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1.  High rates of pregnancy loss by subordinates leads to high reproductive skew in wild golden lion tamarins (Leontopithecus rosalia) 
Hormones and behavior  2013;63(5):675-683.
Across taxa, cooperative breeding has been associated with high reproductive skew. Cooperatively breeding golden lion tamarins (Leontopithecus rosalia) were long thought to have a monogynous mating system in which reproduction was limited to a single dominant female. Subordinates with few reproductive opportunities delayed dispersal and remained in the natal group to provide alloparental care to siblings, thus allowing dominant reproductive females to meet the energetic needs associated with high rates of reproduction and successful infant rearing. The goal of this study was to re-assess monogyny in wild golden lion tamarin groups based upon pregnancy diagnoses that used non-invasive enzyme immunoassay for progesterone and cortisol, combined with weekly data on individual weight gain, bi-annual physical examinations noting pregnancy and lactation status and daily behavioral observations. We established quantitative and qualitative criteria to detect and determine the timing of pregnancies that did not result in the birth of infants. Pregnancy polygyny occurred in 83% of golden lion tamarin groups studied. The loss of 64% of subordinate pregnancies compared to only 15% by dominant females limited reproductive success mainly to dominant females, thus maintaining high reproductive skew in female golden lion tamarins. Pregnancy loss by subordinate adults did not appear to result from dominant interference in subordinate hormonal mechanisms, but more likely resulted from subordinate abandonment of newborn infants to mitigate dominant aggression.
doi:10.1016/j.yhbeh.2013.02.009
PMCID: PMC3667972  PMID: 23454002
cooperative breeding; reproductive skew; polygyny; reproductive suppression; pregnancy loss; dominant control; subordination; progesterone; cortisol; Leontopithecus rosalia
2.  Forest type affects prey foraging of saddleback tamarins, Saguinus nigrifrons 
Primates; Journal of Primatology  2014;55(3):403-413.
Callitrichids can persist in secondary forests where they may benefit from elevated prey abundance. However, how tamarins forage for prey in secondary forest compared to primary forest has not been examined. Using scan and focal sampling, we compared prey foraging and capture success of two groups of Saguinus nigrifrons in north-eastern Peru: one ranging in primary forest, the other with access to a 10-year-old anthropogenic secondary forest. There was a trend for more prey search in the secondary forest, but prey feeding, capture success and size were lower compared to the primary forest. Tamarins avoided the forest floor, used vertical supports less often and searched on a lower variety of substrates in the secondary forest. In the secondary forest, tamarins did not capture flushed prey, which make up a substantial part of the total prey captures biomass in primary forests. Reduced prey capture success is unlikely to reflect reduced prey availability, since more Orthoptera were found in secondary forest through ultrasonic surveys. Therefore, the prey search activity of S. nigrifrons in young secondary forests seemed rather opportunistic, presumably influenced by altered predation patterns, vegetation structure, as well as prey diversity.
Electronic supplementary material
The online version of this article (doi:10.1007/s10329-014-0416-4) contains supplementary material, which is available to authorized users.
doi:10.1007/s10329-014-0416-4
PMCID: PMC4082136  PMID: 24687729
Saguinus nigrifrons; Tamarin; Prey foraging; Secondary forest; Primary forest; Habitat use
3.  Social Learning of a Novel Foraging Task by Big Brown Bats (Eptesicus fuscus) 
Animal behaviour  2011;82(5):1075-1083.
Acquiring information via observation of others can be an efficient way to respond to changing situations or learn skills, particularly for inexperienced individuals. Many bat species are gregarious, yet few studies have investigated their capacity for learning from conspecifics. We tested whether big brown bats (Eptesicus fuscus) can learn a novel foraging task by interacting with knowledgeable conspecifics. In experimental trials 11 naïve bats (7 juveniles, 4 adults) interacted freely with trained bats that were capturing tethered mealworms, while in control trials 11 naïve bats (7 juveniles, 4 adults) flew with untrained bats. Naïve bats were then assessed for their ability to capture tethered mealworms. While no bat in the control group learned the task, a significant number of experimental bats, including juveniles with little or no experience foraging, showed evidence of learning. Eighty-two per cent of experimental bats and 27% of control bats directed feeding buzzes (echolocation calls associated with prey capture) at the mealworm. Furthermore, seven experimental bats (64%) showed evidence of learning by attacking and/or capturing the mealworm, while no bat in the control group attacked or captured the prey. Analyses of high-speed stereo video recordings revealed increased interaction with demonstrators among bats attacking or capturing the mealworm. At the time they displayed evidence of learning, bats flew closer together during feeding buzzes than during other portions of trials. Our results demonstrate that social interaction with experienced bats, and listening to feeding buzzes in particular, may play an integral role in development of foraging skills in bats.
doi:10.1016/j.anbehav.2011.07.044
PMCID: PMC3274777  PMID: 22328786
big brown bat; Eptesicus fuscus; feeding buzzes; foraging; information transfer; juvenile development; local enhancement; social learning
4.  Foraging Behaviour of Juvenile Female New Zealand Sea Lions (Phocarctos hookeri) in Contrasting Environments 
PLoS ONE  2013;8(5):e62728.
