Mauricio Cantor

The interplay between social networks and culture: theoretically and among whales and dolphins

Culture is increasingly being understood as a driver of mammalian phenotypes. Defined as group-specific behaviour transmitted by social learning, culture is shaped by social structure. However, culture can itself affect social structure if individuals preferentially interact with others whose behaviour is similar, or cultural symbols are used to mark groups. Using network formalism, this interplay can be depicted by the coevolution of nodes and edges together with the coevolution of network topology and transmission patterns. We review attempts to model the links between the spread, persistence and diversity of culture and the network topology of non-human societies. We illustrate these processes using cetaceans. The spread of socially learned begging behaviour within a population of bottlenose dolphins followed the topology of the social network, as did the evolution of the song of the humpback whale between breeding areas. In three bottlenose dolphin populations, individuals preferentially associated with animals using the same socially learned foraging behaviour. Homogeneous behaviour within the tight, nearly permanent social structures of the large matrilineal whales seems to result from transmission bias, with cultural symbols marking social structures. We recommend the integration of studies of culture and society in species for which social learning is an important determinant of behaviour.

The structure of a bottlenose dolphin society is coupled to a unique foraging cooperation with artisanal fishermen.

Diverse and localized foraging behaviours have been reported in isolated populations of many animal species around the world. In Laguna, southern Brazil, a subset of resident bottlenose dolphins (Tursiops truncatus) uses a foraging tactic involving cooperative interactions with local, beach-casting fishermen. We used individual photo-identification data to assess whether cooperative and non-cooperative dolphins were socially segregated. The social structure of the population was found to be a fission–fusion system with few non-random associations, typical for this species. However, association values were greater among cooperative dolphins than among non-cooperative dolphins or between dolphins from different foraging classes. Furthermore, the dolphin social network was divided into three modules, clustering individuals that shared or lacked the cooperative foraging tactic. Space-use patterns were not sufficient to explain this partitioning, indicating a behavioural factor. The segregation of dolphins using different foraging tactics could result from foraging behaviour driving social structure, while the closer association between dolphins engaged in the cooperation could facilitate the transmission and learning of this behavioural trait from conspecifics. This unique case of a dolphin–human interaction represents a valuable opportunity to explore hypotheses on the role of social learning in wild cetaceans.

Multilevel animal societies can emerge from cultural transmission

Multilevel societies, containing hierarchically nested social levels, are remarkable social structures whose origins are unclear. The social relationships of sperm whales are organized in a multilevel society with an upper level composed of clans of individuals communicating using similar patterns of clicks (codas). Using agent-based models informed by an 18-year empirical study, we show that clans are unlikely products of stochastic processes (genetic or cultural drift) but likely originate from cultural transmission via biased social learning of codas. Distinct clusters of individuals with similar acoustic repertoires, mirroring the empirical clans, emerge when whales learn preferentially the most common codas (conformism) from behaviourally similar individuals (homophily). Cultural transmission seems key in the partitioning of sperm whales into sympatric clans. These findings suggest that processes similar to those that generate complex human cultures could not only be at play in non-human societies but also create multilevel social structures in the wild.

Potential seed dispersal by Didelphis albiventris (Marsupialia, Didelphidae) in highly disturbed environment

Urban forests are usually isolated and highly disturbed, however they are important shelters for tolerant animal species. Their food habits expose the different ecological roles these animals perform in the habitat. We analyzed the contribution of Didelphis albiventris Lund (1840), as a seed disperser, to the vegetation renewal of an urban forest fragment, describing its frugivorous diet and testing the viability of ingested seeds. Both male and female of white-eared opossum included a vast variety of items in their diet, mainly invertebrates and fruits. Fruits were consumed during all year round and seasonality was not observed. The majority of consumed fruits was from pioneer plant species, which is common in disturbed areas, in accordance to the opossums opportunistic habits. The viability of ingested seeds, evaluated by linear logistic regression models applied to data from germination tests, was different of the seeds collected directly from ripe fruits; it varied among species, maybe due to the intrinsic characteristics of plant species. As a highly generalist species, D. albiventris can inhabit disturbed environments and then disperse seeds from pioneer plants, where the vegetation must be restored. It is crucial that this process does not depend only on the specialist frugivores, which are frequently absent in urban forest fragments. Therefore, the presence of generalist species of secondary environments has its importance emphasized.Florestas urbanas sao geralmente isoladas e altamente degradadas; contudo sao importantes abrigos para especies de animais tolerantes. Os habitos alimentares destes animais explicitam os diferentes papeis ecologicos que eles desempenham no habitat. Nos analisamos a contribuicao de Didelphis albiventris Lund (1840) como dispersor de sementes para a regeneracao da vegetacao de um fragmento florestal urbano. Para isso, descrevemos sua dieta frugivora e testamos a viabilidade das sementes por ele ingeridas. Tanto machos quanto femeas de gamba-de-orelha-branca incluiram uma grande variedade de itens alimentares na dieta, principalmente invertebrados e frutos. Frutos foram consumidos durante todo o ano e a sazonalidade nao foi observada. A maioria das sementes defecadas era proveniente de plantas pioneiras, comuns em ambientes perturbados, o que concorda com seu habito oportunista. A viabilidade das sementes ingeridas, verificada mediante modelos de regressao logistica linear aplicada a dados de testes de germinacao, foi diferente das sementes obtidas de frutos maduros e variou entre especies, talvez devido a caracteristicas intrinsecas da planta. Enquanto uma especie generalista, D. albiventris e capaz de habitar ambientes perturbados, e dispersar as sementes de plantas de estagio inicial de sucessao, onde a vegetacao necessita ser restaurada. E essencial que este processo nao dependa exclusivamente de frugivoros especialistas, que na maioria das vezes estao ausentes nos fragmentos florestais urbanos. Consequentemente, a presenca de especies generalistas de ambientes secundarios tem sua importância enfatizada.

