3D visualization processes for recreating and studying organismal form.

The study of biological form is a vital goal of evolutionary biology and functional morphology. We review an emerging set of methods that allow scientists to create and study accurate 3D models of living organisms and animate those models for biomechanical and fluid dynamic analyses. The methods for creating such models include 3D photogrammetry, laser and CT scanning, and 3D software. New multi-camera devices can be used to create accurate 3D models of living animals in the wild and captivity. New websites and virtual reality/augmented reality devices now enable the visualization and sharing of these data. We provide examples of these approaches for animals ranging from large whales to lizards and show applications for several areas: Natural history collections; body condition/scaling, bioinspired robotics, computational fluids dynamics (CFD), machine learning, and education. We provide two datasets to demonstrate the efficacy of CFD and machine learning approaches and conclude with a prospectus.

Multivariate analysis of biologging data reveals the environmental determinants of diving behaviour in a marine reptile.

Diving behaviour of 'surfacers' such as sea snakes, cetaceans and turtles is complex and multi-dimensional, thus may be better captured by multi-sensor biologging data. However, analysing these large multi-faceted datasets remains challenging, though a high priority. We used high-resolution multi-sensor biologging data to provide the first detailed description of the environmental influences on flatback turtle (Natator depressus) diving behaviour, during its foraging life-history stage. We developed an analytical method to investigate seasonal, diel and tidal effects on diving behaviour for 24 adult flatback turtles tagged with biologgers. We extracted 16 dive variables associated with three-dimensional and kinematic characteristics for 4128 dives. K-means and hierarchical cluster analyses failed to identify distinct dive types. Instead, principal component analysis objectively condensed the dive variables, removing collinearity and highlighting the main features of diving behaviour. Generalized additive mixed models of the main principal components identified significant seasonal, diel and tidal effects on flatback turtle diving behaviour. Flatback turtles altered their diving behaviour in response to extreme tidal and water temperature ranges, displaying thermoregulation and predator avoidance strategies while likely optimizing foraging in this challenging environment. This study demonstrates an alternative statistical technique for objectively interpreting diving behaviour from multivariate collinear data derived from biologgers.

Metabolic Rates and Thermal Thresholds of Embryonic Flatback Turtles (Natator depressus) from the North West Shelf of Australia.

AbstractNest microclimates influence embryonic development and survival in many lineages, including reptiles with temperature-dependent sex determination. These microclimates are dependent on physical drivers and biological processes, such as embryonic metabolism, that generate heat. The flatback turtle (Natator depressus) has among the largest hatchlings of the seven extant sea turtle species, making it an excellent candidate for quantifying the contribution of embryonic metabolism to the nest microclimate. Consequently, we measured embryonic metabolic rates, development rates, and the relationship between temperature and sex determination for a N. depressus population nesting at Cemetery Beach in Western Australia, a mainland beach characterized by high sand temperatures. Total oxygen consumed at 29.5°C during an average 52-d incubation period was 2,622 mL, total carbon dioxide produced was 1,886 mL, and estimated embryonic heat production reached 38 mW at 90% of development. Adjustment of metabolic rates to 32°C and 34°C increased peak heat production by 18% and 27%, respectively. The pivotal temperature (TPIV) producing an equal sex ratio was 30.3°C, mixed sexes were produced between 29.3°C and 31.2°C, and only females were produced above 31.2°C. The TPIV was similar (within 0.2°C) to that of an island rookery within the same genetic stock (North West Shelf), but the peak development rate (2.5% d-1) was estimated to be achieved at a temperature ~2.5°C higher (34.7°C) than the island rookery. Our results add to a growing consensus that thermal thresholds vary among sea turtle populations, even within the same genetic stock. Furthermore, we show that metabolic heat will have an appreciable impact on the nest microclimate, which has implications for embryonic survival and fitness under a future climate with warmer sand temperatures.

Regional movements of satellite-tagged whale sharks Rhincodon typus in the Gulf of Aden.

