Yannis P. Papastamatiou

Analysis of animal accelerometer data using hidden Markov models

1.Use of accelerometers is now widespread within animal biotelemetry as they provide a means of measuring an animals activity in a meaningful and quantitative way where direct observation is not possible. In sequential acceleration data there is a natural dependence between observations of behaviour, a fact that has been largely ignored in most analyses. n n2.Analyses of acceleration data where serial dependence has been explicitly modelled have largely relied on hidden Markov models (HMMs). Depending on the aim of an analysis, an HMM can be used for state prediction or to make inferences about drivers of behaviour. For state prediction, a supervised learning approach can be applied. That is, an HMM is trained to classify unlabelled acceleration data into a finite set of pre-specified categories. An unsupervised learning approach can be used to infer new aspects of animal behaviour when biologically meaningful response variables are used, with the caveat that the states may not map to specific behaviours. n n3.We will provide the details necessary to implement and assess an HMM in both the supervised and unsupervised learning context and discuss the data requirements of each case. We outline two applications to marine and aerial systems (shark and eagle) taking the unsupervised learning approach, which is more readily applicable to animal activity measured in the field. HMMs were used to infer the effects of temporal, atmospheric and tidal inputs on animal behaviour. n n4.Animal accelerometer data allow ecologists to identify important correlates and drivers of animal activity (and hence behaviour). The HMM framework is well suited to deal with the main features commonly observed in accelerometer data, and can easily be extended to suit a wide range of types of animal activity data. The ability to combine direct observations of animal activity with statistical models, which account for the features of accelerometer data, offers a new way to quantify animal behaviour, energetic expenditure and deepen our insights into individual behaviour as a constituent of populations and ecosystems. n nThis article is protected by copyright. All rights reserved.

Into the deep: the functionality of mesopelagic excursions by an oceanic apex predator

Abstract Comprehension of ecological processes in marine animals requires information regarding dynamic vertical habitat use. While many pelagic predators primarily associate with epipelagic waters, some species routinely dive beyond the deep scattering layer. Actuation for exploiting these aphotic habitats remains largely unknown. Recent telemetry data from oceanic whitetip sharks (Carcharhinus longimanus) in the Atlantic show a strong association with warm waters (>20°C) less than 200 m. Yet, individuals regularly exhibit excursions into the meso‐ and bathypelagic zone. In order to examine deep‐diving behavior in oceanic whitetip sharks, we physically recovered 16 pop‐up satellite archival tags and analyzed the high‐resolution depth and temperature data. Diving behavior was evaluated in the context of plausible functional behavior hypotheses including interactive behaviors, energy conservation, thermoregulation, navigation, and foraging. Mesopelagic excursions (n = 610) occurred throughout the entire migratory circuit in all individuals, with no indication of site specificity. Six depth‐versus‐time descent and ascent profiles were identified. Descent profile shapes showed little association with examined environmental variables. Contrastingly, ascent profile shapes were related to environmental factors and appear to represent unique behavioral responses to abiotic conditions present at the dive apex. However, environmental conditions may not be the sole factors influencing ascents, as ascent mode may be linked to intentional behaviors. While dive functionality remains unconfirmed, our study suggests that mesopelagic excursions relate to active foraging behavior or navigation. Dive timing, prey constituents, and dive shape support foraging as the most viable hypothesis for mesopelagic excursions, indicating that the oceanic whitetip shark may regularly survey extreme environments (deep depths, low temperatures) as a foraging strategy. At the apex of these deep‐water excursions, sharks exhibit a variable behavioral response, perhaps, indicating the presence or absence of prey.

Relations between morphology, buoyancy and energetics of requiem sharks

Sharks have a distinctive shape that remained practically unchanged through hundreds of millions of years of evolution. Nonetheless, there are variations of this shape that vary between and within species. We attempt to explain these variations by examining the partial derivatives of the cost of transport of a generic shark with respect to buoyancy, span and chord of its pectoral fins, length, girth and body temperature. Our analysis predicts an intricate relation between these parameters, suggesting that ectothermic species residing in cooler temperatures must either have longer pectoral fins and/or be more buoyant in order to maintain swimming performance. It also suggests that, in general, the buoyancy must increase with size, and therefore, there must be ontogenetic changes within a species, with individuals getting more buoyant as they grow. Pelagic species seem to have near optimally sized fins (which minimize the cost of transport), but the majority of reef sharks could have reduced the cost of transport by increasing the size of their fins. The fact that they do not implies negative selection, probably owing to decreased manoeuvrability in confined spaces (e.g. foraging on a reef).

