Shane Gero

Incorporating uncertainty into the study of animal social networks

Network analysis is rapidly establishing itself as a powerful tool for studying the structure and dynamics of complex systems (Albert & Barabasi, 2002; Newman, 2003). It has proven useful in understanding social interactions among humans and non-humans and how global properties emerge from them (Girvan & Newman, 2002; Watts et al., 2002; Dodds et al., 2003; Lusseau, 2003; Lusseau & Newman, 2004; Croft et al., 2005; Flack et al., 2006; Lusseau, 2007b). It has also been helpful in describing and predicting the behavior of technological networks and some biological systems for which all interactions can be described as known absolute values. However, the application of network analysis to social systems involving non-human organisms has been slower, because it has been difficult to infer the statistical and biological significance of observed network statistics and structures (Croft et al., 2005; Lusseau et al., 2006). Two key aspects have presented difficulties. Firstly, in contrast to some human studies, analysts estimate social relationships among individuals, they do not know them, and often they estimate those based on quite limited data. Researchers estimate relationships by observing interactions or associations between individuals, ranging from behavioral events (such as grooming) to co-occurrence. They can then build relationship measures using interaction rates or association indices (Whitehead & Dufault, 1999). Yet these observations do not represent all the interactions occurring between individuals, they are a sample. Studies in animal network analyses have never discussed sampling uncertainty even though its consequences can greatly affect the results of such analyses when sample size, i.e. the number of times individuals are observed, is small. For example if two individuals are together 50% of the time and so have a true association index (Cairns & Schwager, 1987) of 0.5, if they were identified together 10 times the 95% confidence interval for the estimated association index is about 0.3-0.7 (Whitehead, 2008). A second problem is that most network analyses of non-humans have focused on binary networks, in which relationships are defined as being either present or absent. The matrix that represents the network contains only ones (when two individuals are defined as associated) and zeros (when they are not). Researchers have used binary transformations of continuous matrices of interaction rates or association indices to describe animal social networks. These transformations require certain arbitrary manipulations which can be justified to varying degrees (Lusseau, 2003; Croft et al., 2005). For example, one might decide that association indices smaller than an arbitrary value (say 0.5) should indicate the lack of a relationship (assigned a value of zero in the binary matrix) and those greater than 0.5 as a relationship (assigned a value of one in the binary matrix). Another example is to define pairs of which the association index is greater than expected if interactions occurred by chance as relationships (ones) and others not possessing relationships (zeros). Authors largely ignore these manipulations

Female philopatry in coastal basins and male dispersion across the North Atlantic in a highly mobile marine species, the sperm whale (Physeter macrocephalus).

The mechanisms that determine population structure in highly mobile marine species are poorly understood, but useful towards understanding the evolution of diversity, and essential for effective conservation and management. In this study, we compare putative sperm whale populations located in the Gulf of Mexico, western North Atlantic, Mediterranean Sea and North Sea using mtDNA control region sequence data and 16 polymorphic microsatellite loci. The Gulf of Mexico, western North Atlantic and North Sea populations each possessed similar low levels of haplotype and nucleotide diversity at the mtDNA locus, while the Mediterranean Sea population showed no detectable mtDNA diversity. Mitochondrial DNA results showed significant differentiation between all populations, while microsatellites showed significant differentiation only for comparisons with the Mediterranean Sea, and at a much lower level than seen for mtDNA. Samples from either side of the North Atlantic in coastal waters showed no differentiation for mtDNA, while North Atlantic samples from just outside the Gulf of Mexico (the western North Atlantic sample) were highly differentiated from samples within the Gulf at this locus. Our analyses indicate a previously unknown fidelity of females to coastal basins either side of the North Atlantic, and suggest the movement of males among these populations for breeding.

Overlapping and matching of codas in vocal interactions between sperm whales: insights into communication function

Many animals engage in dyadic vocal exchanges. Studying the patterns of vocal output and spatial arrangement of individuals in these interactions can often reveal information concerning their function. Sperm whales, Physeter macrocephalus, frequently exchange short sequences of clicks, termed codas, in social contexts. We analysed the coda vocalizations of sperm whale social units encountered in two different oceans to test hypotheses about how coda exchanges are organized. We also used a dynamic recording array to estimate the spatial scale of these vocal interactions. Coda production was influenced by the timing and types of codas produced by other unit members, resulting in the production of duet-like sequences of coda exchanges between pairs of whales. Codas were more likely to be made within 2 s of another coda than expected by chance, and whales were more likely to match previously produced codas than expected by chance, although matching appeared to be largely a result of the matching of one particular coda type within each social unit. Patterns of overlapping and matching exchanges did not seem to be correlated with relatedness or social affiliation. These exchanges occurred over a range of spatial scales, and are thus likely to be functional both between whales that are near and between those that are comparatively far from one another. The context of these exchanges, reciprocity in coda overlapping, and the sequencing of exchanges into duet-like chains all suggest that coda overlapping and matching function to reinforce social bonds between whales.

Heterogeneous social associations within a sperm whale, Physeter macrocephalus, unit reflect pairwise relatedness

A good description of a social structure in which individuals live in stable social groups must also capture individual differences in social behaviour in order to understand the selective pressures behind formation and maintenance of those groups. Depending on the evolutionary mechanism acting and the nature of the benefits incurred by individuals, we might expect different patterns of intra-group associations. Female and immature sperm whales (Physeter macrocephalus, Linnaeus 1758) live in stable and partially matrilineal social units. Using photo identification and sloughed skin sampling for genetic determination of sex and relatedness, we investigated patterns of association within a social unit of sperm whales from the eastern Caribbean. Focus was given to how short-term spatio-temporal associations reflect relatedness among unit members. Contrary to previous findings, we found that the patterns of association among members of this unit were heterogeneous and that individuals had preferred associations or avoidances with specific individuals. Furthermore, these preferred associations correlate with relatedness between individuals, such that individuals associated more with their close relatives when variation in sociability of the individuals is controlled. These results are inconsistent with the simple equivalence model of homogeneous associations between members of a social unit. They indicate intra-unit social complexity, a basis for which seems to be genetic relatedness.