To gain insight into whale shark (Rhincodon typus) movement patterns in the Western Indian Ocean, we deployed eight pop-up satellite tags at an aggregation site in the Arta Bay region of the Gulf of Tadjoura, Djibouti in the winter months of 2012, 2016, and 2017. Tags revealed movements ranging from local-scale around the Djibouti aggregation site, regional movements along the coastline of Somaliland, movements north into the Red Sea, and a large-scale (>1,000 km) movement to the east coast of Somalia, outside of the Gulf of Aden. Vertical movement data revealed high occupation of the top ten meters of the water column, diel vertical movement patterns, and deep diving behavior. Long-distance movements recorded both here and in previous studies suggest that connectivity between the whale sharks tagged at the Djibouti aggregation and other documented aggregations in the region are likely within annual timeframes. In addition, wide-ranging movements through multiple nations, as well as the high use of surface waters recorded, likely exposes whale sharks in this region to several anthropogenic threats, including targeted and bycatch fisheries and ship-strikes. Area-based management approaches focusing on seasonal hotspots offer a way forward in the conservation of whale sharks in the Western Indian Ocean.

Predicting seasonal movements and distribution of the sperm whale using machine learning algorithms.

Implementation of effective conservation planning relies on a robust understanding of the spatiotemporal distribution of the target species. In the marine realm, this is even more challenging for species rarely seen at the sea surface due to their extreme diving behavior like the sperm whales. Our study aims at (a) investigating the seasonal movements, (b) predicting the potential distribution, and (c) assessing the diel vertical behavior of this species in the Mascarene Archipelago in the south-west Indian Ocean. Using 21 satellite tracks of sperm whales and eight environmental predictors, 14 supervised machine learning algorithms were tested and compared to predict the whales' potential distribution during the wet and dry season, separately. Fourteen of the whales remained in close proximity to Mauritius, while a migratory pattern was evidenced with a synchronized departure for eight females that headed towards Rodrigues Island. The best performing algorithm was the random forest, showing a strong affinity of the whales for sea surface height during the wet season and for bottom temperature during the dry season. A more dispersed distribution was predicted during the wet season, whereas a more restricted distribution to Mauritius and Reunion waters was found during the dry season, probably related to the breeding period. A diel pattern was observed in the diving behavior, likely following the vertical migration of squids. The results of our study fill a knowledge gap regarding seasonal movements and habitat affinities of this vulnerable species, for which a regional IUCN assessment is still missing in the Indian Ocean. Our findings also confirm the great potential of machine learning algorithms in conservation planning and provide highly reproductible tools to support dynamic ocean management.

Characterizing habitat suitability for a central-place forager in a dynamic marine environment.

Characterizing habitat suitability for a marine predator requires an understanding of the environmental heterogeneity and variability over the range in which a population moves during a particular life cycle. Female California sea lions (Zalophus californianus) are central-place foragers and are particularly constrained while provisioning their young. During this time, habitat selection is a function of prey availability and proximity to the rookery, which has important implications for reproductive and population success. We explore how lactating females may select habitat and respond to environmental variability over broad spatial and temporal scales within the California Current System. We combine near-real-time remotely sensed satellite oceanography, animal tracking data (n = 72) from November to February over multiple years (2003-2009) and Generalized Additive Mixed Models (GAMMs) to determine the probability of sea lion occurrence based on environmental covariates. Results indicate that sea lion presence is associated with cool (<14°C), productive waters, shallow depths, increased eddy activity, and positive sea-level anomalies. Predictive habitat maps generated from these biophysical associations suggest winter foraging areas are spatially consistent in the nearshore and offshore environments, except during the 2004-2005 winter, which coincided with an El Niño event. Here, we show how a species distribution model can provide broadscale information on the distribution of female California sea lions during an important life history stage and its implications for population dynamics and spatial management.

Resource partitioning facilitates coexistence in sympatric cetaceans in the California Current.

