Bottlenose dolphins that forage with artisanal fishermen whistle differently

Acoustic communication is a taxonomically widespread phenomenon, crucial for social animals. We evaluate social sounds from bottlenose dolphins (Tursiops truncatus) of Laguna, southern Brazil, whose social structure is organized around a cooperative foraging tactic with artisanal fishermen. This tactic involves stereotyped and coordinated behaviour by dolphins and fishermen and is performed by a subset of the dolphin population, splitting it into two distinct social communities. We compared the acoustic parameters and type of whistles emitted by dolphins of the “non‐cooperative” and “cooperative” communities, both during their interactions with fishermen and in times where dolphins were engaged in other types of foraging. Our findings show how dolphins’ social sounds differ between foraging tactics and social communities. The frequencies of six whistle types (ascending, descending, concave, convex, multiple, flat) were significantly dependent on tactics and communities. Ascending whistles were more common than expected during foraging without fishermen, and among dolphins of the non‐cooperative community. Whistle acoustic parameters (duration, number of inclination changes and inflection points, and initial, final, maximum, minimum frequencies) also varied between social communities. In general, whistles emitted by cooperative dolphins, mainly when not interacting with fishermen, tended to be shorter, had higher frequency and more inflections than those emitted by non‐cooperative dolphins. These results suggest that different whistles may convey specific information among dolphins related to foraging, which we hypothesize promote social cohesion among members of the same social community. These differences in acoustic repertoires add a new dimension of complexity to this unique human–animal interaction.     

Where to catch a fish? The influence of foraging tactics on the ecology of bottlenose dolphins (Tursiops truncatus) in Florida Bay,Florida

Observations of bottlenose dolphins ( Tursiops truncatus ) in Florida Bay, Florida, between 2002 and 2005 revealed the use of three distinct foraging tactics. The goal of this study was to identify ecological correlates with tactic use and describe the impact of foraging specializations on the overall habitat use and distribution patterns of this dolphin population. Foraging tactics showed strong association with contrasting environmental characteristics, primarily depth. Locations of two of these tactic groups were spatially repulsed. Analyses of sighting histories of individual dolphins observed at foraging events determined that dolphins which employed one tactic never employed the other, and vice versa . Although bottlenose dolphins have plastic foraging behaviors, dolphins in Florida Bay appear to specialize in one tactic and subsequently limit their overall distribution patterns to coincide with habitats that facilitate success using that foraging tactic. This study demonstrates how foraging behavior can be an ecological determinant of overall dolphin habitat use patterns and works to create spatial structure within a population due to consistent mapping of tactics onto environmental variation. These foraging specializations potentially impact the social and demographic patterns of this dolphin population. The possible evolutionary mechanisms behind this intraspecific variation, including resource limitation and social learning, are considered.     

Social diffusion of novel foraging methods in brown capuchin monkeys (Cebus apella)

It has been reported that wild capuchin monkeys exhibit several group-specific behavioural traditions. By contrast, experiments have found little evidence for the social learning assumed necessary to support such traditions. The present study used a diffusion chain paradigm to investigate whether a novel foraging task could be observationally learned by capuchins (Cebus apella) and then transmitted along a chain of individuals. We used a two-action paradigm to control for independent learning. Either of two methods (lift or slide) could be used to open the door of a foraging apparatus to retrieve food. Two chains were tested (N1=4; N2=5), each beginning with an experimenter-trained model who demonstrated to a partner its group-specific method for opening the foraging apparatus. After the demonstration, if the observer was able to open the apparatus 20 times by either method, then it became the demonstrator for a new subject, thus simulating the spread of a foraging tradition among 'generations' of group members. Each method was transmitted along these respective chains with high fidelity, echoing similar results presently available only for chimpanzees and children. These results provide the first clear evidence for faithful diffusion of alternative foraging methods in monkeys, consistent with claims for capuchin traditions in the wild.     