Inferring animal social networks and leadership: applications for passive monitoring arrays

Analyses of animal social networks have frequently benefited from techniques derived from other disciplines. Recently, machine learning algorithms have been adopted to infer social associations from time-series data gathered using remote, telemetry systems situated at provisioning sites. We adapt and modify existing inference methods to reveal the underlying social structure of wide-ranging marine predators moving through spatial arrays of passive acoustic receivers. From six months of tracking data for grey reef sharks (Carcharhinus amblyrhynchos) at Palmyra atoll in the Pacific Ocean, we demonstrate that some individuals emerge as leaders within the population and that this behavioural coordination is predicted by both sex and the duration of co-occurrences between conspecifics. In doing so, we provide the first evidence of long-term, spatially extensive social processes in wild sharks. To achieve these results, we interrogate simulated and real tracking data with the explicit purpose of drawing attention to the key considerations in the use and interpretation of inference methods and their impact on resultant social structure. We provide a modified translation of the GMMEvents method for R, including new analyses quantifying the directionality and duration of social events with the aim of encouraging the careful use of these methods more widely in less tractable social animal systems but where passive telemetry is already widespread.

Mesophotic coral ecosystems are threatened and ecologically distinct from shallow water reefs

Deep coral reefs are different Coral reefs are under intense pressure from anthropogenically induced climate warming and habitat destruction. It has been suggested that coral reefs in deeper waters may provide a refuge less affected by human development and climate change. Rocha et al., however, show that shallow and deep reefs are biologically different. Furthermore, deep (or mesophotic) reefs are also suffering from human impacts. Thus, deep reefs do not represent a potential refuge for other reef ecosystems. Indeed, they too are threatened and need protection. Science, this issue p. 281 Deep water reefs will not provide a refuge for shallow reef ecosystems. The rapid degradation of coral reefs is one of the most serious biodiversity problems facing our generation. Mesophotic coral reefs (at depths of 30 to 150 meters) have been widely hypothesized to provide refuge from natural and anthropogenic impacts, a promise for the survival of shallow reefs. The potential role of mesophotic reefs as universal refuges is often highlighted in reef conservation research. This hypothesis rests on two assumptions: (i) that there is considerable overlap in species composition and connectivity between shallow and deep populations and (ii) that deep reefs are less susceptible to anthropogenic and natural impacts than their shallower counterparts. Here we present evidence contradicting these assumptions and argue that mesophotic reefs are distinct, impacted, and in as much need of protection as shallow coral reefs.

A global perspective on the trophic geography of sharks

Sharks are a diverse group of mobile predators that forage across varied spatial scales and have the potential to influence food web dynamics. The ecological consequences of recent declines in shark biomass may extend across broader geographic ranges if shark taxa display common behavioural traits. By tracking the original site of photosynthetic fixation of carbon atoms that were ultimately assimilated into muscle tissues of 5,394 sharks from 114 species, we identify globally consistent biogeographic traits in trophic interactions between sharks found in different habitats. We show that populations of shelf-dwelling sharks derive a substantial proportion of their carbon from regional pelagic sources, but contain individuals that forage within additional isotopically diverse local food webs, such as those supported by terrestrial plant sources, benthic production and macrophytes. In contrast, oceanic sharks seem to use carbon derived from between 30° and 50° of latitude. Global-scale compilations of stable isotope data combined with biogeochemical modelling generate hypotheses regarding animal behaviours that can be tested with other methodological approaches.Carbon isotopic analysis reveals global biogeographic traits in shark trophic interactions, and sheds light on the diverse foraging behaviour of sharks.

Growth and life history variability of the grey reef shark (Carcharhinus amblyrhynchos) across its range

