Scaling of Activity Space in Marine Organisms across Latitudinal Gradients.

AbstractUnifying models have shown that the amount of space used by animals (e.g., activity space, home range) scales allometrically with body mass for terrestrial taxa; however, such relationships are far less clear for marine species. We compiled movement data from 1,596 individuals across 79 taxa collected using a continental passive acoustic telemetry network of acoustic receivers to assess allometric scaling of activity space. We found that ectothermic marine taxa do exhibit allometric scaling for activity space, with an overall scaling exponent of 0.64. However, body mass alone explained only 35% of the variation, with the remaining variation best explained by trophic position for teleosts and latitude for sharks, rays, and marine reptiles. Taxon-specific allometric relationships highlighted weaker scaling exponents among teleost fish species (0.07) than sharks (0.96), rays (0.55), and marine reptiles (0.57). The allometric scaling relationship and scaling exponents for the marine taxonomic groups examined were lower than those reported from studies that had collated both marine and terrestrial species data derived using various tracking methods. We propose that these disparities arise because previous work integrated summarized data across many studies that used differing methods for collecting and quantifying activity space, introducing considerable uncertainty into slope estimates. Our findings highlight the benefit of using large-scale, coordinated animal biotelemetry networks to address cross-taxa evolutionary and ecological questions.

Elephant seal foraging success is enhanced in Antarctic coastal polynyas.

Antarctic polynyas are persistent open water areas which enable early and large seasonal phytoplankton blooms. This high primary productivity, boosted by iron supply from coastal glaciers, attracts organisms from all trophic levels to form a rich and diverse community. How the ecological benefit of polynya productivity is translated to the highest trophic levels remains poorly resolved. We studied 119 southern elephant seals feeding over the Antarctic shelf and demonstrated that: (i) 96% of seals foraging here used polynyas, with individuals spending on average 62% of their time there; (ii) the seals exhibited more area-restricted search behaviour when in polynyas; and (iii) these seals gained more energy (indicated by increased buoyancy from greater fat stores) when inside polynyas. This higher-quality foraging existed even when ice was not present in the study area, indicating that these are important and predictable foraging grounds year-round. Despite these energetic advantages from using polynyas, not all the seals used them extensively. Factors other than food supply may influence an individual's choice in their use of feeding grounds, such as exposure to predation or the probability of being able to return to distant sub-Antarctic breeding sites.

Mother-pup recognition mechanisms in Australia sea lion (Neophoca cinerea) using uni- and multi-modal approaches.

Communication is the process by which one emitter conveys information to one or several receivers to induce a response (behavioral or physiological) by the receiver. Communication plays a major role in various biological functions and may involve signals and cues from different sensory modalities. Traditionally, investigations of animal communication focused on a single sensory modality, yet communication is often multimodal. As these different processes may be quite complex and therefore difficult to disentangle, one approach is to first study each sensorial modality separately. With this refined understanding of individual senses, revealing how they interact becomes possible as the characteristics and properties of each modality can be accounted for, making a multimodal approach feasible. Using this framework, researchers undertook systematic, experimental investigations on mother-pup recognition processes in a colonial pinniped species, the Australian sea lion Neophoca cinerea. The research first assessed the abilities of mothers and pups to identify each other by their voice using playback experiments. Second, they assessed whether visual cues are used by both mothers and pups to distinguish them from conspecifics, and/or whether females discriminate the odor of their filial pup from those from non-filial pups. Finally, to understand if the information transmitted by different sensory modalities is analyzed synergistically or if there is a hierarchy among the sensory modalities, experiments were performed involving different sensory cues simultaneously. These findings are discussed with regards to the active space of each sensory cue, and of the potential enhancements that may arise by assessing information from different modalities.

Lipid extraction has tissue-dependent effects on isotopic values (δ34 S, δ13 C, and δ15 N) from different marine predators.

