From low to high latitudes: changes in fatty acid desaturation in mammalian fat tissue suggest a thermoregulatory role.

BACKGROUND: Most fatty acids (FAs) making up the adipose tissue in mammals have a dietary origin and suffer little modification when they are stored. However, we propose that some of those FAs, specifically those that can be synthesised or modified by mammals, are also being influenced by thermal forces and used as part of the mechanism to regulate core body temperature. As FA desaturation increases, adipose tissues can reach colder temperatures without solidifying. The ability to cool the superficial fat tissues helps create a thermal gradient, which contributes to body heat loss reduction. Therefore, it is expected that animals exposed to colder environments will possess adipose tissues with higher proportions of desaturated FAs. Here, through a model selection approach that accounts for phylogeny, we investigate how the variation in FA desaturation in 54 mammalian species relates to the thermal proxies: latitude, physical environment (terrestrial, semi-aquatic and fully-aquatic) and hair density. RESULTS: The interaction between the environment (terrestrial, semi- or fully-aquatic) and the latitude in which the animals lived explained best the variation of FA desaturation in mammals. Aquatic mammals had higher FA desaturation compared to terrestrial mammals. Semi-aquatic mammals had significantly higher levels of desaturated FAs when living in higher latitudes whereas terrestrial and fully-aquatic mammals did not. To account for dietary influence, a double bond index was calculated including all FAs, and revealed no correlation with latitude in any of the groups. CONCLUSIONS: We propose that FA modification is an important component of the thermoregulatory strategy, particularly in semi-aquatic mammals. Potentially this is because, like terrestrial mammals, they experience the greatest air temperature variations across latitudes, but they lack a thick fur coat and rely primarily on their blubber. Unlike fully-aquatic mammals, extremely thick blubber is not ideal for semi-aquatic mammals, as this is detrimental to their manoeuvrability on land. Therefore, the adipose tissue in semi-aquatic mammals plays a more important role in keeping warm, and the modification of FAs becomes crucial to withstand cold temperatures and maintain a pliable blubber.

Examining predator-prey body size, trophic level and body mass across marine and terrestrial mammals.

Predator-prey relationships and trophic levels are indicators of community structure, and are important for monitoring ecosystem changes. Mammals colonized the marine environment on seven separate occasions, which resulted in differences in species' physiology, morphology and behaviour. It is likely that these changes have had a major effect upon predator-prey relationships and trophic position; however, the effect of environment is yet to be clarified. We compiled a dataset, based on the literature, to explore the relationship between body mass, trophic level and predator-prey ratio across terrestrial (n = 51) and marine (n = 56) mammals. We did not find the expected positive relationship between trophic level and body mass, but we did find that marine carnivores sit 1.3 trophic levels higher than terrestrial carnivores. Also, marine mammals are largely carnivorous and have significantly larger predator-prey ratios compared with their terrestrial counterparts. We propose that primary productivity, and its availability, is important for mammalian trophic structure and body size. Also, energy flow and community structure in the marine environment are influenced by differences in energy efficiency and increased food web stability. Enhancing our knowledge of feeding ecology in mammals has the potential to provide insights into the structure and functioning of marine and terrestrial communities.

Source levels of the underwater calls of a male leopard seal.

Leopard seals (Hydrurga leptonyx) are top predators in the Antarctic ecosystem. They produce stereotyped calls as part of a stylized underwater vocal display. Understanding of their acoustic behavior is improved by identifying the amplitude of their calls. The amplitude of five types of calls (n = 50) from a single male seal were measured as broadband source levels and ranged from 153 to 177 dB re 1 µPa at 1 m. The mean source levels differed between call types, the lower frequency calls (L, D, and O) tended to have source levels 10 dB higher than the higher frequency calls (H and M). Information on call-type source levels is important to take into account for passive acoustic studies investigating repertoire usage as calls produced with greater amplitudes are likely to have larger acoustic ranges, especially when these are also the calls with lower frequencies, such as is the case in leopard seals.

BASSA: New software tool reveals hidden details in visualisation of low-frequency animal sounds.