Foragers can show adaptive responses to changes within their environment through morphological and behavioural plasticity. We investigated the plasticity in body size, at sea movements and diving behaviour of juvenile female New Zealand (NZ) sea lions (Phocarctos hookeri) in two contrasting environments. The NZ sea lion is one of the rarest pinnipeds in the world. Most of the species is based at the subantarctic Auckland Islands (AI; considered to be marginal foraging habitat), with a recolonizing population on the Otago Peninsula, NZ mainland (considered to be more optimal habitat). We investigated how juvenile NZ sea lions adjust their foraging behaviour in contrasting environments by deploying satellite-linked platform transmitting terminals (PTTs) and time-depth recorders (TDRs) on 2–3 year-old females at AI (2007–2010) and Otago (2009–2010). Juvenile female NZ sea lions exhibited plasticity in body size and behaviour. Otago juveniles were significantly heavier than AI juveniles. Linear mixed effects models showed that study site had the most important effect on foraging behaviour, while mass and age had little influence. AI juveniles spent more time at sea, foraged over larger areas, and dove deeper and longer than Otago juveniles. It is difficult to attribute a specific cause to the observed contrasts in foraging behaviour because these differences may be driven by disparities in habitat/prey characteristics, conspecific density levels or interseasonal variation. Nevertheless, the smaller size and increased foraging effort of AI juveniles, combined with the lower productivity in this region, support the hypothesis that AI are less optimal habitat than Otago. It is more difficult for juveniles to forage in suboptimal habitats given their restricted foraging ability and lower tolerance for food limitation compared to adults. Thus, effective management measures should consider the impacts of low resource environments, along with changes that can alter food availability such as potential resource competition with fisheries.
doi:10.1371/journal.pone.0062728
PMCID: PMC3646001  PMID: 23671630
5.  The Forager Oral Tradition and the Evolution of Prolonged Juvenility 
The foraging niche is characterized by the exploitation of nutrient-rich resources using complex extraction techniques that take a long time to acquire. This costly period of development is supported by intensive parental investment. Although human life history theory tends to characterize this investment in terms of food and care, ethnographic research on foraging skill transmission suggests that the flow of resources from old-to-young also includes knowledge. Given the adaptive value of information, parents may have been under selection pressure to invest knowledge – e.g., warnings, advice – in children: proactive provisioning of reliable information would have increased offspring survival rates and, hence, parental fitness. One way that foragers acquire subsistence knowledge is through symbolic communication, including narrative. Tellingly, oral traditions are characterized by an old-to-young transmission pattern, which suggests that, in forager groups, storytelling might be an important means by which adults transfer knowledge to juveniles. In particular, by providing juveniles with vicarious experience, storytelling may expand episodic memory, which is believed to be integral to the generation of possible future scenarios (i.e., planning). In support of this hypothesis, this essay reviews evidence that: mastery of foraging knowledge and skill sets takes a long time to acquire; foraging knowledge is transmitted from parent to child; the human mind contains adaptations specific to social learning; full assembly of learning mechanisms is not complete in early childhood; and forager oral traditions contain a wide range of information integral to occupation of the foraging niche. It concludes with suggestions for tests of the proposed hypothesis.
doi:10.3389/fpsyg.2011.00133
PMCID: PMC3160140  PMID: 21897825
embodied capital; foraging niche; information exchange; mental time travel; oral tradition; prolonged juvenility; social learning; storytelling
6.  The role of social context and individual experience in novel task acquisition in cottontop tamarins, Saguinus oedipus 
Animal behaviour  2006;71(4):933-943.
In socially tolerant settings, naïve individuals may have opportunities to interact jointly with knowledgeable demonstrators and novel tasks. This process is expected to facilitate social learning. Individual experience may also be important for reinforcing and honing socially acquired behaviours. We examined the role of joint interaction and individual experience in the acquisition of a novel foraging task in captive cottontop tamarins. The task involved learning how to locate and access two hidden food rewards from among 10 differently cued forage sites. Tamarins were tested in three different conditions: (1) individually, (2) while interacting with a naïve mate, and (3) while interacting with a mate trained as a knowledgeable demonstrator. For tamarins tested with mates present, we interspersed social input test days with exposure to the task while alone. Tamarins were tested again 17 months after their last exposure to the task, to assess long-term memory. All tamarins tested with knowledgeable demonstrators solved the task. In contrast, tamarins tested alone or with naïve mates had similarly high levels of neophobia and low levels of task acquisition. We conclude that joint interaction occurs in mated pairs of cottontop tamarins and facilitates the spread of novel behaviour. Interspersing test days with a knowledgeable demonstrator present and test days alone with the task helped tamarins to achieve the ultimate goal of the task: obtaining food rewards. Tamarins performed similarly when tested 17 months later, regardless of their initial learning environment. Tamarins had memory deficits for the location of hidden food rewards, but retained memory of the necessary motor actions and solved the task.
doi:10.1016/j.anbehav.2005.09.007
PMCID: PMC1540457  PMID: 16912811
7.  Loggerhead Turtles (Caretta caretta) Use Vision to Forage on Gelatinous Prey in Mid-Water 
PLoS ONE  2013;8(6):e66043.