RATIONALE: The use of sulfur isotopes to study trophic ecology in marine ecosystems has increased in the past decade. Unlike other commonly used isotopes (e.g., carbon), sulfur can better discriminate benthic and pelagic productivity. However, how lipid extraction affects sulfur isotopic values has not been assessed, despite its frequent use to remove lipid effects on δ13 C values. METHODS: We used white muscle and liver samples from two species of sharks and skin samples from two species of pinnipeds (sea lion and fur seal) to assess the effects of lipid extraction on stable isotope values for δ34 S, δ13 C, and δ15 N. Isotopic values were determined using a continuous flow-isotope ratio mass spectrometer coupled to an elemental analyzer. RESULTS: Lipid extraction significantly decreased δ34 S values in shark tissues, more so for liver than muscle (-4.6 ± 0.9‰ vs -0.8 ± 0.3‰, average change), with nearly no change in their standard deviations. Lipid extraction did not affect δ34 S values from pinniped skin samples (0.2 ± 0.8‰, average change). After lipid extraction, consistent increases in δ13 C values (0.2‰-7.3‰) were detected as expected, especially in tissue with high lipid content (C:N >4). After lipid extraction, significant increases in δ15 N values (0.5‰-1.4‰) were found in shark muscle and liver tissues. For pinniped skin samples, δ15 N values were not significantly lower after lipid extraction (-0.4‰ to -0.1‰). CONCLUSIONS: Lipid extraction did not have a strong impact on δ34 S values of shark muscle and pinniped skin (≤1‰). However, our results suggest it is essential to consider the effects of lipid extraction when interpreting results from δ34 S values of shark liver tissue, as they significantly depleted values relative to bulk tissue (~5‰). This may reflect selective removal of sulfolipids and glutathione present in higher concentrations in the liver than in muscle and skin and requires further investigation.

Pelagic and benthic ecosystems drive differences in population and individual specializations in marine predators.

Individual specialization, which describes whether populations are comprised of dietary generalists or specialists, has profound ecological and evolutionary implications. However, few studies have quantified individual specialization within and between sympatric species that are functionally similar but have different foraging modes. We assessed the relationship between individual specialization, isotopic niche metrics and foraging behaviour of two marine predators with contrasting foraging modes: pelagic foraging female South American fur seals (Arctocephalus australis) and benthic foraging female southern sea lions (Otaria byronia). Stable isotope analysis of carbon and nitrogen was conducted along the length of adult female vibrissae to determine isotopic niche metrics and the degree of individual specialization. Vibrissae integrated time ranged between 1.1 and 5.5 years, depending on vibrissae length. We found limited overlap in dietary niche-space. Broader population niche sizes were associated with higher degrees of individual specialization, while narrower population niches with lower degrees of individual specialization. The degree of individual specialization was influenced by pelagic and benthic foraging modes. Specifically, South American fur seals, foraging in dynamic pelagic environments with abundant but similar prey, comprised specialist populations composed of generalist individuals. In contrast, benthic southern sea lions foraging in habitats with diverse but less abundant prey had more generalist populations composed of highly specialized individuals. We hypothesize that differences in specialization within and between populations were related to prey availability and habitat differences. Our study supports growing body of literature highlighting that individual specialization is a critical factor in shaping the ecological niche of higher marine predators.

Chemical Profiles of Integumentary and Glandular Substrates in Australian Sea Lion Pups (Neophoca cinerea).

Recognition of individuals or classes of individuals plays an important role in the communication systems of many mammals. The ability of otariid (i.e., fur seal and sea lion) females to locate and identify their offspring in colonies after returning from regular foraging trips is essential to successful pup rearing. It has been shown that olfaction is used to confirm the identity of the pup by the mother when they reunite, yet the processes by which this chemical recognition occurs remain unclear. Using gas chromatography-mass spectrometry, we examined chemical profiles of integumentary and glandular secretions/excretions from pre- and post-molt Australian sea lion pups (Neophoca cinerea) and compared fur and swab samples to assess data collection methods. Multivariate statistics were applied to assess differences in chemical composition between body regions and sexes. We found differences among secretions from various body regions, driven by the distinctiveness of the oral odor mixture. The fine-scale trends in pre- and post-molt pups seem to differ due to changes in the behavior of pups and consequent decrease in the transfer of compounds among adjacent body regions in older pups. Volatile compounds from exocrine substrates were not distinct for different sexes. We also show that swab samples provide better data for exploring social olfaction than fur samples for this species. Obtaining fundamental chemical information, in this case chemical profiles of animals, and discerning differences in chemical composition is an important step toward fully exploring the intricacies of mother-offspring olfactory recognition and its underlying processes.

