Lars Bejder

A method for testing association patterns of social animals

Association indices were originally developed to describe species co-occurrences, but have been used increasingly to measure associations between individuals. However, no statistical method has been published that allows one to test the extent to which the observed association index values differ from those of a randomly associating population. Here, we describe an adaptation of a test developed by Manly (1995, Ecology, 76, 1109-1115), which uses the observed association data as a basis for a computer-generated randomization. The observed pattern of association is tested against a randomly created one while retaining important features of the original data, for example group size and sighting frequency. We applied this new method to test four data sets of associations from two populations of Hectors dolphin, Cephalorhynchus hectori, using the Half-Weight Index (HWI) as an example of a measure of association. The test demonstrated that populations with similar median HWI values showed clear differences in association patterns, that is, some were associating nonrandomly whereas others were not. These results highlight the benefits of using this new testing method in order to validate the analysis of association indices. Copyright 1998 The Association for the Study of Animal Behaviour.

Interpreting short-term behavioural responses to disturbance within a longitudinal perspective

We documented immediate, behavioural responses of Indo-Pacific bottlenose dolphins (Tursiops sp.) to experimental vessel approaches in regions of high and low vessel traffic in Shark Bay, Western Australia. Experimental vessel approaches elicited significant changes in the behaviour of targeted dolphins when compared with their behaviour before and after approaches. During approaches, focal dolphin groups became more compact, had higher rates of change in membership and had more erratic speeds and directions of travel. Dolphins in the region of low vessel traffic (control site) had stronger and longer-lasting responses than did dolphins in the region of high vessel traffic (impact site). In the absence of additional information, the moderated behavioural responses of impact-site dolphins probably would be interpreted to mean that long-term vessel activity within a region of tourism had no detrimental effect on resident dolphins. However, another study showed that dolphin-watching tourism in Shark Bay has contributed to a long-term decline in dolphin abundance within the impact site (Bejder et al., in press, Conservation Biology). Those findings suggest that we documented moderated responses not because impact-site dolphins had become habituated to vessels but because those individuals that were sensitive to vessel disturbance left the region before our study began. This reinterpretation of our findings led us to question the traditional premise that short-term behavioural responses are sufficient indicators of impacts of anthropogenic disturbance on wildlife.

Social and genetic interactions drive fitness variation in a free-living dolphin population

The evolutionary forces that drive fitness variation in species are of considerable interest. Despite this, the relative importance and interactions of genetic and social factors involved in the evolution of fitness traits in wild mammalian populations are largely unknown. To date, a few studies have demonstrated that fitness might be influenced by either social factors or genes in natural populations, but none have explored how the combined effect of social and genetic parameters might interact to influence fitness. Drawing from a long-term study of wild bottlenose dolphins in the eastern gulf of Shark Bay, Western Australia, we present a unique approach to understanding these interactions. Our study shows that female calving success depends on both genetic inheritance and social bonds. Moreover, we demonstrate that interactions between social and genetic factors also influence female fitness. Therefore, our study represents a major methodological advance, and provides critical insights into the interplay of genetic and social parameters of fitness.

Testing association patterns: issues arising and extensions

A reasonable necessary condition for a population to be socially structured is that individuals associate in a nonrandom fashion. Thus, testing for preferred or avoided companions is a fundamental step in analyses of social structure (Whitehead & Dufault 1999). Cluster analyses, sociograms and their ilk (e.g. Morgan et al. 1976) all assume nonrandom associations, and if associations are random, none of these mean anything. Unfortunately testing nonrandom association on real data is not simple. A suitable test statistic is the standard deviation of the association indexes, which will be higher than expected if individuals have preferred or avoided associates. But what is ‘expected’ in the case of no preference or avoidance? The distributions of the standard deviation of association indexes, or any other suitable test statistic, are not analytically tractable under the null hypothesis. A solution is to use permutation tests in which the association data are randomized many times subject to certain constraints, each time calculating the test statistic (Manly 1997). The mean of these randomized test statistics can be considered its ‘expected value’, and a P value is then calculated as the proportion of times that the permuted statistics are more extreme than the real test statistic. A number of analyses of animal social structure have taken this approach (e.g. Whitehead et al., 1982, Smolker et al., 1992, Slooten et al., 1993 and Pepper et al., 1999). However, it was not easy to design an efficient computational routine that randomly permutes the records of which individuals were found in which groups in such a way that the number of individuals in each group and the number of groups containing each individual are both held constant. There are conceptual difficulties with such tests (Manly 1997).