For broadly distributed, often overexploited species such as elasmobranchs (sharks and rays), conservation management would benefit from understanding how life history traits change in response to local environmental and ecological factors. However, fishing obfuscates this objective by causing complex and often mixed effects on the life histories of target species. Disentangling the many drivers of life history variability requires knowledge of elasmobranch populations in the absence of fishing, which is rarely available. Here, we describe the growth, maximum size, sex ratios, size at maturity, and offer a direct estimate of survival of an unfished population of grey reef sharks (Carcharhinus amblyrhynchos) using data from an eight year tag-recapture study. We then synthesized published information on the life history of C. amblyrhynchos from across its geographic range, and for the first time, we attempted to disentangle the contribution of fishing from geographic variation in an elasmobranch species. For Palmyra’s unfished C. amblyrhynchos population, the von Bertalanffy growth function (VBGF) growth coefficient k was 0.05 and asymptotic length L∞ was 163.3 cm total length (TL). Maximum size was 175.5 cm TL from a female shark, length at maturity was estimated at 116.7–123.2 cm TL for male sharks, maximum lifespan estimated from VBGF parameters was 18.1 years for both sexes combined, and annual survival was 0.74 year-1. Consistent with findings from studies on other elasmobranch species, we found significant intraspecific variability in reported life history traits of C. amblyrhynchos. However, contrary to what others have reported, we did not find consistent patterns in life history variability as a function of biogeography or fishing. Ultimately, the substantial, but not yet predictable variability in life history traits observed for C. amblyrhynchos across its geographic range suggests that regional management may be necessary to set sustainable harvest targets and to recover this and other shark species globally.

Combining abundance and performance data reveals how temperature regulates coastal occurrences and activity of a roaming apex predator

The redistribution of species has emerged as one of the most pervasive impacts of anthropogenic climate warming, and presents many societal challenges. Understanding how temperature regulates species distributions is particularly important for mobile marine fauna such as sharks given their seemingly rapid responses to warming, and the socio-political implications of human encounters with some dangerous species. The predictability of species distributions can potentially be improved by accounting for temperatures influence on performance, an elusive relationship for most large animals. We combined multi-decadal catch data and bio-logging to show that coastal abundance and swimming performance of tiger sharks Galeocerdo cuvier are both highest at ~22°C, suggesting thermal constraints on performance may regulate this species distribution. Tiger sharks are responsible for a large proportion of shark bites on humans, and a focus of controversial control measures in several countries. The combination of distribution and performance data moves towards a mechanistic understanding of tiger sharks thermal niche, and delivers a simple yet powerful indicator for predicting the location and timing of their occurrences throughout coastlines. For example, tiger sharks are mostly caught at Australias popular New South Wales beaches (i.e. near Sydney) in the warmest months, but our data suggest similar abundances will occur in winter and summer if annual sea surface temperatures increase by a further 1-2°C.

Mobile marine predators: an understudied source of nutrients to coral reefs in an unfished atoll

Animal movements can facilitate important ecological processes, and wide-ranging marine predators, such as sharks, potentially contribute significantly towards nutrient transfer between habitats. We applied network theory to 4 years of acoustic telemetry data for grey reef sharks (Carcharhinus amblyrhynchos) at Palmyra, an unfished atoll, to assess their potential role in nutrient dynamics throughout this remote ecosystem. We evaluated the dynamics of habitat connectivity and used network metrics to quantify shark-mediated nutrient distribution. Predator movements were consistent within year, but differed between years and by sex. Females used higher numbers of routes throughout the system, distributing nutrients over a larger proportion of the atoll. Extrapolations of tagged sharks to the population level suggest that prey consumption and subsequent egestion leads to the heterogeneous deposition of 94.5 kg d−1 of nitrogen around the atoll, with approximately 86% of this probably derived from pelagic resources. These results suggest that sharks may contribute substantially to nutrient transfer from offshore waters to near-shore reefs, subsidies that are important for coral reef health.

Optimal swimming strategies and behavioral plasticity of oceanic whitetip sharks

Animal behavior should optimize the difference between the energy theyxa0gain from prey and the energy theyxa0spend searching for prey. This is all the more critical for predators occupying the pelagic environment, as prey is sparse and patchily distributed. We theoretically derive two canonical swimming strategiesxa0for pelagic predators, that maximize theirxa0energy surplusxa0while foraging. They predict that while searching, a pelagicxa0predator should maintain small dive angles, swim at speeds near those that minimize the cost of transport, and maintain constant speed throughout the dive. Using biologging sensors, we show that oceanic whitetip shark (Carcharhinus longimanus) behavior matches these predictions. We estimate that daily energy requirements of an adult shark can be met by consuming approximately 1–1.5u2009kg of prey (1.5% body mass) per day; shark-borne video footage shows a shark encountering potential prey numbers exceeding that amount. Oceanic whitetip sharks showed incredible plasticity in their behavioral strategies, ranging from short low-energy bursts on descents, to high-speed vertical surface breaches from considerable depth. Oceanic whitetips live a life of energy speculation with minimization, very different to those of tunas and billfish.