Geographic vocal variation and perceptual discrimination abilities in male Australian sea lions.

Vocal characteristics can vary among and within populations. In species with geographic variation in the structure of vocalizations, individuals may have the ability to discriminate between calls from local and non-local individuals. The ability to distinguish differences in acoustic signals is likely to have a significant influence on the outcome of social interactions between individuals, including potentially mate selection and breeding success. Pinnipeds (seals, fur seals, sea lions and walruses) are highly vocal yet the Australian sea lion (Neophoca cinerea) is the only eared seal known to show geographic vocal variation in male barks. Barks are produced in many social interactions and encode sufficient information for both individual and colony identity to be discriminable. Yet until now, whether males could themselves discriminate these bark differences was unclear. We performed playback experiments in four breeding colonies to investigate whether males can discriminate local from non-local barks. Overall, males responded more strongly to barks from their own colony compared to barks from other colonies regardless of whether those other colonies were close or distant. Competition for females is high in Australian sea lions, but mating periods are asynchronous across colonies. The ability to correctly assess whether a male is from the same colony, thus representing a potential competitor for mates, or merely a visitor from elsewhere, may influence how males interact with others. Given the high cost of fighting, the ability to discern competitors may influence the nature of male-male interactions and ultimately influence how they allocate reproductive effort.

Optimizing lifetime reproductive output: Intermittent breeding as a tactic for females in a long-lived, multiparous mammal.

In iteroparous species, intermittent breeding is an important life-history tactic that can greatly affect animal population growth and viability. Despite its importance, few studies have quantified the consequences of breeding pauses on lifetime reproductive output, principally because calculating lifetime reproductive output requires knowledge of each individual's entire reproductive history. This information is extremely difficult to obtain in wild populations. We applied novel statistical approaches that account for uncertainty in state assessment and individual heterogeneity to an 18-year capture-recapture dataset of 6,631 female southern elephant seals from Macquarie Island. We estimated survival and breeding probabilities, and investigated the consequences of intermittent breeding on lifetime reproductive output. We found consistent differences in females' demographic performance between two heterogeneity classes. In particular, breeding imbued a high cost on survival in the females from the heterogeneity class 2, assumed to be females of lower quality. Individual quality also appeared to play a major role in a female's decision to skip reproduction with females of poorer quality more likely to skip breeding events than females of higher quality. Skipping some breeding events allowed females from both heterogeneity classes to increase lifetime reproductive output over females that bred annually. However, females of lower quality produced less offspring over their lifetime. Intermittent breeding seems to be used by female southern elephant seals as a tactic to offset reproductive costs on survival and enhance lifetime reproductive output but remains unavoidable and driven by individual-specific constraints in some other females.

Decadal changes in habitat characteristics influence population trajectories of southern elephant seals.

Understanding divergent biological responses to climate change is important for predicting ecosystem level consequences. We use species habitat models to predict the winter foraging habitats of female southern elephant seals and investigate how changes in environmental variables within these habitats may be related to observed decreases in the Macquarie Island population. There were three main groups of seals that specialized in different ocean realms (the sub-Antarctic, the Ross Sea and the Victoria Land Coast). The physical and climate attributes (e.g. wind strength, sea surface height, ocean current strength) varied amongst the realms and also displayed different temporal trends over the last two to four decades. Most notably, sea ice extent increased on average in the Victoria Land realm while it decreased overall in the Ross Sea realm. Using a species distribution model relating mean residence times (time spent in each 50 × 50 km grid cell) to 9 climate and physical co-variates, we developed spatial predictions of residence time to identify the core regions used by the seals across the Southern Ocean from 120°E to 120°W. Population size at Macquarie Island was negatively correlated with ice concentration within the core habitat of seals using the Victoria Land Coast and the Ross Sea. Sea ice extent and concentration is predicted to continue to change in the Southern Ocean, having unknown consequences for the biota of the region. The proportion of Macquarie Island females (40%) utilizing the relatively stable sub-Antarctic region, may buffer this population against longer-term regional changes in habitat quality, but the Macquarie Island population has persistently decreased (-1.45% per annum) over seven decades indicating that environmental changes in the Antarctic are acting on the remaining 60% of the population to impose a long-term population decline in a top Southern Ocean predator.