Limbs in whales and limblessness in other vertebrates: mechanisms of evolutionary and developmental transformation and loss

SUMMARY We address the developmental and evolutionary mechanisms underlying fore‐ and hindlimb development and progressive hindlimb reduction and skeletal loss in whales and evaluate whether the genetic, developmental, and evolutionary mechanisms thought to be responsible for limb loss in snakes “explain” loss of the hindlimbs in whales. Limb loss and concurrent morphological and physiological changes associated with the transition from land to water are discussed within the context of the current whale phylogeny. Emphasis is placed on fore‐ and hindlimb development, how the forelimbs transformed into flippers, and how the hindlimbs regressed, leaving either no elements or vestigial skeletal elements. Hindlimbs likely began to regress only after the ancestors of whales entered the aquatic environment: Hindlimb function was co‐opted by the undulatory vertical axial locomotion made possible by the newly evolved caudal flukes. Loss of the hindlimbs was associated with elongation of the body during the transition from land to water. Limblessness in most snakes is also associated with adoption of a new (burrowing) lifestyle and was driven by developmental changes associated with elongation of the body. Parallels between adaptation to burrowing or to the aquatic environment reflect structural and functional changes associated with the switch to axial locomotion. Because they are more fully studied and to determine whether hindlimb loss in lineages that are not closely related could result from similar genetically controlled developmental pathways, we discuss developmental (cellular and genetic) processes that may have driven limb loss in snakes and leg‐less lizards and compare these processes to the loss of hindlimbs in whales. In neither group does ontogenetic or phylogenetic limb reduction result from failure to initiate limb development. In both groups limb loss results from arrested development at the limb bud stage, as a result of inability to maintain necessary inductive tissue interactions and enhanced cell death over that seen in limbed tetrapods. An evolutionary change in Hox gene expression—as occurs in snakes—or in Hox gene regulation—as occurs in some limb‐less mutants—is unlikely to have initiated loss of the hindlimbs in cetaceans. Selective pressures acting on a wide range of developmental processes and adult traits other than the limbs are likely to have driven the loss of hindlimbs in whales.

Home range overlap, matrilineal and biparental kinship drive female associations in bottlenose dolphins

Few studies of kinship in mammalian societies have been able to consider the complex interactions between home range overlap, association patterns and kinship, which have created a critical gap in our understanding of social evolution. We investigated the association patterns of female bottlenose dolphins, Tursiops aduncus, in the eastern gulf of Shark Bay, Western Australia and found that they depended upon the complex interplay of at least three factors: home range overlap, matrilineal kinship and biparental kinship. While home range overlap was positively correlated with female association patterns, preferred associations were found between females showing as little as 27% home range overlap, and some pairs showed avoidance despite 100% home range overlap. Furthermore, on average, both casual and preferred associations took place between females that were more closely biparentally related than expected by chance and this pattern varied depending upon whether or not pairs of females shared the same matriline.

Biosonar adjustments to target range of echolocating bottlenose dolphins(Tursiops sp.) in the wild

SUMMARY Toothed whales use echolocation to locate and track prey. Most knowledge of toothed whale echolocation stems from studies on trained animals, and little is known about how toothed whales regulate and use their biosonar systems in the wild. Recent research suggests that an automatic gain control mechanism in delphinid biosonars adjusts the biosonar output to the one-way transmission loss to the target, possibly a consequence of pneumatic restrictions in how fast the sound generator can be actuated and still maintain high outputs. This study examines the relationships between target range (R), click intervals, and source levels of wild bottlenose dolphins (Tursiops sp.) by recording regular (non-buzz) echolocation clicks with a linear hydrophone array. Dolphins clicked faster with decreasing distance to the array, reflecting a decreasing delay between the outgoing echolocation click and the returning array echo. However, for interclick intervals longer than 30–40 ms, source levels were not limited by the repetition rate. Thus, pneumatic constraints in the sound-production apparatus cannot account for source level adjustments to range as a possible automatic gain control mechanism for target ranges longer than a few body lengths of the dolphin. Source level estimates drop with reducing range between the echolocating dolphins and the target as a function of 17 log(R). This may indicate either (1) an active form of time-varying gain in the biosonar independent of click intervals or (2) a bias in array recordings towards a 20 log(R) relationship for apparent source levels introduced by a threshold on received click levels included in the analysis.