Identifying characteristics of foraging activity is fundamental to understanding an animals’ lifestyle and foraging ecology. Despite its importance, monitoring the foraging activities of marine animals is difficult because direct observation is rarely possible. In this study, we use an animal-borne imaging system and three-dimensional data logger simultaneously to observe the foraging behaviour of large juvenile and adult sized loggerhead turtles (Caretta caretta) in their natural environment. Video recordings showed that the turtles foraged on gelatinous prey while swimming in mid-water (i.e., defined as epipelagic water column deeper than 1 m in this study). By linking video and 3D data, we found that mid-water foraging events share the common feature of a marked deceleration phase associated with the capture and handling of the sluggish prey. Analysis of high-resolution 3D movements during mid-water foraging events, including presumptive events extracted from 3D data using deceleration in swim speed as a proxy for foraging (detection rate = 0.67), showed that turtles swam straight toward prey in 171 events (i.e., turning point absent) but made a single turn toward the prey an average of 5.7±6.0 m before reaching the prey in 229 events (i.e., turning point present). Foraging events with a turning point tended to occur during the daytime, suggesting that turtles primarily used visual cues to locate prey. In addition, an incident of a turtle encountering a plastic bag while swimming in mid-water was recorded. The fact that the turtle’s movements while approaching the plastic bag were analogous to those of a true foraging event, having a turning point and deceleration phase, also support the use of vision in mid-water foraging. Our study shows that integrated video and high-resolution 3D data analysis provides unique opportunities to understand foraging behaviours in the context of the sensory ecology involved in prey location.
doi:10.1371/journal.pone.0066043
PMCID: PMC3680403  PMID: 23776603
8.  Animal-Borne Imaging Reveals Novel Insights into the Foraging Behaviors and Diel Activity of a Large-Bodied Apex Predator, the American Alligator (Alligator mississippiensis) 
PLoS ONE  2014;9(1):e83953.
Large-bodied, top- and apex predators (e.g., crocodilians, sharks, wolves, killer whales) can exert strong top-down effects within ecological communities through their interactions with prey. Due to inherent difficulties while studying the behavior of these often dangerous predatory species, relatively little is known regarding their feeding behaviors and activity patterns, information that is essential to understanding their role in regulating food web dynamics and ecological processes. Here we use animal-borne imaging systems (Crittercam) to study the foraging behavior and activity patterns of a cryptic, large-bodied predator, the American alligator (Alligator mississippiensis) in two estuaries of coastal Florida, USA. Using retrieved video data we examine the variation in foraging behaviors and activity patterns due to abiotic factors. We found the frequency of prey-attacks (mean = 0.49 prey attacks/hour) as well as the probability of prey-capture success (mean = 0.52 per attack) were significantly affected by time of day. Alligators attempted to capture prey most frequently during the night. Probability of prey-capture success per attack was highest during morning hours and sequentially lower during day, night, and sunset, respectively. Position in the water column also significantly affected prey-capture success, as individuals’ experienced two-fold greater success when attacking prey while submerged. These estimates are the first for wild adult American alligators and one of the few examples for any crocodilian species worldwide. More broadly, these results reveal that our understandings of crocodilian foraging behaviors are biased due to previous studies containing limited observations of cryptic and nocturnal foraging interactions. Our results can be used to inform greater understanding regarding the top-down effects of American alligators in estuarine food webs. Additionally, our results highlight the importance and power of using animal-borne imaging when studying the behavior of elusive large-bodied, apex predators, as it provides critical insights into their trophic and behavioral interactions.
doi:10.1371/journal.pone.0083953
PMCID: PMC3893291  PMID: 24454711
9.  When to approach novel prey cues? Social learning strategies in frog-eating bats 
Animals can use different sources of information when making decisions. Foraging animals often have access to both self-acquired and socially acquired information about prey. The fringe-lipped bat, Trachops cirrhosus, hunts frogs by approaching the calls that frogs produce to attract mates. We examined how the reliability of self-acquired prey cues affects social learning of novel prey cues. We trained bats to associate an artificial acoustic cue (mobile phone ringtone) with food rewards. Bats were assigned to treatments in which the trained cue was either an unreliable indicator of reward (rewarded 50% of the presentations) or a reliable indicator (rewarded 100% of the presentations), and they were exposed to a conspecific tutor foraging on a reliable (rewarded 100%) novel cue or to the novel cue with no tutor. Bats whose trained cue was unreliable and who had a tutor were significantly more likely to preferentially approach the novel cue when compared with bats whose trained cue was reliable, and to bats that had no tutor. Reliability of self-acquired prey cues therefore affects social learning of novel prey cues by frog-eating bats. Examining when animals use social information to learn about novel prey is key to understanding the social transmission of foraging innovations.
doi:10.1098/rspb.2013.2330
PMCID: PMC3813345  PMID: 24266035
bat; novel prey; social information; social learning; Trachops cirrhosus
10.  Social Familiarity Governs Prey Patch-Exploitation, - Leaving and Inter-Patch Distribution of the Group-Living Predatory Mite Phytoseiulus persimilis 
PLoS ONE  2012;7(8):e42889.
Background
In group-living animals, social interactions and their effects on other life activities such as foraging are commonly determined by discrimination among group members. Accordingly, many group-living species evolved sophisticated social recognition abilities such as the ability to recognize familiar individuals, i.e. individuals encountered before. Social familiarity may affect within-group interactions and between-group movements. In environments with patchily distributed prey, group-living predators must repeatedly decide whether to stay with the group in a given prey patch or to leave and search for new prey patches and groups.
Methodology/Principal Findings
Based on the assumption that in group-living animals social familiarity allows to optimize the performance in other tasks, as for example predicted by limited attention theory, we assessed the influence of social familiarity on prey patch exploitation, patch-leaving, and inter-patch distribution of the group-living, plant-inhabiting predatory mite Phytoseiulus persimilis. P. persimilis is highly specialized on herbivorous spider mite prey such as the two-spotted spider mite Tetranychus urticae, which is patchily distributed on its host plants. We conducted two experiments with (1) groups of juvenile P. persimilis under limited food on interconnected detached leaflets, and (2) groups of adult P. persimilis females under limited food on whole plants. Familiar individuals of both juvenile and adult predator groups were more exploratory and dispersed earlier from a given spider mite patch, occupied more leaves and depleted prey more quickly than individuals of unfamiliar groups. Moreover, familiar juvenile predators had higher survival chances than unfamiliar juveniles.