Advantages of social foraging in crab spiders: Groups capture more and larger prey despite the absence of a web

Among group‐living spiders, subsocial representatives in the family of crab spiders (Thomisidae) are a special case, as they build protective communal leaf nests instead of extensive communal capture webs. It could thus be inferred that antipredator benefits (e.g., enhanced protection in larger nests) rather than foraging‐related advantages (e.g., capture of more and larger prey) promote sociality in this family. Nonetheless, subsocial crab spiders do share prey, and if this behaviour does not reflect mere food scramble but has a cooperative character, crab spiders may offer insights into the evolution of social foraging applicable to many other cooperative predators that hunt without traps. Here, we performed a comparative laboratory feeding experiment on three of the four subsocial crab spider species—Australomisidia ergandros, Australomisidia socialis and Xysticus bimaculatus—to determine if crab spiders derive advantages from foraging in groups. In particular, we tested artificially composed groups of five sibling spiderlings vs. single siblings in terms of prey capture success and prey size preference. Across species, groups had higher prey capture success (measured in terms of capture rates and capture latency) and were more likely to attack large, sharable prey—dynamics leading to reduced food competition among group members in favour of living and foraging in groups. Within groups, we further compared prey extraction efficiency among the three applied social foraging tactics: producing, scrounging and feeding alone. In A. ergandros, individuals were exceptionally efficient when using the non‐cooperative scrounger tactic, which entails feeding on the prey provided by others. Thus, our multispecies comparison confirms foraging advantages in maintaining a cooperative lifestyle for crab spiders, but also demonstrates the relevance of research into exploitation of cooperative foraging in this family.     

Cultural transmission of tool use combined with habitat specializations leads to fine-scale genetic structure in bottlenose dolphins

Socially learned behaviours leading to genetic population structure have rarely been described outside humans. Here, we provide evidence of fine-scale genetic structure that has probably arisen based on socially transmitted behaviours in bottlenose dolphins (Tursiops sp.) in western Shark Bay, Western Australia. We argue that vertical social transmission in different habitats has led to significant geographical genetic structure of mitochondrial DNA (mtDNA) haplotypes. Dolphins with mtDNA haplotypes E or F are found predominantly in deep (more than 10 m) channel habitat, while dolphins with a third haplotype (H) are found predominantly in shallow habitat (less than 10 m), indicating a strong haplotype–habitat correlation. Some dolphins in the deep habitat engage in a foraging strategy using tools. These ‘sponging’ dolphins are members of one matriline, carrying haplotype E. This pattern is consistent with what had been demonstrated previously at another research site in Shark Bay, where vertical social transmission of sponging had been shown using multiple lines of evidence. Using an individual-based model, we found support that in western Shark Bay, socially transmitted specializations may have led to the observed genetic structure. The reported genetic structure appears to present an example of cultural hitchhiking of mtDNA haplotypes on socially transmitted foraging strategies, suggesting that, as in humans, genetic structure can be shaped through cultural transmission.     

Behavioural flexibility and problem-solving in a tropical lizard

The role of behavioural flexibility in responding to new or changing environmental challenges is a central theme in cognitive ecology. Studies of behavioural flexibility have focused mostly on mammals and birds because theory predicts that behavioural flexibility is favoured in species or clades that exploit a diversity of habitats or food sources and/or have complex social structure, attributes not associated with ectothermic vertebrates. Here, we present the results of a series of experiments designed to test cognitive abilities across multiple cognitive modules in a tropical arboreal lizard: Anolis evermanni. This lizard shows behavioural flexibility across multiple cognitive tasks, including solving a novel motor task using multiple strategies and reversal learning, as well as rapid associative learning. This flexibility was unexpected because lizards are commonly believed to have limited cognitive abilities and highly stereotyped behaviour. Our findings indicate that the cognitive abilities of A. evermanni are comparable with those of some endothermic species that are recognized to be highly flexible, and strongly suggest a re-thinking of our understanding of the cognitive abilities of ectothermic tetrapods and of the factors favouring the evolution of behavioural flexibility.     