Resource partitioning is an important process driving habitat use and foraging strategies in sympatric species that potentially compete. Differences in foraging behavior are hypothesized to contribute to species coexistence by facilitating resource partitioning, but little is known on the multiple mechanisms for partitioning that may occur simultaneously. Studies are further limited in the marine environment, where the spatial and temporal distribution of resources is highly dynamic and subsequently difficult to quantify. We investigated potential pathways by which foraging behavior may facilitate resource partitioning in two of the largest co-occurring and closely related species on Earth, blue (Balaenoptera musculus) and humpback (Megaptera novaeangliae) whales. We integrated multiple long-term datasets (line-transect surveys, whale-watching records, net sampling, stable isotope analysis, and remote-sensing of oceanographic parameters) to compare the diet, phenology, and distribution of the two species during their foraging periods in the highly productive waters of Monterey Bay, California, USA within the California Current Ecosystem. Our long-term study reveals that blue and humpback whales likely facilitate sympatry by partitioning their foraging along three axes: trophic, temporal, and spatial. Blue whales were specialists foraging on krill, predictably targeting a seasonal peak in krill abundance, were present in the bay for an average of 4.7 months, and were spatially restricted at the continental shelf break. In contrast, humpback whales were generalists apparently feeding on a mixed diet of krill and fishes depending on relative abundances, were present in the bay for a more extended period (average of 6.6 months), and had a broader spatial distribution at the shelf break and inshore. Ultimately, competition for common resources can lead to behavioral, morphological, and physiological character displacement between sympatric species. Understanding the mechanisms for species coexistence is both fundamental to maintaining biodiverse ecosystems, and provides insight into the evolutionary drivers of morphological differences in closely related species.

Key Questions in Marine Megafauna Movement Ecology.

It is a golden age for animal movement studies and so an opportune time to assess priorities for future work. We assembled 40 experts to identify key questions in this field, focussing on marine megafauna, which include a broad range of birds, mammals, reptiles, and fish. Research on these taxa has both underpinned many of the recent technical developments and led to fundamental discoveries in the field. We show that the questions have broad applicability to other taxa, including terrestrial animals, flying insects, and swimming invertebrates, and, as such, this exercise provides a useful roadmap for targeted deployments and data syntheses that should advance the field of movement ecology.

Current-oriented swimming by jellyfish and its role in bloom maintenance.

Cross-flows (winds or currents) affect animal movements [1-3]. Animals can temporarily be carried off course or permanently carried away from their preferred habitat by drift depending on their own traveling speed in relation to that of the flow [1]. Animals able to only weakly fly or swim will be the most impacted (e.g., [4]). To circumvent this problem, animals must be able to detect the effects of flow on their movements and respond to it [1, 2]. Here, we show that a weakly swimming organism, the jellyfish Rhizostoma octopus, can orientate its movements with respect to currents and that this behavior is key to the maintenance of blooms and essential to reduce the probability of stranding. We combined in situ observations with first-time deployment of accelerometers on free-ranging jellyfish and simulated the behavior observed in wild jellyfish within a high-resolution hydrodynamic model. Our results show that jellyfish can actively swim countercurrent in response to current drift, leading to significant life-history benefits, i.e., increased chance of survival and facilitated bloom formation. Current-oriented swimming may be achieved by jellyfish either directly detecting current shear across their body surface [5] or indirectly assessing drift direction using other cues (e.g., magnetic, infrasound). Our coupled behavioral-hydrodynamic model provides new evidence that current-oriented swimming contributes to jellyfish being able to form aggregations of hundreds to millions of individuals for up to several months, which may have substantial ecosystem and socioeconomic consequences [6, 7]. It also contributes to improve predictions of jellyfish blooms' magnitude and movements in coastal waters.

Route optimisation and solving Zermelo's navigation problem during long distance migration in cross flows.

The optimum path to follow when subjected to cross flows was first considered over 80 years ago by the German mathematician Ernst Zermelo, in the context of a boat being displaced by ocean currents, and has become known as the 'Zermelo navigation problem'. However, the ability of migrating animals to solve this problem has received limited consideration, even though wind and ocean currents cause the lateral displacement of flyers and swimmers, respectively, particularly during long-distance journeys of 1000s of kilometres. Here, we examine this problem by combining long-distance, open-ocean marine turtle movements (obtained via long-term GPS tracking of sea turtles moving 1000s of km), with a high resolution basin-wide physical ocean model to estimate ocean currents. We provide a robust mathematical framework to demonstrate that, while turtles eventually arrive at their target site, they do not follow the optimum (Zermelo's) route. Even though adult marine turtles regularly complete incredible long-distance migrations, these vertebrates primarily rely on course corrections when entering neritic waters during the final stages of migration. Our work introduces a new perspective in the analysis of wildlife tracking datasets, with different animal groups potentially exhibiting different levels of complexity in goal attainment during migration.

