact and measured male pre- and post-copulatory investment in response to this manipulation. Using chemical analysis, we verified that this treatment engendered changes to perfumed female CHC profiles, but did not make perfumed females “smell” mated. Despite this, males responded to these chemical changes. Males increased courtship effort under low levels of perceived competition (from 1–3 rivals), but significantly decreased courtship effort as perceived competition rose (from 3–5 rivals). Furthermore, our measurement of ejaculate investment showed that males allocated significantly more sperm to perfumed females than to control females. Together, these results suggest that changes in female chemical profile elicited by contact with rival males do not provide males with information on female mating status, but rather inform males of the presence of rivals within the population and thus provide a means for males to indirectly assess the risk of sperm competition.
doi:10.1093/beheco/arv047
PMCID: PMC4495758  PMID: 26167098
chemical cues; cuticular hydrocarbons; ejaculate expenditure; Gnatocerus cornutus; sperm competition risk.
10.  Dynamics of among-individual behavioral variation over adult lifespan in a wild insect 
Behavioral Ecology  2015;26(4):975-985.
Lay Summary
Wild crickets show consistent patterns of behavior over their adult lifetimes and as they get older they become increasingly predictable. We tagged crickets and then periodically recaptured them and measured their behavior in the lab. This revealed that rather than variation in how age affects behavior, there were consistent patterns across the whole population. We do not have a situation where some crickets live fast and die young while others take it easy and slow.
Investigating patterns of among and within-individual trait variation in populations is essential to understanding how selection shapes phenotypes. Behavior is often the most flexible aspect of the phenotype, and to understand how it is affected by selection, we need to examine how consistent individuals are. However, it is not well understood whether among-individual differences tend to remain consistent over lifetimes, or whether the behavior of individuals relative to one another varies over time. We examined the dynamics of 4 behavioral traits (tendency to leave a refuge, shyness, activity, and exploration) in a wild population of field crickets (Gryllus campestris). We tagged individuals and then temporarily removed them from their natural environment and tested them under laboratory conditions. All 4 traits showed among-individual variance in mean levels of expression across the adult lifespan, but no significant differences in how rapidly expression changed with age. For all traits, among-individual variance increased as individuals got older. Our findings reveal seldom examined changes in variance components over the adult lifetime of wild individuals. Such changes will have important implications for the relationship between behavioral traits, life-histories, and fitness and the consequences of selection on wild individuals.
doi:10.1093/beheco/arv048
PMCID: PMC4495759  PMID: 26167097
animal personality; behavioral reaction norms; Gryllus; plasticity; wild crickets.
11.  Cicadas impact bird communication in a noisy tropical rainforest 
Behavioral Ecology  2015;26(3):839-842.
Lay Summary
When the cicada buzz starts up, bird song shuts down in a neotropical rainforest. When birds do sing at the same time as cicadas, their song bandwidths do not overlap.
Many animals communicate through acoustic signaling, and “acoustic space” may be viewed as a limited resource that organisms compete for. If acoustic signals overlap, the information in them is masked, so there should be selection toward strategies that reduce signal overlap. The extent to which animals are able to partition acoustic space in acoustically diverse habitats such as tropical forests is poorly known. Here, we demonstrate that a single cicada species plays a major role in the frequency and timing of acoustic communication in a neotropical wet forest bird community. Using an automated acoustic monitor, we found that cicadas vary the timing of their signals throughout the day and that the frequency range and timing of bird vocalizations closely track these signals. Birds significantly avoid temporal overlap with cicadas by reducing and often shutting down vocalizations at the onset of cicada signals that utilize the same frequency range. When birds do vocalize at the same time as cicadas, the vocalizations primarily occur at nonoverlapping frequencies with cicada signals. Our results greatly improve our understanding of the community dynamics of acoustic signaling and reveal how patterns in biotic noise shape the frequency and timing of bird vocalizations in tropical forests.
doi:10.1093/beheco/arv018
PMCID: PMC4433330  PMID: 26023277
acoustic partitioning; bird vocalizations.
12.  Mate choice and genetic monogamy in a biparental, colonial fish 
Behavioral Ecology  2015;26(3):782-788.