Multilevel Societies of Female Sperm Whales (Physeter macrocephalus) in the Atlantic and Pacific: Why Are They So Different?

We can examine the evolution of multilevel societies using comparative studies. Intraspecific comparisons are valuable because confounding factors are reduced. Female sperm whales live in multilevel societies. However, studies at several locations have found substantial and consistent differences in social structure between the eastern Pacific and North Atlantic Oceans, even though nuclear DNA shows no significant differentiation between the populations. In the Pacific, female sperm whales live in nearly permanent social units that typically contain about 11 females and immatures of multiple unrelated matrilines. These units form temporary groups with other units for periods of days, apparently exclusively with other units from the same cultural clan. Clans contain thousands of females, are not distinct in nuclear DNA, but are sympatric and have distinctive culturally determined vocalizations and movement patterns. In the North Atlantic social units rarely group with other units, and there is no evidence for sympatric cultural clans. Possible drivers of these contrasts include oceanographic differences, predation, the effects of whaling, and culture. We suggest that protection against predation by killer whales is the primary reason for grouping in the Pacific, and as killer whales do not seem such a threat in the Atlantic, social units there rarely form groups, and have not evolved the clans that primarily function to structure interunit interactions. This analysis highlighted several factors that may influence the evolution of multilevel societies, ranging from the attributes of resources, to predation, anthropogenic effects, culture, and even the cultures of other species.

Individually distinctive acoustic features in sperm whale codas

Social animals may develop behavioural strategies that are based on individualized relationships among members. In these cases, there might be selection pressures for the development of identity signals and mechanisms that allow discrimination and recognition of particular individuals. Female sperm whales, Physeter macrocephalus, live in long-term, stable social units. Differential interactions among unit members suggest the need for an individual discrimination system. Sperm whales produce stereotyped series of click sounds called codas, which are thought to be used for communication. Although codas were initially proposed as individual signatures, later studies did not support this hypothesis. Using linear discriminant functions and Mantel tests, we tested variation within coda types as a means for individual identification, using recordings where codas were assigned to individual whales. While most coda types showed no indication of individual-specific information, individual differences that were robust to variation among recording days were found in the 5 Regular coda type. Differences in individual-specific information between coda types suggest that different coda types may have distinct functions.

Individual, unit and vocal clan level identity cues in sperm whale codas

The ‘social complexity hypothesis’ suggests that complex social structure is a driver of diversity in animal communication systems. Sperm whales have a hierarchically structured society in which the largest affiliative structures, the vocal clans, are marked on ocean-basin scales by culturally transmitted dialects of acoustic signals known as ‘codas’. We examined variation in coda repertoires among both individual whales and social units—the basic element of sperm whale society—using data from nine Caribbean social units across six years. Codas were assigned to individuals using photo-identification and acoustic size measurement, and we calculated similarity between repertoires using both continuous and categorical methods. We identified 21 coda types. Two of those (‘1+1+3’ and ‘5R1’) made up 65% of the codas recorded, were shared across all units and have dominated repertoires in this population for at least 30 years. Individuals appear to differ in the way they produce ‘5R1’ but not ‘1+1+3’ coda. Units use distinct 4-click coda types which contribute to making unit repertoires distinctive. Our results support the social complexity hypothesis in a marine species as different patterns of variation between coda types suggest divergent functions, perhaps representing selection for identity signals at several levels of social structure.

Socially segregated, sympatric sperm whale clans in the Atlantic Ocean

Sperm whales (Physeter macrocephalus) are unusual in that there is good evidence for sympatric populations with distinct culturally determined behaviour, including potential acoustic markers of the population division. In the Pacific, socially segregated, vocal clans with distinct dialects coexist; by contrast, geographical variation in vocal repertoire in the Atlantic has been attributed to drift. We examine networks of acoustic repertoire similarity and social interactions for 11 social units in the Eastern Caribbean. We find the presence of two socially segregated, sympatric vocal clans whose dialects differ significantly both in terms of categorical coda types produced by each clan (Mantel test between clans: matrix correlation = 0.256; p ≤ 0.001) and when using classification-free similarity which ignores defined types (Mantel test between clans: matrix correlation = 0.180; p ≤ 0.001). The more common of the two clans makes a characteristic 1 + 1 + 3 coda, while the other less often sighted clan makes predominantly regular codas. Units were only observed associating with other units within their vocal clan. This study demonstrates that sympatric vocal clans do exist in the Atlantic, that they define a higher order level of social organization as they do in the Pacific, and suggests that cultural identity at the clan level is probably important in this species worldwide.

Critical Decline of the Eastern Caribbean Sperm Whale Population

Sperm whale (Physeter macrocephalus) populations were expected to rebuild following the end of commercial whaling. We document the decline of the population in the eastern Caribbean by tracing demographic changes of well-studied social units. We address hypotheses that, over a ten-year period of dedicated effort (2005–2015), unit size, numbers of calves and/or calving rates have each declined. Across 16 units, the number of adults decreased in 12 units, increased in two, and showed no change in two. The number of adults per unit decreased at -0.195 individuals/yr (95% CI: -0.080 to -0.310; P = 0.001). The number of calves also declined, but the decline was not significant. This negative trend of -4.5% per year in unit size started in about 2010, with numbers being fairly stable until then. There are several natural and anthropogenic threats, but no well-substantiated cause for the decline.

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.