Conclusions/Significance
We argue that patch-exploitation and -leaving, and inter-patch dispersion were more favorably coordinated in groups of familiar than unfamiliar predators, alleviating intraspecific competition and improving prey utilization and suppression.
doi:10.1371/journal.pone.0042889
PMCID: PMC3416787  PMID: 22900062
11.  Do naive juvenile seabirds forage differently from adults? 
Foraging skills of young individuals are assumed to be inferior to those of adults. The reduced efficiency of naive individuals may be the primary cause of the high juvenile mortality and explain the deferment of maturity in long-lived species. However, the study of juvenile and immature foraging behaviour has been limited so far. We used satellite telemetry to compare the foraging movements of juveniles, immatures and breeding adult wandering albatrosses Diomedea exulans, a species where foraging success is positively influenced by the distance covered daily. We showed that juveniles are able to use favourable winds as soon as the first month of independence, but cover shorter distances daily and spend more time sitting on water than adults during the first two months after fledging. These reduced movement capacities do not seem to be the cause of higher juvenile mortality. Moreover, juveniles almost never restrict their movement to specific areas, as adults and immatures frequently do over shelf edges or oceanic zones, which suggest that the location of appropriate areas is learned through experience. Immatures and adults have equivalent movement capacities, but when they are central place foragers, i.e. when adults breed or immatures come to the colony to display and pair, immatures make shorter trips than adults. The long duration of immaturity in this species seems to be related to a long period of learning to integrate the foraging constraints associated with reproduction and central place foraging. Our results indicate that foraging behaviour of young albatrosses is partly innate and partly learned progressively over immaturity. The first months of learning appear critical in terms of survival, whereas the long period of immaturity is necessary for young birds to attain the skills necessary for efficient breeding without fitness costs.
doi:10.1098/rspb.2013.1434
PMCID: PMC3757974  PMID: 23926153
albatross; learning; movement; immaturity; telemetry
12.  Modelling the Effects of Prey Size and Distribution on Prey Capture Rates of Two Sympatric Marine Predators 
PLoS ONE  2013;8(11):e79915.
Understanding how prey capture rates are influenced by feeding ecology and environmental conditions is fundamental to assessing anthropogenic impacts on marine higher predators. We compared how prey capture rates varied in relation to prey size, prey patch distribution and prey density for two species of alcid, common guillemot (Uria aalge) and razorbill (Alca torda) during the chick-rearing period. We developed a Monte Carlo approach parameterised with foraging behaviour from bird-borne data loggers, observations of prey fed to chicks, and adult diet from water-offloading, to construct a bio-energetics model. Our primary goal was to estimate prey capture rates, and a secondary aim was to test responses to a set of biologically plausible environmental scenarios. Estimated prey capture rates were 1.5±0.8 items per dive (0.8±0.4 and 1.1±0.6 items per minute foraging and underwater, respectively) for guillemots and 3.7±2.4 items per dive (4.9±3.1 and 7.3±4.0 items per minute foraging and underwater, respectively) for razorbills. Based on species' ecology, diet and flight costs, we predicted that razorbills would be more sensitive to decreases in 0-group sandeel (Ammodytes marinus) length (prediction 1), but guillemots would be more sensitive to prey patches that were more widely spaced (prediction 2), and lower in prey density (prediction 3). Estimated prey capture rates increased non-linearly as 0-group sandeel length declined, with the slope being steeper in razorbills, supporting prediction 1. When prey patches were more dispersed, estimated daily energy expenditure increased by a factor of 3.0 for guillemots and 2.3 for razorbills, suggesting guillemots were more sensitive to patchier prey, supporting prediction 2. However, both species responded similarly to reduced prey density (guillemot expenditure increased by 1.7; razorbill by 1.6), thus not supporting prediction 3. This bio-energetics approach complements other foraging models in predicting likely impacts of environmental change on marine higher predators dependent on species-specific foraging ecologies.
doi:10.1371/journal.pone.0079915
PMCID: PMC3829866  PMID: 24260318
13.  Ocean climate and seal condition 
BMC Biology  2005;3:9.
Background
The condition of many marine mammals varies with fluctuations in productivity and food supply in the ocean basin where they forage. Prey is impacted by physical environmental variables such as cyclic warming trends. The weaning weight of northern elephant seal pups, Mirounga angustirostris, being closely linked to maternal condition, indirectly reflects prey availability and foraging success of pregnant females in deep waters of the northeastern Pacific. The aim of this study was to examine the effect of ocean climate on foraging success in this deep-diving marine mammal over the course of three decades, using cohort weaning weight as the principal metric of successful resource accrual.
Results
The mean annual weaning weight of pups declined from 1975 to the late 1990s, a period characterized by a large-scale, basin-wide warm decadal regime that included multiple strong or long-duration El Niños; and increased with a return to a cool decadal regime from about 1999 to 2004. Increased foraging effort and decreased mass gain of adult females, indicative of reduced foraging success and nutritional stress, were associated with high ocean temperatures.
Conclusion
Despite ranging widely and foraging deeply in cold waters beyond coastal thermoclines in the northeastern Pacific, elephant seals are impacted significantly by ocean thermal dynamics. Ocean warming redistributes prey decreasing foraging success of females, which in turn leads to lower weaning mass of pups. Annual fluctuations in weaning mass, in turn, reflect the foraging success of females during the year prior to giving birth and signals changes in ocean temperature cycles.
doi:10.1186/1741-7007-3-9
PMCID: PMC1082885  PMID: 15794819
14.  Opportunistic mothers: female marmosets (Callithrix kuhlii) reduce their investment in offspring when they have to, and when they can 
Journal of human evolution  2005;49(1):122-142.