Nestedness across biological scales

Biological networks pervade nature. They describe systems throughout all levels of biological organization, from molecules regulating metabolism to species interactions that shape ecosystem dynamics. The network thinking revealed recurrent organizational patterns in complex biological systems, such as the formation of semi-independent groups of connected elements (modularity) and non-random distributions of interactions among elements. Other structural patterns, such as nestedness, have been primarily assessed in ecological networks formed by two non-overlapping sets of elements; information on its occurrence on other levels of organization is lacking. Nestedness occurs when interactions of less connected elements form proper subsets of the interactions of more connected elements. Only recently these properties began to be appreciated in one-mode networks (where all elements can interact) which describe a much wider variety of biological phenomena. Here, we compute nestedness in a diverse collection of one-mode networked systems from six different levels of biological organization depicting gene and protein interactions, complex phenotypes, animal societies, metapopulations, food webs and vertebrate metacommunities. Our findings suggest that nestedness emerge independently of interaction type or biological scale and reveal that disparate systems can share nested organization features characterized by inclusive subsets of interacting elements with decreasing connectedness. We primarily explore the implications of a nested structure for each of these studied systems, then theorize on how nested networks are assembled. We hypothesize that nestedness emerges across scales due to processes that, although system-dependent, may share a general compromise between two features: specificity (the number of interactions the elements of the system can have) and affinity (how these elements can be connected to each other). Our findings suggesting occurrence of nestedness throughout biological scales can stimulate the debate on how pervasive nestedness may be in nature, while the theoretical emergent principles can aid further research on commonalities of biological networks.

Cultural turnover among Galápagos sperm whales

While populations may wax and wane, it is rare for an entire population to be replaced by a completely different set of individuals. We document the large-scale relocation of cultural groups of sperm whale off the Galápagos Islands, in which two sympatric vocal clans were entirely replaced by two different ones. Between 1985 and 1999, whales from two clans (called Regular and Plus-One) defined by cultural dialects in coda vocalizations were repeatedly photo-identified off Galápagos. Their occurrence in the area declined through the 1990s; by 2000, none remained. We reassessed Galápagos sperm whales in 2013–2014, identifying 463 new females. However, re-sighting rates were low, with no matches with the Galápagos 1985–1999 population, suggesting an eastward shift to coastal areas. Their vocal repertoires matched those of two other clans (called Short and Four-Plus) found across the Pacific but previously rare or absent around Galápagos. The mechanisms behind this cultural turnover may include large-scale environmental regime shifts favouring clan-specific foraging strategies, and a response to heavy whaling in the region involving redistribution of surviving whales into high-quality habitats. The fall and rise of sperm whale cultures off Galápagos reflect the structuring of the Pacific population into large, enduring clans with dynamic ranges. Long-lasting clan membership illustrates how culture can be bound up in the structure and dynamics of animal populations and so how tracking cultural traits can reveal large-scale population shifts.

Social grooming among Indian short-nosed fruit bats

Social grooming is conspicuous in group-living mammals. Bats are gregarious and may groom each other, but the motivation for such social behaviour remains unclear. Here, we describe patterns and infer function of social grooming in tent-making Indian short-nosed fruit bats. Combining field and captivity observations, we found that males and their harem of females mutually groom and apply bodily secretions to one another in tight clusters. Mutual grooming is more commonly initiated by females, before emergence flight at dusk, and during the non-mating season. The within-harem association pattern suggests males may recognize female reproductive status via social grooming. Chemical analysis of the secretions applied during grooming revealed volatile organic compounds that may be involved in chemosensory-mediated communication and/or mate choice. These fruit bat harems were previously seen as simple aggregations, with limited interactions among individuals. Our findings suggest social grooming is multi-functional, with potential implications for the bats’ social lives.