Surfacers change their dive tactics depending on the aim of the dive: evidence from simultaneous measurements of breaths and energy expenditure

Air-breathing divers are assumed to have evolved to apportion their time between surface and underwater periods to maximize the benefit gained from diving activities. However, whether they change their time allocation depending on the aim of the dive is still unknown. This may be particularly crucial for ‘surfacers’ because they dive for various purposes in addition to foraging. In this study, we counted breath events at the surface and estimated oxygen consumption during resting, foraging and other dives in 11 green turtles (Chelonia mydas) in the wild. Breath events were counted by a head-mounted acceleration logger or direct observation based on an animal-borne video logger, and oxygen consumption was estimated by measuring overall dynamic body acceleration. Our results indicate that green turtles maximized their submerged time, following this with five to seven breaths to replenish oxygen for resting dives. However, they changed their dive tactic during foraging and other dives; they surfaced without depleting their estimated stores of oxygen, followed by only a few breaths for effective foraging and locomotion. These dichotomous surfacing tactics would be the result of behavioural modifications by turtles depending on the aim of each dive.     

Cultural transmission of tool use by Indo-Pacific bottlenose dolphins (Tursiops sp.) provides access to a novel foraging niche

Culturally transmitted tool use has important ecological and evolutionary consequences and has been proposed as a significant driver of human evolution. Such evidence is still scarce in other animals. In cetaceans, tool use has been inferred using indirect evidence in one population of Indo-Pacific bottlenose dolphins (Tursiops sp.), where particular dolphins (‘spongers’) use marine sponges during foraging. To date, evidence of whether this foraging tactic actually provides access to novel food items is lacking. We used fatty acid (FA) signature analysis to identify dietary differences between spongers and non-spongers, analysing data from 11 spongers and 27 non-spongers from two different study sites. Both univariate and multivariate analyses revealed significant differences in FA profiles between spongers and non-spongers between and within study sites. Moreover, FA profiles differed significantly between spongers and non-spongers foraging within the same deep channel habitat, whereas the profiles of non-spongers from deep channel and shallow habitats at this site could not be distinguished. Our results indicate that sponge use by bottlenose dolphins is linked to significant differences in diet. It appears that cultural transmission of tool use in dolphins, as in humans, allows the exploitation of an otherwise unused niche.     

Female-mediated causes and consequences of status change in a social fish

In highly social species, dominant individuals often monopolize reproduction, resulting in reproductive investment that is status dependent. Yet, for subordinates, who typically invest less in reproduction, social status can change and opportunities to ascend to dominant social positions are presented suddenly, requiring abrupt changes in behaviour and physiology. In this study, we examined male reproductive anatomy, physiology and behaviour following experimental manipulations of social status in the cooperatively breeding cichlid fish, Neolamprologus pulcher. This unusual fish species lives in permanent social groups composed of a dominant breeding pair and 1-20 subordinates that form a linear social dominance hierarchy. By removing male breeders, we created 18 breeding vacancies and thus provided an opportunity for subordinate males to ascend in status. Dominant females play an important role in regulating status change, as males successfully ascended to breeder status only when they were slightly larger than the female breeder in their social group. Ascending males rapidly assumed behavioural dominance, demonstrated elevated gonadal investment and androgen concentrations compared with males remaining socially subordinate. Interestingly, to increase gonadal investment ascending males appeared to temporarily restrain somatic growth. These results highlight the complex interactions between social status, reproductive physiology and group dynamics, and underscore a convergent pattern of reproductive investment among highly social, cooperative species.     