All female primates incur energetic costs associated with producing and caring for offspring, but females belonging to the New World primate family Callitrichidae, the marmosets and tamarins, appear to face even further demands. In fact, the energetic demands of rearing callitrichid infants are thought to have led to the evolution of cooperative infant care in these species. If this explanation is true, then one might expect that natural selection should also have shaped patterns of maternal behavior to be sensitive to the costs of reproduction and equipped females to reduce their investment in offspring under certain conditions. Therefore, we examined the maternal effort and postpartum endocrine profiles of individual female marmosets (Callithrix kuhlii) across conditions that represented two hallmarks of callitrichid reproduction—conception during the early postpartum period and alloparental assistance. When females conceived during the early postpartum period and faced the upcoming demands of caring for their newly conceived litters (Study 1), they significantly reduced their caregiving effort and had significantly higher postpartum levels of estradiol relative to breeding attempts in which conception occurred later in the postpartum period. Postpartum estradiol was negatively correlated with maternal carrying effort. When experienced alloparents were present (Study 2), females again reduced their caregiving effort relative to breeding attempts in which experienced alloparents were not present. Postpartum cortisol, however, did not vary as a function of experienced alloparental assistance. The results of these studies suggest that female marmosets have been subjected to similar selection pressures as females of other primate taxa—to maximize their reproductive success by reducing their investment in offspring under the worst and best of conditions—and suggest that hormones may mediate within-female variation in maternal care. These studies also provide support for the notion that mothers are “flexible opportunists” when it comes to providing care to their young.
doi:10.1016/j.jhevol.2005.04.003
PMCID: PMC2987622  PMID: 15935439
Wied’s black tufted-ear marmoset; Callitrichidae; Maternal care; Postpartum conception; Lactation; Alloparental care
15.  Gustatory Perception and Fat Body Energy Metabolism Are Jointly Affected by Vitellogenin and Juvenile Hormone in Honey Bees 
PLoS Genetics  2012;8(6):e1002779.
Honey bees (Apis mellifera) provide a system for studying social and food-related behavior. A caste of workers performs age-related tasks: young bees (nurses) usually feed the brood and other adult bees inside the nest, while older bees (foragers) forage outside for pollen, a protein/lipid source, or nectar, a carbohydrate source. The workers' transition from nursing to foraging and their foraging preferences correlate with differences in gustatory perception, metabolic gene expression, and endocrine physiology including the endocrine factors vitellogenin (Vg) and juvenile hormone (JH). However, the understanding of connections among social behavior, energy metabolism, and endocrine factors is incomplete. We used RNA interference (RNAi) to perturb the gene network of Vg and JH to learn more about these connections through effects on gustation, gene transcripts, and physiology. The RNAi perturbation was achieved by single and double knockdown of the genes ultraspiracle (usp) and vg, which encode a putative JH receptor and Vg, respectively. The double knockdown enhanced gustatory perception and elevated hemolymph glucose, trehalose, and JH. We also observed transcriptional responses in insulin like peptide 1 (ilp1), the adipokinetic hormone receptor (AKHR), and cGMP-dependent protein kinase (PKG, or “foraging gene” Amfor). Our study demonstrates that the Vg–JH regulatory module controls changes in carbohydrate metabolism, but not lipid metabolism, when worker bees shift from nursing to foraging. The module is also placed upstream of ilp1, AKHR, and PKG for the first time. As insulin, adipokinetic hormone (AKH), and PKG pathways influence metabolism and gustation in many animals, we propose that honey bees have conserved pathways in carbohydrate metabolism and conserved connections between energy metabolism and gustatory perception. Thus, perhaps the bee can make general contributions to the understanding of food-related behavior and metabolic disorders.
Author Summary
Communication between internal energetic state and taste perception helps animals control food uptake and maintain normal life functions. Honey bees provide an animal model for studies of food-related behavior, such as the role of taste sensitivity in choice-making between carbohydrate- and protein-rich foods (nectar versus pollen for honey bees). A young bee's taste sensitivity to sugar predicts when she begins foraging later in life and influences her choice of foods. Vitellogenin (Vg), a protein produced in the bee's fat cells, and juvenile hormone (JH) influence honey bee taste perception and food-related behavior. Vg and JH are connected by a feedback loop, and we perturbed this Vg–JH circuit using a double gene knockdown approach. In response, bees became more sensitive to sugar, had higher sugar levels in the blood, and died faster during starvation, while lipid levels remained constant. We identified that insulin like peptide 1 (ilp1), the adipokinetic hormone receptor (AKHR), and PKG (the foraging gene) were altered in the bees' fat cells after the perturbation. Our study demonstrates a new role for the Vg–JH circuit in honey bee carbohydrate metabolism, and it places Vg–JH upstream of the three metabolic genes that have conserved roles in food-related behaviors and energy metabolism in many animals.
doi:10.1371/journal.pgen.1002779
PMCID: PMC3386229  PMID: 22761585
16.  Seasonal Diet and Prey Preference of the African Lion in a Waterhole-Driven Semi-Arid Savanna 
PLoS ONE  2013;8(2):e55182.