Lay Summary
We report a rare case of genetic monogamy in a biparental fish species. Males and females paired assortatively by size, which is compatible with mutual mate choice. Mate choice in monogamous species is interesting because both sexes provide essential parental care, making males, as well as females, choosy. Social monogamy in the form of biparental care is well known from a variety of species, but uncommon in fish.
In socially monogamous species, in which both sexes provide essential parental care, males as well as females are expected to be choosy. Whereas hundreds of studies have examined monogamy in biparental birds, only several such studies exist in fish. We examined mate choice in the biparental, colonial cichlid fish Neolamprologus caudopunctatus in Lake Tanganyika, Zambia. We genotyped more than 350 individuals at 11 microsatellite loci to investigate their mating system. We found no extrapair paternity, identifying this biparental fish as genetically monogamous. Breeders paired randomly according to their genetic similarity, suggesting a lack of selection against inbreeding avoidance. We further found that breeders paired assortatively by body size, a criterion of quality in fish, suggesting mutual mate choice. In a subsequent mate preference test in an aquarium setup, females showed a strong preference for male size by laying eggs near the larger of 2 males in 13 of 14 trials.
doi:10.1093/beheco/arv011
PMCID: PMC4433329  PMID: 26023276
assortative mating; cichlid; colony; extrapair paternity.
13.  Populations, pools, and peccaries: simulating the impact of ecosystem engineers on rainforest frogs 
Behavioral Ecology  2015;26(2):340-349.
Lay Summary
Peccary wallows and footprints are important breeding pools for rainforest frogs. We performed a resource supplementation experiment with artificial pools, simulating peccary actions, in a population of the poison frog Allobates femoralis. The population almost doubled resulting from increased local reproduction, but not from immigration. These findings demonstrate the importance of “ecosystem engineers,” such as peccaries, for other species, the frogs. Our results also indicate that human engineering may help to protect amphibian populations.
“Ecosystem engineering” describes habitat alteration by an organism that affects another organism; such nontrophic interactions between organisms are a current focus in ecological research. Our study quantifies the actual impact an ecosystem engineer can have on another species by using a previously identified model system—peccaries and rainforest frogs. In a 4-year experiment, we simulated the impact of peccaries on a population of Allobates femoralis (Dendrobatidae) by installing an array of artificial pools to mimic a forest patch modified by peccaries. The data were analyzed using a gradual before-after control-impact (gBACI) model. Following the supplementation, population size almost doubled as a result of increased autochthonous recruitment driven by a higher per-capita reproduction of males and a higher proportion of reproducing females. The effect was evenly distributed across the population. The differential response of males and females reflects the reproductive behavior of A. femoralis, as only the males use the aquatic sites for tadpole deposition. Our study shows that management and conservation must consider nontrophic relationships and that human “ecosystem engineering” can play a vital role in efforts against the “global amphibian decline.”
doi:10.1093/beheco/aru243
PMCID: PMC4374131  PMID: 25825586
Allobates femoralis; Dendrobatidae; ecosystem engineering; nontrophic interaction; population manipulation experiment; reproductive resource supplementation.
14.  A larger brain confers a benefit in a spatial mate search learning task in male guppies 
Behavioral Ecology  2014;26(2):527-532.
Lay Summary
Does a large brain make you smarter? If you are a guppy male searching for a female in a maze, it does. The association between brain size and smartness is a debated issue, largely due to the lack of experimental data. We compared guppies artificially bred for large and small brains and found that large-brained males learned the route through a spatial maze faster. These results thus support a link between brain size and smartness.
Brain size varies dramatically among vertebrates, and selection for increased cognitive abilities is thought to be the key force underlying the evolution of a large brain. Indeed, numerous comparative studies suggest positive relationships between cognitively demanding aspects of behavior and brain size controlled for body size. However, experimental evidence for the link between relative brain size and cognitive ability is surprisingly scarce and to date stems from a single study on brain size selected guppies (Poecilia reticulata), where large-brained females were shown to outperform small-brained females in a numerical learning assay. Because the results were inconclusive for males in that study, we here use a more ecologically relevant test of male cognitive ability to investigate whether or not a relatively larger brain increases cognitive ability also in males. We compared mate search ability of these artificially selected large- and small-brained males in a maze and found that large-brained males were faster at learning to find a female in a maze. Large-brained males decreased the time spent navigating the maze faster than small-brained males and were nearly twice as fast through the maze after 2 weeks of training. Our results support that relatively larger brains are better also for males in some contexts, which further substantiates that variation in vertebrate brain size is generated through the balance between energetic costs and cognitive benefits.
doi:10.1093/beheco/aru227
PMCID: PMC4374130  PMID: 25825587
brain size; cognition; guppy; maze.