Seal mothers expend more on offspring under favourable conditions and less when resources are limited.

In mammals, maternal expenditure on offspring is a complex mix of several factors including the species' mating system, offspring sex and the condition and age of the mother. While theory suggests that in polygynous species mothers should wean larger male offspring than females when resources and maternal conditions allow, the evidence for this remains equivocal. Southern elephant seals are highly dimorphic, polygynous capital breeders existing in an environment with highly variable resources and should therefore provide clear evidence to support the theoretical expectations of differential maternal expenditure in male and female pups. We quantified maternal size (mass and length) and pup size at birth and weaning for 342 elephant seal mothers at Macquarie Island. The study was conducted over 11 years of contrasting sea-ice and Southern Annular Mode values, both indices of maternal prey resources. Overall, large females weaned male pups that weighed 17 kg (15·5%) more than female pups. Maternal condition varied by as much as 59 kg among years, and was positively related to Southern Annular Mode, and negatively to maximum sea-ice extent. Smaller mothers weaned relatively larger male pups under favourable conditions, this effect was less apparent for larger mothers. We developed a simple model linking environmental variation to maternal masses post-partum, followed by maternal masses post-partum to weaning masses and then weaning masses to pup survival and demonstrated that environmental conditions affected predicted survival so that the pups of small mothers had an estimated 7% increase in first year survival in 'good' vs. 'bad' years compared to 1% for female pups of large mothers. Co-occurrence of environmental quality and conservative reproductive tactics suggests that mothers retain substantial plasticity in maternal care, enhancing their lifetime reproductive success by adjusting reproductive expenditure relative to both prevailing environmental conditions and their own capabilities.

Colony Location and Captivity Influence the Gut Microbial Community Composition of the Australian Sea Lion (Neophoca cinerea).

UNLABELLED: Gut microbiota play an important role in maintenance of mammalian metabolism and immune system regulation, and disturbances to this community can have adverse impacts on animal health. To better understand the composition of gut microbiota in marine mammals, fecal bacterial communities of the Australian sea lion (Neophoca cinerea), an endangered pinniped with localized distribution, were examined. A comparison of samples from individuals across 11 wild colonies in South and Western Australia and three Australian captive populations showed five dominant bacterial phyla: Firmicutes, Proteobacteria, Bacteroidetes, Actinobacteria, and Fusobacteria The phylum Firmicutes was dominant in both wild (76.4% ± 4.73%) and captive animals (61.4% ± 10.8%), while Proteobacteria contributed more to captive (29.3% ± 11.5%) than to wild (10.6% ± 3.43%) fecal communities. Qualitative differences were observed between fecal communities from wild and captive animals based on principal-coordinate analysis. SIMPER (similarity percentage procedure) analyses indicated that operational taxonomic units (OTU) from the bacterial families Clostridiaceae and Ruminococcaceae were more abundant in wild than in captive animals and contributed most to the average dissimilarity between groups (SIMPER contributions of 19.1% and 10.9%, respectively). Differences in the biological environment, the foraging site fidelity, and anthropogenic impacts may provide various opportunities for unique microbial establishment in Australian sea lions. As anthropogenic disturbances to marine mammals are likely to increase, understanding the potential for such disturbances to impact microbial community compositions and subsequently affect animal health will be beneficial for management of these vulnerable species. IMPORTANCE: The Australian sea lion is an endangered species for which there is currently little information regarding disease and microbial ecology. In this work, we present an in-depth study of the fecal microbiota of a large number of Australian sea lions from geographically diverse wild and captive populations. Colony location and captivity were found to influence the gut microbial community compositions of these animals. Our findings significantly extend the baseline knowledge of marine mammal gut microbiome composition and variability.

Taking animal tracking to new depths: synthesizing horizontal--vertical movement relationships for four marine predators.