Large carnivores inhabiting ecosystems with heterogeneously distributed environmental resources with strong seasonal variations frequently employ opportunistic foraging strategies, often typified by seasonal switches in diet. In semi-arid ecosystems, herbivore distribution is generally more homogeneous in the wet season, when surface water is abundant, than in the dry season when only permanent sources remain. Here, we investigate the seasonal contribution of the different herbivore species, prey preference and distribution of kills (i.e. feeding locations) of African lions in Hwange National Park, Zimbabwe, a semi-arid African savanna structured by artificial waterholes. We used data from 245 kills and 74 faecal samples. Buffalo consistently emerged as the most frequently utilised prey in all seasons by both male (56%) and female (33%) lions, contributing the most to lion dietary biomass. Jacobs’ index also revealed that buffalo was the most intensively selected species throughout the year. For female lions, kudu and to a lesser extent the group “medium Bovidae” are the most important secondary prey. This study revealed seasonal patterns in secondary prey consumption by female lions partly based on prey ecology with browsers, such as giraffe and kudu, mainly consumed in the early dry season, and grazers, such as zebra and suids, contributing more to female diet in the late dry season. Further, it revealed the opportunistic hunting behaviour of lions for prey as diverse as elephants and mice, with elephants taken mostly as juveniles at the end of the dry season during droughts. Jacobs’ index finally revealed a very strong preference for kills within 2 km from a waterhole for all prey species, except small antelopes, in all seasons. This suggested that surface-water resources form passive traps and contribute to the structuring of lion foraging behaviour.
doi:10.1371/journal.pone.0055182
PMCID: PMC3566210  PMID: 23405121
17.  Foraging Responses of Black-Legged Kittiwakes to Prolonged Food-Shortages around Colonies on the Bering Sea Shelf 
PLoS ONE  2014;9(3):e92520.
We hypothesized that changes in southeastern Bering Sea foraging conditions for black-legged kittiwakes (Rissa tridactyla) have caused shifts in habitat use with direct implications for population trends. To test this, we compared at-sea distribution, breeding performance, and nutritional stress of kittiwakes in three years (2008–2010) at two sites in the Pribilof Islands, where the population has either declined (St. Paul) or remained stable (St. George). Foraging conditions were assessed from changes in (1) bird diets, (2) the biomass and distribution of juvenile pollock (Theragra chalcogramma) in 2008 and 2009, and (3) eddy kinetic energy (EKE; considered to be a proxy for oceanic prey availability). In years when biomass of juvenile pollock was low and patchily distributed in shelf regions, kittiwake diets included little or no neritic prey and a much higher occurrence of oceanic prey (e.g. myctophids). Birds from both islands foraged on the nearby shelves, or made substantially longer-distance trips overnight to the basin. Here, feeding was more nocturnal and crepuscular than on the shelf, and often occurred near anticyclonic, or inside cyclonic eddies. As expected from colony location, birds from St. Paul used neritic waters more frequently, whereas birds from St. George typically foraged in oceanic waters. Despite these distinctive foraging patterns, there were no significant differences between colonies in chick feeding rates or fledging success. High EKE in 2010 coincided with a 63% increase in use of the basin by birds from St. Paul compared with 2008 when EKE was low. Nonetheless, adult nutritional stress, which was relatively high across years at both colonies, peaked in birds from St. Paul in 2010. Diminishing food resources in nearby shelf habitats may have contributed to kittiwake population declines at St Paul, possibly driven by increased adult mortality or breeding desertion due to high foraging effort and nutritional stress.
doi:10.1371/journal.pone.0092520
PMCID: PMC3966792  PMID: 24671108
18.  Maternal Food Provisioning in a Substrate-Brooding African Cichlid 
PLoS ONE  2014;9(6):e99094.
Fish demonstrate the greatest variety of parental care strategies within the animal kingdom. Fish parents seldom provision food for offspring, with some exceptions predominantly found in substrate-brooding Central American cichlids and mouth-brooding African cichlids. Here, we provide the first evidence of food provisioning in a substrate-brooding African cichlid Neolamprologus mondabu. This fish is a maternal substrate-brooding cichlid endemic to Lake Tanganyika, and feeds on benthic animals using unique techniques–individuals typically feed on the surface of sandy substrates, but also expose prey by digging up substrates with vigorous wriggling of their body and fins. Young also feed on benthos on the substrate surface, but only using the first technique. We observed that feeding induced by digging accounted for 30% of total feeding bouts in adult females, demonstrating that digging is an important foraging tactic. However, parental females fed less frequently after digging than non-parental females, although both females stayed in pits created by digging for approximately 30 s. Instead, young gathered in the pit and fed intensively, suggesting that parental females provision food for young by means of digging. We tested this hypothesis by comparing the feeding frequency of young before and after digging that was simulated by hand, and observed that young doubled their feeding frequency after the simulated digging. This suggests that parental females engage in digging to uncover food items that are otherwise unavailable to young, and provision food for them at the expense of their own foraging. This behavior was similar to what has been observed in Central American cichlids.
doi:10.1371/journal.pone.0099094
PMCID: PMC4049616  PMID: 24911060
19.  Behavioral flexibility of the trawling long-legged bat, Macrophyllum macrophyllum (Phyllostomidae) 
We assessed the behavioral flexibility of the trawling long-legged bat, Macrophyllum macrophyllum (Phyllostomidae) in flight cage experiments by exposing it to prey suspended from nylon threads in the air and to food placed onto the water surface at varying distances to clutter-producing background (water plants). The bat revealed flexibility in foraging mode and caught prey in the air (aerial hawking) and from the water surface (trawling). M. macrophyllum was constrained in finding food very near to and within clutter. As echolocation was the prime sensory mode used by M. macrophyllum for detection and localization of food, the bat might have been unable to perceive sufficient information from prey near clutter as background echoes from the water plant increasingly overlapped with echoes from food. The importance of echolocation for foraging is reflected in a stereotypic call pattern of M. macrophyllum that resembles other aerial insectivorous and trawling bats with a pronounced terminal phase (buzz) prior to capture attempts. Our findings contrast studies of other phyllostomid bats that glean prey very near or from vegetation, often using additional sensory cues, such as prey-produced noise, to find food and that lack a terminal phase in echolocation behavior. In M. macrophyllum, acoustic characteristics of its foraging habitat have shaped its sonar system more than phylogeny.