15.  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.
doi:10.1093/beheco/art062
PMCID: PMC3796708  PMID: 24137044
cooperative breeding; flight call; individual recognition; kin recognition; Lamprotornis superbus; vocal communication.
16.  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.
doi:10.1093/beheco/art079
PMCID: PMC3796710  PMID: 24137046
decision making; producer; risk sensitivity; scrounger; social foraging; social learning.
17.  Cortisol in mother’s milk across lactation reflects maternal life history and predicts infant temperament 
Behavioral Ecology  2014;26(1):269-281.
Lay Summary
In monkeys, high cortisol and changes in cortisol levels in mother’s milk are associated with more nervous and less confident infants. Sons are more sensitive than are daughters to changes in cortisol in mother’s milk across lactation. Females that are earlier in their reproductive career tend to have higher cortisol in their milk. Mothers may be “programming” behaviorally cautious offspring that prioritize growth through cortisol signaling.
The maternal environment exerts important influences on offspring mass/growth, metabolism, reproduction, neurobiology, immune function, and behavior among birds, insects, reptiles, fish, and mammals. For mammals, mother’s milk is an important physiological pathway for nutrient transfer and glucocorticoid signaling that potentially influences offspring growth and behavioral phenotype. Glucocorticoids in mother’s milk have been associated with offspring behavioral phenotype in several mammals, but studies have been handicapped by not simultaneously evaluating milk energy density and yield. This is problematic as milk glucocorticoids and nutrients likely have simultaneous effects on offspring phenotype. We investigated mother’s milk and infant temperament and growth in a cohort of rhesus macaque (Macaca mulatta) mother–infant dyads at the California National Primate Research Center (N = 108). Glucocorticoids in mother’s milk, independent of available milk energy, predicted a more Nervous, less Confident temperament in both sons and daughters. We additionally found sex differences in the windows of sensitivity and the magnitude of sensitivity to maternal-origin glucocorticoids. Lower parity mothers produced milk with higher cortisol concentrations. Lastly, higher cortisol concentrations in milk were associated with greater infant weight gain across time. Taken together, these results suggest that mothers with fewer somatic resources, even in captivity, may be “programming” through cortisol signaling, behaviorally cautious offspring that prioritize growth. Glucocorticoids ingested through milk may importantly contribute to the assimilation of available milk energy, development of temperament, and orchestrate, in part, the allocation of maternal milk energy between growth and behavioral phenotype.
doi:10.1093/beheco/aru186
PMCID: PMC4309982  PMID: 25713475
behavioral phenotype; breast milk composition; developmental programming; glucocorticoids; life-history theory; personality.
18.  Effects of age, size, and mating history on sex role decision of a simultaneous hermaphrodite 
Behavioral Ecology  2014;26(1):232-241.
Lay summary
Quite a few animals are male and female at the same time, so they can choose to mate either as male or female on copulation. The decision to perform either sex role was known to be highly flexible depending on various, but often confounding, factors. For the pond snail, we report that young and small snails tend to mate as males first, though old and large snails do not seem to be better females.
