Modelling the emergence and stability of a vertically transmitted cultural trait in bottlenose dolphins

doi:10.1016/j.anbehav.2012.08.029

Animal Behaviour

Volume 84, Issue 6, December 2012, Pages 1347-1362

https://doi.org/10.1016/j.anbehav.2012.08.029 Get rights and content

An apparently vertically, socially transmitted foraging specialization (‘sponging’) in bottlenose dolphins (Tursiops sp.) is observed in two adjacent gulfs within Shark Bay, Western Australia, where sponging has possibly spread from independent innovations. We designed an individual-based model based on empirical data, to investigate the conditions (of learning fidelity and fitness benefits for spongers) under which sponging could be established and maintained. Simulations show that sponging is unlikely to be established from a single innovation event but the probability increases with independent innovation events. Once established, however, it can be maintained in the absence of fitness benefits for spongers, if learning fidelity of daughters is virtually 100%. Smaller learning fidelities can be compensated for with fitness benefits for spongers, but these benefits must be 5% and 10%, respectively, to compensate for learning fidelities of 96.25% and 92%. Furthermore, we estimated the time since the emergence of sponging by tracking the average pairwise relatedness among spongers over time and comparing it to empirical estimates. For the eastern gulf of Shark Bay, we show that sponging might have been in place for at least 120 years if it originated from a single innovation event. For comparison of vertical, social transmission to other trait acquisition methods, we ran simulations in which sponging was either a genetic trait or acquired solely by innovation. In these simulations, sponging could be maintained but the simulation results and empirical data did not match. Hence vertical social transmission is a more feasible mechanism to explain the spread of sponging.

Highlights

► Sponging is a vertically, socially transmitted foraging behaviour in bottlenose dolphins. ► We investigated sponging stability and establishment with an individual-based model. ► Sponging is stably transmitted under certain conditions of learning fidelity and fitness benefits. ► Based on pairwise relatedness, sponging might have been present for at least 120 years.

Section snippets

The Sponging Behaviour

Despite the low likelihood predicted for vertically, socially transmitted behaviours to be established and maintained, at least one such behaviour (‘sponging’) has been established in each of the two gulfs of Shark Bay, Western Australia (Smolker et al. 1997; Mann et al. 2008; Bacher et al. 2010). A subset of the bottlenose dolphin population wears conical marine sponges on their rostra when apparently foraging along the seafloor (Smolker et al. 1997; Mann et al. 2008). This behaviour appears

The Model

We built an individual-based model of a diploid, sexually reproducing dolphin population in Matlab R2010a (MathWorks, Natick, MA, U.S.A.). Simulations were run and then compared to empirical results from the eastern and western gulfs of Shark Bay independently. The two populations are connected by high dispersal (number of migrants is much greater than one; Crow & Kimura 1970; Krützen et al. 2004a); however, the 110 km separation between the study sites has led to low, but significant, genetic

Sponger Stability

The simulations show that an initial proportion of 0.05 female spongers in the population does not change significantly, under certain conditions of learning fidelity of daughters born to spongers, and fitness benefits for spongers compared to nonspongers (Fig. 1). For example, if the learning fidelity equals 1, there cannot be any fitness costs for spongers otherwise sponging will disappear. With lower learning fidelity, progressively higher fitness benefits are required for stability of the

Discussion

Enquist et al. (2010) showed that conditions for stable vertical transmission from a single cultural parent exist, but are so restrictive as to be very unlikely. However, in this study, we used a different modelling approach to show that there are conditions that allow stable vertical social transmission from a single cultural parent, and that these conditions are representative of a natural population in which vertical transmission is supported by genetic data. Our stochastic model did not

Acknowledgments

This study was inspired by work to be published elsewhere and funded by Sea World Research and Rescue Foundation, National Geographic Society, Claraz-Schenkung, A.-H. Schultz Stiftung and Julius-Klaus Stiftung (grants to Michael Krützen, Lars Bejder and W.S.). We thank Janet Mann, Eric Patterson, Simon Allen and three anonymous referees for their helpful comments. A.M.K. was supported by a UNSW University International Postgraduate Award and by the E&ERC.