Leatherback turtles are capital breeders: morphometric and physiological evidence from longitudinal monitoring.

Organisms compensate for reproduction costs through two major strategies: capital breeders store body reserves before reproduction and do not feed during the breeding season, whereas income breeders adjust their food intake depending on concurrent reproductive needs. Sea turtles are commonly considered capital breeders. Yet recent biometric and behavioral studies have suggested that sea turtles may in fact feed during reproduction. We tested this hypothesis in the leatherback turtle Dermochelys coriacea, nesting in French Guiana. Our study is based on the innovative use of longitudinal monitoring for morphological (body size, body mass, and body condition) and physiological (plasma glucose, triacylglycerides, urea, calcium, and hematocrit) measurements in 35 females throughout the 2006 nesting season. During their 71-d nesting period, leatherbacks lost a mean (±SE) of [Formula: see text] kg (i.e., ∼11% of their initial body mass of [Formula: see text] kg). Simultaneously, a significant decrease in plasma concentrations of glucose, triacylglycerides, and urea was observed throughout the nesting season, following typical patterns reported in other long-fasting animals that rely on lipid body stores. At the end of the nesting season, the interindividual variability in plasma concentrations was very low, which may characterize some minimum thresholds associated with the end of reproduction. We also identified a minimum necessary threshold for female body condition at the onset of reproduction; the body condition of any females beginning the nesting period below this threshold decreased dramatically. This study makes a compelling case that, in French Guiana, gravid leatherback females are anorexic during the nesting season (i.e., leatherback turtles are capital breeders). We further highlight the mechanisms that prevent this multiparous reptile from jeopardizing its own body condition while not feeding during reproduction.

The significance of the north water polynya to arctic top predators.

The North Water polynya (~76°N to 79°N and 70°W to 80°W) is known to be an important habitat for several species of marine mammals and sea birds. For millennia, it has provided the basis for subsistence hunting and human presence in the northernmost part of Baffin Bay. The abundance of air-breathing top predators also represents a potential source of nutrient cycling that maintains primary production. In this study, aerial surveys conducted in 2009 and 2010 were used for the first time to map the distribution and estimate the abundance of top predators during spring in the North Water. Belugas (Delphinapterus leucas) were not detected north of 77°20'N but were found along the coast of West Greenland and offshore in the middle of the North Water with an abundance estimated at 2245 (95 % CI 1811-2783). Narwhals (Monodon monoceros) were widely distributed on the eastern side of the North Water with an estimate of abundance of 7726 (3761-15 870). Walruses (Odobenus rosmarus) were found across the North Water over both shallow and deep (>500 m) water with an estimated abundance of 1499 (1077-2087). Bearded (Erignathus barbatus) and ringed seals (Phoca hispida) used the large floes of ice in the southeastern part of the North Water for hauling out. Most polar bears (Ursus maritimus) were detected in the southern part of the polynya. The abundances of bearded and ringed seals were 6016 (3322-10 893) and 9529 (5460-16 632), respectively, and that of polar bears was 60 (12-292). Three sea bird species were distributed along the Greenland coast (eiders, Somateria spp.), in leads and cracks close to the Greenland coast (little auks, Alle alle) or widely in open water (thick-billed guillemots, Uria lomvia).

Movement patterns for a critically endangered species, the leatherback turtle (Dermochelys coriacea), linked to foraging success and population status.

Foraging success for pelagic vertebrates may be revealed by horizontal and vertical movement patterns. We show markedly different patterns for leatherback turtles in the North Atlantic versus Eastern Pacific, which feed on gelatinous zooplankton that are only occasionally found in high densities. In the Atlantic, travel speed was characterized by two modes, indicative of high foraging success at low speeds (<15 km d(-1)) and transit at high speeds (20-45 km d(-1)). Only a single mode was evident in the Pacific, which occurred at speeds of 21 km d(-1) indicative of transit. The mean dive depth was more variable in relation to latitude but closer to the mean annual depth of the thermocline and nutricline for North Atlantic than Eastern Pacific turtles. The most parsimonious explanation for these findings is that Eastern Pacific turtles rarely achieve high foraging success. This is the first support for foraging behaviour differences between populations of this critically endangered species and suggests that longer periods searching for prey may be hindering population recovery in the Pacific while aiding population maintenance in the Atlantic.