doi:10.3389/fphys.2013.00342
PMCID: PMC3838978  PMID: 24324442
sensory ecology; aerial hawking; gleaning; bat echolocation; clutter; echo overlap
20.  Restricting Prey Dispersal Can Overestimate the Importance of Predation in Trophic Cascades 
PLoS ONE  2013;8(2):e55100.
Predators can affect prey populations and, via trophic cascades, predators can indirectly impact resource populations (2 trophic levels below the predator) through consumption of prey (density-mediated indirect effects; DMIEs) and by inducing predator-avoidance behavior in prey (trait-mediated indirect effects; TMIEs). Prey often employ multiple predator-avoidance behaviors, such as dispersal or reduced foraging activity, but estimates of TMIEs are usually on individual behaviors. We assessed direct and indirect predator effects in a mesocosm experiment using a marine food chain consisting of a predator (toadfish – Opsanus tau), prey (mud crab - Panopeus herbstii) and resource (ribbed mussel – Geukensia demissa). We measured dispersal and foraging activity of prey separately by manipulating both the presence and absence of the predator, and whether prey could or could not disperse into a predator-free area. Consumption of prey was 9 times greater when prey could not disperse, probably because mesocosm boundaries increased predator capture success. Although predator presence did not significantly affect the number of crabs that emigrated, the presence of a predator decreased resource consumption by prey, which resulted in fewer resources consumed for each prey that emigrated in the presence of a predator, and reduced the overall TMIE. When prey were unable to disperse, TMIEs on mussel survival were 3 times higher than the DMIEs. When prey were allowed to disperse, the TMIEs on resource survival increased to 11-times the DMIEs. We found that restricting the ability of prey to disperse, or focusing on only one predator-avoidance behavior, may be underestimating TMIEs. Our results indicate that the relative contribution of behavior and consumption in food chain dynamics will depend on which predator-avoidance behaviors are allowed to occur and measured.
doi:10.1371/journal.pone.0055100
PMCID: PMC3567106  PMID: 23408957
21.  Tactile experience shapes prey-capture behavior in Etruscan shrews 
A crucial role of tactile experience for the maturation of neural response properties in the somatosensory system is well established, but little is known about the role of tactile experience in the development of tactile behaviors. Here we study how tactile experience affects prey capture behavior in Etruscan shrews, Suncus etruscus. Prey capture in adult shrews is a high-speed behavior that relies on precise attacks guided by tactile Gestalt cues. We studied the role of tactile experience by three different approaches. First, we analyzed the hunting skills of young shrews' right after weaning. We found that prey capture in young animals in most, but not all, aspects is similar to that of adults. Second, we performed whisker trimming for 3–4 weeks after birth. Such deprivation resulted in a lasting disruption of prey capture even after whisker re-growth: attacks lacked precise targeting and had a lower success rate. Third, we presented adult shrews with an entirely novel prey species, the giant cockroach. The shape of this roach is very different from the shrew's normal (cricket) prey and the thorax—the preferred point of attack in crickets—is protected by a heavy cuticle. Initially shrews attacked giant roaches the same way they attack crickets and targeted the thoracic region. With progressive experience, however, shrews adopted a new attack strategy targeting legs and underside of the roaches while avoiding other body parts. Speed and efficiency of attacks improved. These data suggest that tactile experience shapes prey capture behavior.
doi:10.3389/fnbeh.2012.00028
PMCID: PMC3372980  PMID: 22701408
whisker; vibrissa; experience; shrew; Suncus etruscus; object recognition
22.  Does Foraging Behaviour Affect Female Mate Preferences and Pair Formation in Captive Zebra Finches? 
PLoS ONE  2010;5(12):e14340.
Background
Successful foraging is essential for survival and reproductive success. In many bird species, foraging is a learned behaviour. To cope with environmental change and survive periods in which regular foods are scarce, the ability to solve novel foraging problems by learning new foraging techniques can be crucial. Although females have been shown to prefer more efficient foragers, the effect of males' foraging techniques on female mate choice has never been studied. We tested whether females would prefer males showing the same learned foraging technique as they had been exposed to as juveniles, or whether females would prefer males that showed a complementary foraging technique.
Methodology/Principal Findings
We first trained juvenile male and female zebra finches (Taeniopygia guttata) to obtain a significant proportion of their food by one of two foraging techniques. We then tested whether females showed a preference for males with the same or the alternative technique. We found that neither a male's foraging technique nor his foraging performance affected the time females spent in his proximity in the mate-choice apparatus. We then released flocks of these finches into an aviary to investigate whether assortative pairing would be facilitated by birds taught the same technique exploiting the same habitat. Zebra finches trained as juveniles in a specific foraging technique maintained their foraging specialisation in the aviary as adults. However, pair formation and nest location were random with regard to foraging technique.