Infectious disease,behavioural flexibility and the evolution of culture in primates

Culturally transmitted traits are observed in a wide array of animal species, yet we understand little about the costs of the behavioural patterns that underlie culture, such as innovation and social learning. We propose that infectious diseases are a significant cost associated with cultural transmission. We investigated two hypotheses that may explain such a connection: that social learning and exploratory behaviours (specifically, innovation and extractive foraging) either compensate for existing infection or increase exposure to infectious agents. We used Bayesian comparative methods, controlling for sampling effort, body mass, group size, geographical range size, terrestriality, latitude and phylogenetic uncertainty. Across 127 primate species, we found a positive association between pathogen richness and rates of innovation, extractive foraging and social learning. This relationship was driven by two independent phenomena: socially contagious diseases were positively associated with rates of social learning, and environmentally transmitted diseases were positively associated with rates of exploration. Because higher pathogen burdens can contribute to morbidity and mortality, we propose that parasitism is a significant cost associated with the behavioural patterns that underpin culture, and that increased pathogen exposure is likely to have played an important role in the evolution of culture in both non-human primates and humans.     

Frequency-dependent payoffs and sequential decision-making favour consistent tactic use

Although natural selection should have favoured individuals capable of adjusting the weight they give to personal and social information according to circumstances, individuals generally differ consistently in their individual weighting of both types of information. Such individual differences are correlated with personality traits, suggesting that personality could directly affect individuals' ability to collect personal or social information. Alternatively, the link between personality and information use could simply emerge as a by-product of the sequential decision-making process in a frequency-dependent context. Indeed, when the gains associated with behavioural options depend on the choices of others, an individual's sequence of arrival could constrain its choice of options leading to the emergence of correlated behaviours. Any factor such as personality that affects decision order could thus be correlated with information use. To test this new explanation, we developed an individual-based model that simulates a group of animals engaged in a game of sequential frequency-dependent decision: a producer-scrounger game. Our results confirm that the sequence of decision, in this case enforced by the order in which animals enter a foraging area, consistently influences their mean tactic use and their individual plasticity, an outcome reminiscent of the correlation reported between personality and social information use.     

Dusky dolphin group dynamics and association patterns in Península Valdés,Argentina

We inspected dusky dolphin (Lagenorhynchus obscurus) group dynamics in Golfo Nuevo and found differences in social organization between cold and warm seasons. Surveys were conducted onboard a research vessel, from which we collected behavioral observations and group fission‐fusion data from 2001 to 2008; we also collected photo‐identification data from 2004 to 2012. To analyze association patterns, we calculated half‐weight association index (HWI) and social differentiation (S). We conducted a Monte Carlo permutation test to determine whether observed association patterns were significantly different from random association using a compiled version of SOCPROG 2.7. Group fission and fusion dynamics depended on group behavior, the main activity after the groups' fusion was feeding, and they never fission before socializing. The social structure of dusky dolphins included long‐term preferred companions in the cold season; during the warm season, there were no preferred companions. This seasonal difference in social structure could be related to an accompanying shift in foraging behaviors that appears to be driven by changes in prey availability. If so, then a loosening of bonds among individuals during the warm season, when prey is more available, would reflect these social structure changes.     

Aggressive monopolization of mobile carers by young of a cooperative breeder

Competition between young of the same brood or litter is of particular interest in the fields of behavioural and evolutionary ecology, because the competing individuals are likely to be closely related, where evolutionary theory predicts a greater degree of cooperation. Studies of cooperative breeding species typically concentrate on who contributes care to rearing young, and assume a passive role of the young. Relatively, little attention has been devoted to considering how intralitter competition between young affects the distribution of care in cooperative breeders. In banded mongoose (Mungos mungo) groups, the majority of pups each form a stable exclusive one-to-one association with an adult group member (its 'escort') that is its principal care provider. This paper presents experimental evidence that each pup aggressively defends access to its escort, preventing other pups approaching, and therefore monopolizes the care provided by its escort. Each pup travels with the group and follows its escort, around which its exclusion zone is fixed: a form of mobile territoriality. This represents a novel system of care of young in a mammal species, but has general implications for the study of the distribution of care of young, particularly in cooperative breeding species. Parents and helpers may provide biased care to young, not due to preference but due to the competitive actions of the young within the brood or litter.     