The study of animal sounds in biology and ecology relies heavily upon time-frequency (TF) visualisation, most commonly using the short-time Fourier transform (STFT) spectrogram. This method, however, has inherent bias towards either temporal or spectral details that can lead to misinterpretation of complex animal sounds. An ideal TF visualisation should accurately convey the structure of the sound in terms of both frequency and time, however, the STFT often cannot meet this requirement. We evaluate the accuracy of four TF visualisation methods (superlet transform [SLT], continuous wavelet transform [CWT] and two STFTs) using a synthetic test signal. We then apply these methods to visualise sounds of the Chagos blue whale, Asian elephant, southern cassowary, eastern whipbird, mulloway fish and the American crocodile. We show that the SLT visualises the test signal with 18.48%-28.08% less error than the other methods. A comparison between our visualisations of animal sounds and their literature descriptions indicates that the STFT's bias may have caused misinterpretations in describing pygmy blue whale songs and elephant rumbles. We suggest that use of the SLT to visualise low-frequency animal sounds may prevent such misinterpretations. Finally, we employ the SLT to develop 'BASSA', an open-source, GUI software application that offers a no-code, user-friendly tool for analysing short-duration recordings of low-frequency animal sounds for the Windows platform. The SLT visualises low-frequency animal sounds with improved accuracy, in a user-friendly format, minimising the risk of misinterpretation while requiring less technical expertise than the STFT. Using this method could propel advances in acoustics-driven studies of animal communication, vocal production methods, phonation and species identification.

Diet and phylogeny shape the gut microbiota of Antarctic seals: a comparison of wild and captive animals.

The gut microbiota of mammals underpins the metabolic capacity and health of the host. Our understanding of what influences the composition of this community has been limited primarily to evidence from captive and terrestrial mammals. Therefore, the gut microbiota of southern elephant seals, Mirounga leonina, and leopard seals, Hydrurga leptonyx, inhabiting Antarctica were compared with captive leopard seals. Each seal exhibited a gut microbiota dominated by four phyla: Firmicutes (41.5 ± 4.0%), Fusobacteria (25.6 ± 3.9%), Proteobacteria (17.0 ± 3.2%) and Bacteroidetes (14.1 ± 1.7%). Species, age, sex and captivity were strong drivers of the composition of the gut microbiota, which can be attributed to differences in diet, gut length and physiology and social interactions. Differences in particular prey items consumed by seal species could contribute to the observed differences in the gut microbiota. The longer gut of the southern elephant seal provides a habitat reduced in available oxygen and more suitable to members of the phyla Bacteroidetes compared with other hosts. Among wild seals, 16 'core' bacterial community members were present in the gut of at least 50% of individuals. As identified between southern elephant seal mother-pup pairs, 'core' members are passed on via vertical transmission from a young age and persist through to adulthood. Our study suggests that these hosts have co-evolved with their gut microbiota and core members may provide some benefit to the host, such as developing the immune system. Further evidence of their strong evolutionary history is provided with the presence of 18 shared 'core' members in the gut microbiota of related seals living in the Arctic. The influence of diet and other factors, particularly in captivity, influences the composition of the community considerably. This study suggests that the gut microbiota has co-evolved with wild mammals as is evident in the shared presence of 'core' members.

Living in human-modified landscapes narrows the dietary niche of a specialised mammalian scavenger.

Anthropogenic impacts on carnivores can be complex, posing numerous threats to many species, yet also benefits to those able to exploit certain resources. This balancing act is particularly precarious for those adapters that exploit dietary resources provided by humans, but still require other resources only available in native habitat. Here we measure the dietary niche of one such species, the Tasmanian devil (Sarcophilus harrisii), a specialised mammalian scavenger, across an anthropogenic habitat gradient stretching from cleared pasture to undisturbed rainforest. Populations inhabiting areas of greater disturbance showed restricted dietary niches, suggesting that all individuals fed on similar food items, even within regenerated native forest. Populations in undisturbed rainforest habitats had comparatively broad diets and showed evidence of niche partitioning by body size, which may reduce intraspecific competition. Despite the potential benefits of reliable access to high-quality food items in anthropogenically-modified habitats, the constrained niches we observed may be harmful, indicating altered behaviours and potentially increasing the rate of fights between individuals over food. This is of particular concern for a species at risk of extinction due to a deadly cancer primarily transmitted through aggressive interactions. The lack of diversity in devil diets within regenerated native forest compared to those in old-growth rainforest also indicates the conservation value of the latter for both the devil and the species which they consume.