Contrasting with separate-sexed animals, simultaneous hermaphrodites display unique reproductive strategies as they are male and female at the same time. Simultaneous hermaphrodites that copulate unilaterally, for instance, make a decision to mate as a male or female. Previous studies have demonstrated that sex role preference in hermaphrodites is flexible and is controlled by several, often confounding, factors. We examined the relationship between sex role decisions and 3 life-history traits (age, size, and mating history) in the great pond snail, Lymnaea stagnalis. Based on our field observations, which indicate that adult individuals show overlapping generations and large variation in body size during the breeding season, we performed a sex role choice experiment in the laboratory. We found that young and small snails mate as males first. Both age and size significantly affected sex role decision, with age having a stronger effect. Furthermore, we tested whether L. stagnalis becomes reluctant to inseminate a mate after being inseminated because it is known that after insemination, male investment substantially reduces. Contrary to expectations, our results indicate that the receipt of seminal fluid does not seem to reduce male motivation. In sum, sex role decisions in L. stagnalis are largely determined by age and size but not by having received seminal fluid. This mating pattern, however, does not fully support the size-advantage model because large or old individuals did not perform better as females in our experiment. These results imply a conflicting mating interest, rather than harmonious agreement, between age- and size-different hermaphrodites.
doi:10.1093/beheco/aru184
PMCID: PMC4309981  PMID: 25713474
Lymnaea stagnalis; reproductive strategy; sex allocation; sexual conflict; size-advantage model.
19.  Biparental incubation-scheduling: no experimental evidence for major energetic constraints 
Behavioral Ecology  2014;26(1):30-37.
Lay Summary
It is believed that a bird’s energetic reserves determine when and for how long it incubates its eggs. We challenge this view for species where both parents incubate. We experimentally reduced the energetic demands of incubation by heating and insulating the nest. These treatments had no major effect on the length of incubation bouts.
Incubation is energetically demanding, but it is debated whether these demands constrain incubation-scheduling (i.e., the length, constancy, and timing of incubation bouts) in cases where both parents incubate. Using 2 methods, we experimentally reduced the energetic demands of incubation in the semipalmated sandpiper, a biparental shorebird breeding in the harsh conditions of the high Arctic. First, we decreased the demands of incubation for 1 parent only by exchanging 1 of the 4 eggs for an artificial egg that heated up when the focal bird incubated. Second, we reanalyzed the data from the only published experimental study that has explicitly tested energetic constraints on incubation-scheduling in a biparentally incubating species (Cresswell et al. 2003). In this experiment, the energetic demands of incubation were decreased for both parents by insulating the nest cup. We expected that the treated birds, in both experiments, would change the length of their incubation bouts, if biparental incubation-scheduling is energetically constrained. However, we found no evidence that heating or insulation of the nest affected the length of incubation bouts: the combined effect of both experiments was an increase in bout length of 3.6min (95% CI: −33 to 40), which is equivalent to a 0.5% increase in the length of the average incubation bout. These results demonstrate that the observed biparental incubation-scheduling in semipalmated sandpipers is not primarily driven by energetic constraints and therefore by the state of the incubating bird, implying that we still do not understand the factors driving biparental incubation-scheduling.
doi:10.1093/beheco/aru156
PMCID: PMC4309980  PMID: 25713473
Arctic; biparental incubation; Calidris pusilla; constancy; cross-over design; energetic constraints; energetic demands; incubation bout length; replication; scheduling; semipalmated sandpiper; shorebird; statistical power.
20.  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.
doi:10.1093/beheco/art052
PMCID: PMC3739417  PMID: 23935257
behavioral syndrome; foraging mode; intraspecific variation; personality; predator–prey interaction.
21.  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.
doi:10.1093/beheco/aru143
PMCID: PMC4235584  PMID: 25419087
cooperation; mammals; maternal care; maternal defense; multiple mating; Mus musculus domesticus.
22.  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.
doi:10.1093/beheco/aru134
PMCID: PMC4235582  PMID: 25419085
Canis lupus; functional response; movement; resource selection; road; step selection function; travel speed.
23.  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.
doi:10.1093/beheco/aru128
PMCID: PMC4235581  PMID: 25419084
cooperative breeding; humidity; moisture; nestbuilding; niche construction; parental investment; sociality; water balance.
24.  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.
doi:10.1093/beheco/aru126
PMCID: PMC4235580  PMID: 25419083
camouflage; color variation; communication; signal partitioning; trade-offs; vision.
25.  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.
doi:10.1093/beheco/aru108
PMCID: PMC4160112  PMID: 25214755
Formica lugubris; levels of selection; network analysis; polydomy; self-organization; wood ants.

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