Conclusions/Significance
Our findings show that zebra finches can be successfully trained to be foraging specialists. However, the robust negative results of the conditions tested here suggest that learned foraging specializations do not affect mate choice or pair formation in our experimental context.
doi:10.1371/journal.pone.0014340
PMCID: PMC3002270  PMID: 21179514
23.  Stomach Temperature Records Reveal Nursing Behaviour and Transition to Solid Food Consumption in an Unweaned Mammal, the Harbour Seal Pup (Phoca vitulina) 
PLoS ONE  2014;9(2):e90329.
Knowledge of milk transfer from mother to offspring and early solid food ingestions in mammals allows for a greater understanding of the factors affecting transition to nutritional independence and pre-weaning growth and survival. Yet studies monitoring suckling behaviour have often relied on visual observations, which might not accurately represent milk intake. We assessed the use of stomach temperature telemetry to monitor suckling and foraging behaviour in free-ranging harbour seal (Phoca vitulina) pups during lactation. Stomach temperature declines were analysed using principal component and cluster analyses, as well as trials using simulated stomachs resulting in a precise classification of stomach temperature drops into milk, seawater and solid food ingestions. Seawater and solid food ingestions represented on average 15.3±1.6% [0–40.0%] and 0.7±0.2% [0–13.0%], respectively, of individual ingestions. Overall, 63.7% of milk ingestions occurred while the pups were in the water, of which 13.9% were preceded by seawater ingestion. The average time between subsequent ingestions was significantly less for seawater than for milk ingestions. These results suggest that seawater ingestion might represent collateral ingestion during aquatic suckling attempts. Alternatively, as solid food ingestions (n = 19) were observed among 7 pups, seawater ingestion could result from missed prey capture attempts. This study shows that some harbour seals start ingesting prey while still being nursed, indicating that weaning occurs more gradually than previously thought in this species. Stomach temperature telemetry represents a promising method to study suckling behaviour in wild mammals and transition to nutritional independence in various endotherm species.
doi:10.1371/journal.pone.0090329
PMCID: PMC3936010  PMID: 24587327
24.  Jellyfish Support High Energy Intake of Leatherback Sea Turtles (Dermochelys coriacea): Video Evidence from Animal-Borne Cameras 
PLoS ONE  2012;7(3):e33259.
The endangered leatherback turtle is a large, highly migratory marine predator that inexplicably relies upon a diet of low-energy gelatinous zooplankton. The location of these prey may be predictable at large oceanographic scales, given that leatherback turtles perform long distance migrations (1000s of km) from nesting beaches to high latitude foraging grounds. However, little is known about the profitability of this migration and foraging strategy. We used GPS location data and video from animal-borne cameras to examine how prey characteristics (i.e., prey size, prey type, prey encounter rate) correlate with the daytime foraging behavior of leatherbacks (n = 19) in shelf waters off Cape Breton Island, NS, Canada, during August and September. Video was recorded continuously, averaged 1:53 h per turtle (range 0:08–3:38 h), and documented a total of 601 prey captures. Lion's mane jellyfish (Cyanea capillata) was the dominant prey (83–100%), but moon jellyfish (Aurelia aurita) were also consumed. Turtles approached and attacked most jellyfish within the camera's field of view and appeared to consume prey completely. There was no significant relationship between encounter rate and dive duration (p = 0.74, linear mixed-effects models). Handling time increased with prey size regardless of prey species (p = 0.0001). Estimates of energy intake averaged 66,018 kJ•d−1 but were as high as 167,797 kJ•d−1 corresponding to turtles consuming an average of 330 kg wet mass•d−1 (up to 840 kg•d−1) or approximately 261 (up to 664) jellyfish•d-1. Assuming our turtles averaged 455 kg body mass, they consumed an average of 73% of their body mass•d−1 equating to an average energy intake of 3–7 times their daily metabolic requirements, depending on estimates used. This study provides evidence that feeding tactics used by leatherbacks in Atlantic Canadian waters are highly profitable and our results are consistent with estimates of mass gain prior to southward migration.
doi:10.1371/journal.pone.0033259
PMCID: PMC3306388  PMID: 22438906
25.  Plasticity of Noddy Parents and Offspring to Sea-Surface Temperature Anomalies 
PLoS ONE  2010;5(7):e11891.
Behavioral and/or developmental plasticity is crucial for resisting the impacts of environmental stressors. We investigated the plasticity of adult foraging behavior and chick development in an offshore foraging seabird, the black noddy (Anous minutus), during two breeding seasons. The first season had anomalously high sea-surface temperatures and ‘low’ prey availability, while the second was a season of below average sea-surface temperatures and ‘normal’ food availability. During the second season, supplementary feeding of chicks was used to manipulate offspring nutritional status in order to mimic conditions of high prey availability. When sea-surface temperatures were hotter than average, provisioning rates were significantly and negatively impacted at the day-to-day scale. Adults fed chicks during this low-food season smaller meals but at the same rate as chicks in the unfed treatment the following season. Supplementary feeding of chicks during the second season also resulted in delivery of smaller meals by adults, but did not influence feeding rate. Chick begging and parental responses to cessation of food supplementation suggested smaller meals fed to artificially supplemented chicks resulted from a decrease in chick demands associated with satiation, rather than adult behavioral responses to chick condition. During periods of low prey abundance, chicks maintained structural growth while sacrificing body condition and were unable to take advantage of periods of high prey abundance by increasing growth rates. These results suggest that this species expresses limited plasticity in provisioning behavior and offspring development. Consequently, responses to future changes in sea-surface temperature and other environmental variation may be limited.
doi:10.1371/journal.pone.0011891
PMCID: PMC2912368  PMID: 20686693

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