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Citation Excerpt :
However, due to the limited number of observations of those individuals, it may also be that we failed to capture some of the connections with other shellers in our dataset. In this context, it is worth noting that sponging appears to have arisen independently in each gulf of Shark Bay [48], highlighting the potential for complex behavioral innovations in this population. Along with sponging [6, 9, 49], shelling represents only the second reported case of tool use in dolphins.
Cultural behavior, which is transmitted among conspecifics through social learning [1], is found across various taxa [2, 3, 4, 5, 6]. Vertical social transmission from parent to offspring [7] is thought to be adaptive because of the parental generation being more skilled than maturing individuals. It is found throughout the animal kingdom, particularly in species with prolonged parental care, e.g., [8, 9]. Social learning can also occur among members of the same generation [4, 10, 11] or between older, non-parental individuals and younger generations [7] via horizontal or oblique transmission, respectively. Extensive work on primate culture has shown that horizontal transmission of foraging behavior is biased toward species with broad cultural repertoires [12] and those with increased levels of social tolerance [13, 14], such as great apes. Vertical social transmission has been established as the primary transmission mechanism of foraging behaviors in the Indo-Pacific bottlenose dolphin (Tursiops aduncus) population of Shark Bay, Western Australia [6, 9, 15, 16]. Here, we investigated the spread of another foraging strategy, “shelling” [17], whereby some dolphins in this population feed on prey trapped inside large marine gastropod shells. Using a multi-network version of “network-based diffusion analysis” (NBDA), we show that shelling behavior spreads primarily through non-vertical social transmission. By statistically accounting for both environmental and genetic influences, our findings thus represent the first evidence of non-vertical transmission of a foraging tactic in toothed whales. This research suggests there are multiple transmission pathways of foraging behaviors in dolphins, highlighting the similarities between cetaceans and great apes in the nature of the transmission of cultural behaviors.
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Given the extended parental care period, the cooperative foraging techniques may be passed down from mothers to offspring (Simões-Lopes et al., 2016). In these two aspects—innovation and vertical transmission—foraging with fishermen resembles the well-studied foraging specialization of dolphins that use marine sponges as tools in Shark Bay (e.g. Kopps et al., 2014; Kopps & Sherwin, 2012; Krützen et al., 2005). At the same time, dolphins learn from unrelated individuals, and this horizontal transmission can occur simultaneously with the tendency to interact more often with those individuals who forage in the same way.
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.
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View full text

Modelling the emergence and stability of a vertically transmitted cultural trait in bottlenose dolphins

Highlights

Section snippets

The Sponging Behaviour

The Model

Sponger Stability

Discussion

Acknowledgments

Animal Behaviour

Trends in Genetics

Animal Behaviour

Animal Behaviour

Journal of Human Evolution

Genes or culture: are mitochondrial genes associated with tool use in bottlenose dolphins (Tursiops sp.)?

Behavior Genetics

Habituated dolphins (Tursiops sp) in Western Australia

Journal of Mammalogy

The bottlenose dolphin: social relationships in a fission–fusion society

Observational conditioning of fear to fear-relevant and fear-irrelevant stimuli in rhesus monkeys

Journal of Abnormal Psychology

An Introduction to Population Genetics Theory

Individual-based modeling of ecological and evolutionary processes

Annual Review of Ecology, Evolution, and Systematics

One cultural parent makes no culture

Animal Behaviour

Individual variation in prey selection by sea otters: patterns, causes and implications

Journal of Animal Ecology

Social learning in animals: empirical studies and theoretical models

BioScience

Introduction to Population Genetics

Social learning of diet and foraging skills by wild immature Bornean orangutans: implications for culture

American Journal of Primatology

Cultural drift: a primary process of culture change

Journal of Anthropological Research

Population structure in an inshore cetacean revealed by microsatellite and mtDNA analysis: bottlenose dolphins (Tursiops sp.) in Shark Bay, Western Australia

Marine Mammal Science

‘O father: where art thou?’ Paternity assessment in an open fission-fusion society of wild bottlenose dolphins (Tursiops sp.) in Shark Bay, Western Australia

Molecular Ecology