Male reproductive success increases with alliance size in Indo-Pacific bottlenose dolphins (Tursiops aduncus)

1. Determining the extent of variation in male mating strategies and reproductive success is necessary to understand the fitness benefits of social and cooperative behaviour. 2. This study assesses the reproductive success of male Indo-Pacific bottlenose dolphins in a small embayment population where different behavioural strategies of males have previously been identified. Parentage for 44 sampled calves was examined using 23 microsatellite loci and one mitochondrial DNA marker. Our candidate parent pool of 70 males and 64 females contained individuals sampled from both the embayment and adjacent coastal populations. 3. A moderate level of polygyny was detected in our sample. We assigned paternity of 23 calves to 12 males at the strict 95% confidence level and an additional nine calves to two males at the 80% confidence level. The majority (92%) of successful males were identified as residents to the embayment, and 46% of offspring were located within the same social group or community as their father. 4. Our results suggest that the size of alliances was the best predictor of reproductive success for males in this population, while the strength of association among allied males, alliance stability and male ranging patterns had little influence. In line with predictions for male alliances formed between unrelated individuals, we found that reproductive skew within alliances was not large. 5. Together, our genetic and behavioural analyses demonstrate that alliance formation between male dolphins is a successful strategy to enhance reproductive output.     

Complex Social Structure of an Endangered Population of Bottlenose Dolphins (Tursiops truncatus) in the Aeolian Archipelago (Italy)

We investigated social structure and association patterns for a small population of Mediterranean bottlenose dolphins, Tursiops truncatus, inhabiting the Aeolian Archipelago (southern Italy). Specifically we evaluate the role of sex and age composition, residency patterns and interaction with trammel nets on this social organization. Association data for 23 regularly sighted individuals were obtained from summer photoidentification surveys collected from 2005–2012. Using a combined cluster and social network analysis approach, we found associations between dolphins were hierarchically structured, where two mixed-sex social units were subdivided into smaller temporarily dynamic groups. We found non-random and long-term preferred associations in the population; however, the degree of social cohesion, residence pattern and interaction with trammel nets differed considerably between the two social units. Six of eight females occurred in the more resident social unit-1; in addition, social unit-1 individuals had significantly stronger associations, higher preferred associates, lived in larger groups and occurred less frequently with trammel nets. Nine of eleven males were clustered in social unit-2 and five of these males, interacting with trammel nets, formed small groups and preferred associations. We propose that female and male groups associate in the study area during the breeding season and that some males choose to interact with reproductive females forming a distinct but interrelated social unit. Other males may be associating in a larger fission-fusion network, which consists of dolphins that appear to temporarily join the network from the coastal population. We cannot exclude that some males specialized in trammel net foraging, suggesting that this foraging technique may favor a solitary lifestyle. Large group sizes and high degree of social cohesion for females could be an indication of greater protection and more efficiency in detecting, deterring or repelling anthropogenic pressures. Most likely dolphins'' social organization depends on a combination of socio-ecological, demographic and anthropogenic factors.     

A neurotoxic pesticide changes the outcome of aggressive interactions between native and invasive ants

Neurotoxic pesticides, such as neonicotinoids, negatively affect the cognitive capacity and fitness of non-target species, and could also modify interspecific interactions. We tested whether sublethal contamination with neonicotinoid could affect foraging, colony fitness and the outcome of behavioural interactions between a native (Monomorium antarcticum) and an invasive ant species (Linepithema humile). The foraging behaviour of both ants was not affected by neonicotinoid exposure. Colonies of the invasive species exposed to the neonicotinoid produced significantly fewer brood. In interspecific confrontations, individuals of the native species exposed to the neonicotinoid lowered their aggression towards the invasive species, although their survival probability was not affected. Exposed individuals of the invasive species interacting with non-exposed native ants displayed increased aggression and had their survival probability reduced. Non-exposed individuals of the invasive species were less aggressive but more likely to survive when interacting with exposed native ants. These results suggest that non-target exposure of invaders to neonicotinoids could either increase or decrease the probability of survival according to the exposure status of the native species. Given that, in any community, different species have different food preferences, and thus different exposure to pesticides, non-target exposure could potentially change the dynamics of communities and influence invasion success.     