Reproductive synchrony in a recovering bottlenecked sea turtle population.

1. The assessment of species extinction risk has been well established for some time now. Assessing the potential for recovery in endangered species is however much more challenging, because complementary approaches are required to detect reliable signals of positive trends. 2. This study combines genetics, demography and behavioural data at three different time-scales to assess historical and recent population changes and evidence of reproductive synchrony in a small population of olive ridley sea turtle Lepidochelys olivacea. Lepidochelys is considered as the most extraordinary example of reproductive synchrony in reptiles, yet to date, it has only been reported in large populations. 3. Using Bayesian coalescent-based models on microsatellite nuclear DNA variability, we demonstrate that effective population size in olive ridleys nesting in French Guiana has dramatically declined by 99% over the last 20 centuries. This low current population size is further illustrated by the absence of genetic mitochondrial DNA diversity in the present nesting population. Yet, monitoring of nesting sites in French Guiana suggests a possible recovery of the population over the last decade. 4. Satellite telemetry shows that over the first 14 days of their 28-days inter-nesting interval, i.e. when eggs maturation is likely to occur, gravid females disperse over the continental shelf. They then gather together with a striking spatiotemporal consistency close to the nesting site, where they later emerge for their second nesting event. 5. Our results therefore suggest that reproductive synchrony also occurs in small populations. Olive ridleys may ensure this synchrony by adjusting the duration of the second half of their inter-nesting interval prior to landing, possibly through social mediation. 6. Such reproductive synchrony may be related to the maintenance of some species-specific strategy despite former collapse and may contribute to the present population recovery. The gregarious behaviour of reproductive individuals close to shore where human-induced perturbations occur is however a cause for conservation concern for this still poorly known species.

Does prey size matter? Novel observations of feeding in the leatherback turtle (Dermochelys coriacea) allow a test of predator-prey size relationships.

Optimal foraging models predict that large predators should concentrate on large prey in order to maximize their net gain of energy intake. Here, we show that the largest species of sea turtle, Dermochelys coriacea, does not strictly adhere to this general pattern. Field observations combined with a theoretical model suggest that a 300 kg leatherback turtle would meet its energetic requirements by feeding for 3-4 h a day on 4 g jellyfish, but only if prey were aggregated in high-density patches. Therefore, prey abundance rather than prey size may, in some cases, be the overriding parameter for foraging leatherbacks. This is a classic example where the presence of small prey in the diet of a large marine predator may reflect profitable foraging decisions if the relatively low energy intake per small individual prey is offset by high encounter rates and minimal capture and handling costs. This study provides, to our knowledge, the first quantitative estimates of intake rate for this species.

High activity and Levy searches: jellyfish can search the water column like fish.

Over-fishing may lead to a decrease in fish abundance and a proliferation of jellyfish. Active movements and prey search might be thought to provide a competitive advantage for fish, but here we use data-loggers to show that the frequently occurring coastal jellyfish (Rhizostoma octopus) does not simply passively drift to encounter prey. Jellyfish (327 days of data from 25 jellyfish with depth collected every 1 min) showed very dynamic vertical movements, with their integrated vertical movement averaging 619.2 m d(-1), more than 60 times the water depth where they were tagged. The majority of movement patterns were best approximated by exponential models describing normal random walks. However, jellyfish also showed switching behaviour from exponential patterns to patterns best fitted by a truncated Lévy distribution with exponents (mean µ=1.96, range 1.2-2.9) close to the theoretical optimum for searching for sparse prey (µopt≈2.0). Complex movements in these 'simple' animals may help jellyfish to compete effectively with fish for plankton prey, which may enhance their ability to increase in dominance in perturbed ocean systems.

Animal orientation strategies for movement in flows.