Source parameters of echolocation clicks from wild bottlenose dolphins (Tursiops aduncus and Tursiops truncatus)

The Indian Ocean and Atlantic bottlenose dolphins (Tursiops aduncus and Tursiops truncatus) are among the best studied echolocating toothed whales. However, almost all echolocation studies on bottlenose dolphins have been made with captive animals, and the echolocation signals of free-ranging animals have not been quantified. Here, biosonar source parameters from wild T. aduncus and T. truncatus were measured with linear three- and four-hydrophone arrays in four geographic locations. The two species had similar source parameters, with source levels of 177-228 dB re 1 μPa peak to peak, click durations of 8-72 μs, centroid frequencies of 33-109 kHz and rms bandwidths between 23 and 54 kHz. T. aduncus clicks had a higher frequency emphasis than T. truncatus. The transmission directionality index was up to 3 dB higher for T. aduncus (29 dB) as compared to T. truncatus (26 dB). The high directionality of T. aduncus does not appear to be only a physical consequence of a higher frequency emphasis in clicks, but may also be caused by differences in the internal properties of the sound production system.

An integrated and adaptive management model to address the long-term sustainability of tourist interactions with cetaceans

Rapid growth in demand for tourist interactions with cetaceans in the wild constitutes a challenge to management. Short-term animal behaviour changes can have long-term biological consequences for individual animals and populations. This paper reviews the whale-watching management context, describing the interplay of the macro (global), meso (national/regional) and micro-level (local/site specific) policy, planning and management settings. Here, an integrated and adaptive management model based largely upon the delineation and monitoring of limits of acceptable change (LAC) parameters is proposed to address current shortcomings in the long-term sustainable management of whale-watching activities. Although no integrated management framework currently exists, a comprehensive management approach must be developed and applied in the interests of the long-term sustainable management of tourist interactions with cetaceans in the wild. The proposed management model highlights the importance of integrating multiple stakeholder perspectives in a way that is both research-informed and adaptive. Beyond tourist interactions with cetaceans, this management framework could be applied to a wide range of wildlife management contexts.

Population differentiation and hybridisation of Australian snubfin (Orcaella heinsohni) and Indo-Pacific humpback (Sousa chinensis) dolphins in North-Western Australia

Little is known about the Australian snubfin (Orcaella heinsohni) and Indo-Pacific humpback (Sousa chinensis) dolphins (‘snubfin’ and ‘humpback dolphins’, hereafter) of north-western Australia. While both species are listed as ‘near threatened’ by the IUCN, data deficiencies are impeding rigorous assessment of their conservation status across Australia. Understanding the genetic structure of populations, including levels of gene flow among populations, is important for the assessment of conservation status and the effective management of a species. Using nuclear and mitochondrial DNA markers, we assessed population genetic diversity and differentiation between snubfin dolphins from Cygnet (n = 32) and Roebuck Bays (n = 25), and humpback dolphins from the Dampier Archipelago (n = 19) and the North West Cape (n = 18). All sampling locations were separated by geographic distances >200 km. For each species, we found significant genetic differentiation between sampling locations based on 12 (for snubfin dolphins) and 13 (for humpback dolphins) microsatellite loci (F ST = 0.05–0.09; P<0.001) and a 422 bp sequence of the mitochondrial control region (F ST = 0.50–0.70; P<0.001). The estimated proportion of migrants in a population ranged from 0.01 (95% CI 0.00–0.06) to 0.13 (0.03–0.24). These are the first estimates of genetic diversity and differentiation for snubfin and humpback dolphins in Western Australia, providing valuable information towards the assessment of their conservation status in this rapidly developing region. Our results suggest that north-western Australian snubfin and humpback dolphins may exist as metapopulations of small, largely isolated population fragments, and should be managed accordingly. Management plans should seek to maintain effective population size and gene flow. Additionally, while interactions of a socio-sexual nature between these two species have been observed previously, here we provide strong evidence for the first documented case of hybridisation between a female snubfin dolphin and a male humpback dolphin.