Diving for food: a switch of foraging strategy of dusky dolphins in Argentina

During winter, dusky dolphins (Lagenorhynchus obscurus) were observed in coordinated diving apparently in a feeding activity, contrasting with the surface feeding observed during summer. The aim of this work consisted in analyzing the diving activity as an alternative foraging strategy in Argentine dusky dolphins, based on sequential analysis. The study area was Golfo Nuevo, located in Northern Patagonia, Argentina. Random transects were surveyed by a research boat from 2001 to 2007. During behavioral sampling, group members were observed continuously and the predominant activity was recorded at 2-min intervals. Six predominant activities were identified. Each 2-min interval was classified according to the activity at the previous interval (preceding activity), the activity at the interval (following activity), and the season (cold or warm). Z scores were calculated and then used to construct sequence diagrams. An association between diving and milling behavior was observed. This could be another foraging tactics different to the surface foraging sequences and this could be related with the distribution or abundance of preys.     

Blood mercury concentrations in common bottlenose dolphins from the Indian River Lagoon,Florida: Patterns of social distribution

Social network analysis has been shown to be effective in studying the social structure of cetacean populations. Common bottlenose dolphins (Tursiops truncatus) inhabiting the Indian River Lagoon (IRL), Florida, have among the highest concentrations of total mercury (THg) in blood reported worldwide. The purpose of this study was to examine the relationship between THg concentrations in IRL dolphins and their social affiliations. Whole blood samples from 98 dolphins with photo‐identification sighting histories were collected between 2003–2007 and 2010–2012. Dolphins were categorized into approximate tertiles of low (mean 199.7 μg/L), medium (mean 366.8 μg/L), and high (mean 990.5 μg/L) THg exposure. Social associations between individual dolphins were defined by the proportion of sightings documented with another known individual. Social network measures of individuals and associations between dyads were examined to determine differences among THg categories. Strong social affiliations of individuals within the highest category of THg were found (P = 0.04), suggesting shared exposures among dolphins foraging in specific areas of the estuary. Network measures of strength and affinity were significantly higher in the highest exposure category. This report used social network analysis as a novel way to examine patterns of exposure to an environmental contaminant in a cetacean population.     

Vocal learning by greater spear-nosed bats.

Vocal learning is well known among passerine and psittacine birds, but most data on mammals are equivocal. Specific benefits of vocal learning are poorly understood for most species. One case where vocal learning should be favoured by selection is where calls indicate group membership and group mates are unrelated. Female greater spear-nosed bats, Phyllostomus hastatus, live in stable groups of unrelated bats and use loud, broadband calls to coordinate foraging movements of social group mates. Bats benefit from group foraging. Calls differ between female social groups and cave colonies, and playback experiments demonstrate that bats perceive these acoustic differences. Here I show that the group distinctive structure of calls arises through vocal learning. Females change call structure when group composition changes, resulting in increased similarity among new social group mates. Comparisons of transfers with age-matched half-sibs indicate that call changes are not simply due to maturation, the physical environment or heredity. These results suggest that studies testing vocal learning in mammals could profit by focusing on vocalizations that signify group membership.     

Boldness and Information Use in Three‐Spined Sticklebacks

In foraging groups, individuals may utilise information from their social environment to aid decision making when choosing where to search for food. Little work has looked at the costs or benefits of behavioural differences, such as consistent individual variation in boldness, with respect to learning ability. Here, we investigate the response of three‐spined stickleback (Gasterosteus aculeatus) to ‘social cues’, ‘local enhancement’ and ‘public information’ during foraging tasks. Our results confirm previous work suggesting that this species responds to social cues and local enhancement but not public information. Variation in boldness did not affect the use of different types of information. However, time taken to make a choice and reach a patch varied between fish with different levels of boldness. Contrary to expectation, shy fish were the more variable individuals, having a greater range of reaction times when responding to the tasks. This suggests that individual behavioural differences still play a role when utilising information obtained from the environment and may influence the relative benefits that could result in different contexts.