In animal ecology, a question of key interest for aquatic species is how changes in movement behavior are related in the horizontal and vertical dimensions when individuals forage. Alternative theoretical models and inconsistent empirical findings mean that this question remains unresolved. Here we tested expectations by incorporating the vertical dimension (dive information) when predicting switching between movement states ("resident" or "directed") within a state-space model. We integrated telemetry-based tracking and diving data available for four seal species (southern elephant, Weddell, antarctic fur, and crabeater) in East Antarctica. Where possible, we included dive variables derived from the relationships between (1) dive duration and depth (as a measure of effort), and (2) dive duration and the postdive surface interval (as a physiological measure of cost). Our results varied within and across species, but there was a general tendency for the probability of switching into "resident" state to be positively associated with shorter dive durations (for a given depth) and longer postdive surface intervals (for a given dive duration). Our results add to a growing body of literature suggesting that simplistic interpretations of optimal foraging theory based only on horizontal movements do not directly translate into the vertical dimension in dynamic marine environments. Analyses that incorporate at least two dimensions can test more sophisticated models of foraging behavior.

Frequency of multiple paternity in gummy shark, Mustelus antarcticus, and rig, Mustelus lenticulatus, and the implications of mate encounter rate, postcopulatory influences, and reproductive mode.

Elasmobranchs (sharks and rays) show an amazing diversity of reproductive modes and behaviors. Multiple paternity (MP) has been identified in all species where more than 1 litter has been investigated; yet neither direct nor indirect benefits from MP have been determined in elasmobranchs. This has led to the suggestion that MP in this group may simply be a product of convenience polyandry with variation in the frequency of MP driven by differences in mate encounter rates. Here, we use molecular markers to investigate polyandry and MP in 2 closely related and commercially important species of shark, Mustelus antarcticus and Mustelus lenticulatus. In total, 328 M. antarcticus embryos originating from 29 different mothers and 75 M. lenticulatus embryos originating from 19 different mothers were genotyped using 8 microsatellite loci. We find that MP occurs in both species. However, in both species, the majority of litters were sired by a single father. Our results do not support increased fecundity per se as a driver of MP. Further, our results do not suggest that high population densities with resulting high mate encounter rates generated by breeding aggregations necessarily lead to high frequencies of MP. Importantly, we note evidence of reproductive skew within polyandrous litters, which is a predicted outcome of postcopulatory mechanisms.

Genetic divergence, speciation and biogeography of Mustelus (sharks) in the central Indo-Pacific and Australasia.

The shark genus Mustelus is speciose, commercially important and systematically troublesome. We use a molecular approach combining inter and intra-specific data to investigate Mustelus species in the central Indo-Pacific and Australasia. Our analysis supports two Mustelus clades, one comprising species with no white spots and a placental reproductive mode and a second clade of white spotted, aplacental species. Levels of genetic divergence are low, especially among species in the white spotted, aplacental clade and this should be taken into account when employing molecular data to delineate species. Our data support the hypothesis of a radiation following dispersal from a northern hemisphere ancestor. Molecular dating suggests that localised speciation in Australasia may have occurred during the Pleistocene. We propose that some of the difficulties associated with Mustelus systematics relate to a recent radiation, particularly in the Australasian region.

Social olfaction in marine mammals: wild female Australian sea lions can identify their pup's scent.

Historically, anatomical evidence has suggested that marine mammals are anosmic or at best microsmatic, i.e. absent or reduced olfactory capabilities. However, these neuroanatomical considerations may not be appropriate predictors for the use of olfaction in social interactions. Observations suggest that pinnipeds may use olfaction in mother-pup interactions, accepting or rejecting pups after naso-nasal contact. Such maternal-offspring recognition is a favourable area for investigating the involvement of odours in social recognition and selectivity, as females are evolutionarily constrained to direct resources to filial young. However, there is no experimental, morphological or chemical evidence to date for the use of olfaction in social contexts and for individual odour recognition abilities in pinnipeds. Here, we report unequivocal evidence that Australian sea lion (Neophoca cinerea) females can differentiate between the odour of their own pup and that of another, in the absence of any other distinguishing cues. This study demonstrates individual olfactory recognition in a free-ranging wild mammal and is clear evidence of the social function of olfaction in a marine mammal.