Linking structure and function in food webs: maximization of different ecological functions generates distinct food web structures

Trophic interactions are central to ecosystem functioning, but the link between food web structure and ecosystem functioning remains obscure. Regularities (i.e. consistent patterns) in food web structure suggest the possibility of regularities in ecosystem functioning, which might be used to relate structure to function. We introduce a novel, genetic algorithm approach to simulate food webs with maximized throughput (a proxy for ecosystem functioning) and compare the structure of these simulated food webs to real empirical food webs using common metrics of food web structure. We repeat this analysis using robustness to secondary extinctions (a proxy for ecosystem resilience) instead of throughput to determine the relative contributions of ecosystem functioning and ecosystem resilience to food web structure. Simulated food webs that maximized robustness were similar to real food webs when connectance (i.e. levels of interaction across the food web) was high, but this result did not extend to food webs with low connectance. Simulated food webs that maximized throughput or a combination of throughput and robustness were not similar to any real food webs. Simulated maximum-throughput food webs differed markedly from maximum-robustness food webs, which suggests that maximizing different ecological functions can generate distinct food web structures. Based on our results, food web structure would appear to have a stronger relationship with ecosystem resilience than with ecosystem throughput. Our genetic algorithm approach is general and is well suited to large, realistically complex food webs. Genetic algorithms can incorporate constraints on structure and can generate outputs that can be compared directly to empirical data. Our method can be used to explore a range of maximization or minimization hypotheses, providing new perspectives on the links between structure and function in ecological systems.

The network organization of protein interactions in the spliceosome is reproduced by the simple rules of food-web models.

The network structure of biological systems provides information on the underlying processes shaping their organization and dynamics. Here we examined the structure of the network depicting protein interactions within the spliceosome, the macromolecular complex responsible for splicing in eukaryotic cells. We show the interactions of less connected spliceosome proteins are nested subsets of the connections of the highly connected proteins. At the same time, the network has a modular structure with groups of proteins sharing similar interaction patterns. We then investigated the role of affinity and specificity in shaping the spliceosome network by adapting a probabilistic model originally designed to reproduce food webs. This food-web model was as successful in reproducing the structure of protein interactions as it is in reproducing interactions among species. The good performance of the model suggests affinity and specificity, partially determined by protein size and the timing of association to the complex, may be determining network structure. Moreover, because network models allow building ensembles of realistic networks while encompassing uncertainty they can be useful to examine the dynamics and vulnerability of intracelullar processes. Unraveling the mechanisms organizing the spliceosome interactions is important to characterize the role of individual proteins on splicing catalysis and regulation.

Spatial consequences for dolphins specialized in foraging with fishermen

According to theory, individuals forage in ways that maximize net energy intake. Distinct foraging strategies may emerge within a population in response to heterogeneous resources, competition and learning, among other drivers. We assessed individual variation in, and ecological consequences of, an unusual, specialized foraging tactic between animals and humans. In southern Brazil, bottlenose dolphins, Tursiops truncatus, herd fish schools towards artisanal fishermen, who cast nets in response to behavioural cues from the dolphins. This apparent cooperative tactic likely involves costs as well as benefits for both interacting parties, but such trade-offs remain poorly understood, especially for dolphins. We show that individual dolphins vary markedly in the frequency with which they interact with fishermen, and that this foraging variation is linked to ranging behaviour. Not all individual dolphins interact with fishermen; those that routinely do so concentrate around the limited interaction sites and have smaller home ranges than independent foragers. This suggests that foraging with fishermen increases foraging success and reduces search costs (i.e. foraging range). Competition for interaction sites may offset such benefits, since some individuals often forage at the high-quality sites while others forage at low-quality sites. Taken together, our findings suggest that two alternative tactics emerge in the population from trade-offs involving food access, foraging area, learning techniques and competition: dolphins either forage by themselves over larger areas on unpredictable resource patches (passing fish schools), or learn to interact with fishermen to access and compete for more predictable resource patches (interaction sites). By revealing some of the ecological drivers of this remarkable human–animal interaction, our study contributes two broader insights. First, specialized foraging can have ranging consequences for individuals and so structure the population spatially; second, interspecific cooperation may be founded upon intraspecific competition.