For organisms that fly or swim, movement results from the combined effects of the moving medium - air or water - and the organism's own locomotion. For larger organisms, propulsion contributes significantly to progress but the flow usually still provides significant opposition or assistance, or produces lateral displacement ('drift'). Animals show a range of responses to flows, depending on the direction of the flow relative to their preferred direction, the speed of the flow relative to their own self-propelled speed, the incidence of flows in different directions and the proportion of the journey remaining. We here present a classification of responses based on the direction of the resulting movement relative to flow and preferred direction, which is applicable to a range of taxa and environments. The responses adopted in particular circumstances are related to the organisms' locomotory and sensory capacities and the environmental cues available. Advances in biologging technologies and particle tracking models are now providing a wealth of data, which often demonstrate a striking level of convergence in the strategies that very different animals living in very different environments employ when moving in a flow.

Atlantic leatherback migratory paths and temporary residence areas.

BACKGROUND: Sea turtles are long-distance migrants with considerable behavioural plasticity in terms of migratory patterns, habitat use and foraging sites within and among populations. However, for the most widely migrating turtle, the leatherback turtle Dermochelys coriacea, studies combining data from individuals of different populations are uncommon. Such studies are however critical to better understand intra- and inter-population variability and take it into account in the implementation of conservation strategies of this critically endangered species. Here, we investigated the movements and diving behaviour of 16 Atlantic leatherback turtles from three different nesting sites and one foraging site during their post-breeding migration to assess the potential determinants of intra- and inter-population variability in migratory patterns. METHODOLOGY/PRINCIPAL FINDINGS: Using satellite-derived behavioural and oceanographic data, we show that turtles used Temporary Residence Areas (TRAs) distributed all around the Atlantic Ocean: 9 in the neritic domain and 13 in the oceanic domain. These TRAs did not share a common oceanographic determinant but on the contrary were associated with mesoscale surface oceanographic features of different types (i.e., altimetric features and/or surface chlorophyll a concentration). Conversely, turtles exhibited relatively similar horizontal and vertical behaviours when in TRAs (i.e., slow swimming velocity/sinuous path/shallow dives) suggesting foraging activity in these productive regions. Migratory paths and TRAs distribution showed interesting similarities with the trajectories of passive satellite-tracked drifters, suggesting that the general dispersion pattern of adults from the nesting sites may reflect the extent of passive dispersion initially experienced by hatchlings. CONCLUSIONS/SIGNIFICANCE: Intra- and inter-population behavioural variability may therefore be linked with initial hatchling drift scenarios and be highly influenced by environmental conditions. This high degree of behavioural plasticity in Atlantic leatherback turtles makes species-targeted conservation strategies challenging and stresses the need for a larger dataset (>100 individuals) for providing general recommendations in terms of conservation.

Behaviour and buoyancy regulation in the deepest-diving reptile: the leatherback turtle.

In the face of the physical and physiological challenges of performing breath-hold deep dives, marine vertebrates have evolved different strategies. Although behavioural strategies in marine mammals and seabirds have been investigated in detail, little is known about the deepest-diving reptile - the leatherback turtle (Dermochelys coriacea). Here, we deployed tri-axial accelerometers on female leatherbacks nesting on St Croix, US Virgin Islands, to explore their diving strategy. Our results show a consistent behavioural pattern within dives among individuals, with an initial period of active swimming at relatively steep descent angles (∼-40 deg), with a stroke frequency of 0.32 Hz, followed by a gliding phase. The depth at which the gliding phase began increased with the maximum depth of the dives. In addition, descent body angles and vertical velocities were higher during deeper dives. Leatherbacks might thus regulate their inspired air-volume according to the intended dive depth, similar to hard-shelled turtles and penguins. During the ascent, turtles actively swam with a stroke frequency of 0.30 Hz but with a low vertical velocity (∼0.40 ms(-1)) and a low pitch angle (∼+26 deg). Turtles might avoid succumbing to decompression sickness ('the bends') by ascending slowly to the surface. In addition, we suggest that the low body temperature of this marine ectotherm compared with that of endotherms might help reduce the risk of bubble formation by increasing the solubility of nitrogen in the blood. This physiological advantage, coupled with several behavioural and physical adaptations, might explain the particular ecological niche the leatherback turtle occupies among marine reptiles.