Predicting potential future reduction in shark bites on people.

Despite the low chance of a person being bitten by a shark, there are serious associated costs. Electronic deterrents are currently the only types of personal deterrent with empirical evidence of a substantial reduction in the probability of being bitten by a shark. We aimed to predict the number of people who could potentially avoid being bitten by sharks in Australia if they wear personal electronic deterrents. We used the Australian Shark Attack File from 1900 to 2020 to develop sinusoidal time-series models of per capita incidents, and then stochastically projected these to 2066. We predicted that up to 1063 people (range: 185-2118) could potentially avoid being bitten across Australia by 2066 if all people used the devices. Avoiding death and injury of people over the next half-century is of course highly desirable, especially when considering the additional costs associated with the loss of recreational, commercial and tourism revenue potentially in the tens to hundreds of millions of dollars following clusters of shark-bite events.

The memory remains: long-term vocal recognition in Australian sea lions.

The ability to recognize other individuals plays an important role in mediating social interactions. As longitudinal studies are challenging, there is only limited evidence of long-term memory of individuals and concepts in mammals. We examined the ability of six wild Australian sea lions to discriminate between the voice of their mother and another adult female, both while they were dependent on their mother and when they were independent, 2 years after weaning. Here, we show that even after a long period of independence, juveniles retain the ability to identify their mother's voice. Both when dependent and independent, animals showed stronger responses to maternal calls than to the calls of another female. This demonstration of recognition provides rare evidence of the long-term memory capabilities of wild mammals.

A continuous-time state-space model for rapid quality control of argos locations from animal-borne tags.

BACKGROUND: State-space models are important tools for quality control and analysis of error-prone animal movement data. The near real-time (within 24 h) capability of the Argos satellite system can aid dynamic ocean management of human activities by informing when animals enter wind farms, shipping lanes, and other intensive use zones. This capability also facilitates the use of ocean observations from animal-borne sensors in operational ocean forecasting models. Such near real-time data provision requires rapid, reliable quality control to deal with error-prone Argos locations. METHODS: We formulate a continuous-time state-space model to filter the three types of Argos location data (Least-Squares, Kalman filter, and Kalman smoother), accounting for irregular timing of observations. Our model is deliberately simple to ensure speed and reliability for automated, near real-time quality control of Argos location data. We validate the model by fitting to Argos locations collected from 61 individuals across 7 marine vertebrates and compare model-estimated locations to contemporaneous GPS locations. We then test assumptions that Argos Kalman filter/smoother error ellipses are unbiased, and that Argos Kalman smoother location accuracy cannot be improved by subsequent state-space modelling. RESULTS: Estimation accuracy varied among species with Root Mean Squared Errors usually <5 km and these decreased with increasing data sampling rate and precision of Argos locations. Including a model parameter to inflate Argos error ellipse sizes in the north - south direction resulted in more accurate location estimates. Finally, in some cases the model appreciably improved the accuracy of the Argos Kalman smoother locations, which should not be possible if the smoother is using all available information. CONCLUSIONS: Our model provides quality-controlled locations from Argos Least-Squares or Kalman filter data with accuracy similar to or marginally better than Argos Kalman smoother data that are only available via fee-based reprocessing. Simplicity and ease of use make the model suitable both for automated quality control of near real-time Argos data and for manual use by researchers working with historical Argos data.

Delayed onset of vocal recognition in Australian sea lion pups (Neophoca cinerea).

In pinnipeds, maternal care strategies and colony density may influence a species' individual recognition system. We examined the onset of vocal recognition of mothers by Australian sea lion pups (Neophoca cinerea). At 2 months of age, pups responded significantly more to the calls of their own mothers than alien female calls demonstrating a finely tuned recognition system. However, newborn pups did not respond differentially to the calls of their mother from alien female calls suggesting that vocal recognition had not yet developed or is not yet expressed. These findings are in stark contrast to other otariid species where pups learn their mother's voice before their first separation. Variance in colony density, pup movements, and natal site fidelity may have reduced selective pressures on call recognition in young sea lions, or alternatively, another sensory system may be used for recognition in the early stage of life.