Effects of intraspecific competition and body mass on diet specialization in a mammalian scavenger.

Animals that rely extensively on scavenging rather than hunting must exploit resources that are inherently patchy, dangerous, or subject to competition. Though it may be expected that scavengers should therefore form opportunistic feeding habits in order to survive, a broad species diet may mask specialization occurring at an individual level. To test this, we used stable isotope analysis to analyze the degree of specialization in the diet of the Tasmanian devil, one of few mammalian species to develop adaptations for scavenging. We found that the majority of individuals were dietary specialists, indicating that they fed within a narrow trophic niche despite their varied diet as a species. Even in competitive populations, only small individuals could be classified as true trophic generalists; larger animals in those populations were trophic specialists. In populations with reduced levels of competition, all individuals were capable of being trophic specialists. Heavier individuals showed a greater degree of trophic specialization, suggesting either that mass is an important driver of diet choice or that trophic specialization is an efficient foraging strategy allowing greater mass gain. Devils may be unique among scavenging mammals in the extent to which they can specialize their diets, having been released from the competitive pressure of larger carnivores.

Conditions influencing the appearance of thermal windows and the distribution of surface temperature in hauled-out southern elephant seals.

Pinnipeds (true seals, sea lions and walruses) inhabit two thermally different environments, air and water, so need to make continuous adjustments to maintain a balanced body temperature. The thermal isolation properties of thick blubber keep warmth within the body's core, ideal for mammals while in the water; however, when on land, this thick blubber makes it difficult to lose heat. Some pinnipeds use thermal windows, discrete patches where temperature changes on their body surface, as a mechanism to dissipate excessive heat. We identify the factors that correlate with the appearance of thermal windows and changes in body surface temperature on southern elephant seals, Mirounga leonina, while they are hauled out ashore. Infrared thermography was used to measure surface temperature of the seals. Temperature was lower on the torso than the flippers and head, suggesting that not all body sites have the same role in thermal balance. Air temperature was the main driver of variation in the surface temperature of the seals' flippers and head; seals cool their superficial tissues when the air temperature is below ~ 2°C. This minimizes heat loss by reducing the thermal gradient between their skin and the ambient air. Wind speed was the main predictor of whether thermal windows appear on a seals' body surface. When wind speed was minimal, thermal windows occurred more often, which may be associated with either hair and skin drying, or producing thermal conditions for hair and skin regrowth. The type of aggregation (huddled or alone) influenced the surface temperature of the fore flippers; however, we did not find statistical influence of the seal's sex, state of moult, or the substrate on which they were hauled out (kelp or sand). Understanding how animals maintain their thermal balance is important if we are to predict how they will respond to future climate change.

Multiple pygmy blue whale acoustic populations in the Indian Ocean: whale song identifies a possible new population.

Blue whales were brought to the edge of extinction by commercial whaling in the twentieth century and their recovery rate in the Southern Hemisphere has been slow; they remain endangered. Blue whales, although the largest animals on Earth, are difficult to study in the Southern Hemisphere, thus their population structure, distribution and migration remain poorly known. Fortunately, blue whales produce powerful and stereotyped songs, which prove an effective clue for monitoring their different 'acoustic populations.' The DGD-Chagos song has been previously reported in the central Indian Ocean. A comparison of this song with the pygmy blue and Omura's whale songs shows that the Chagos song are likely produced by a distinct previously unknown pygmy blue whale population. These songs are a large part of the underwater soundscape in the tropical Indian Ocean and have been so for nearly two decades. Seasonal differences in song detections among our six recording sites suggest that the Chagos whales migrate from the eastern to western central Indian Ocean, around the Chagos Archipelago, then further east, up to the north of Western Australia, and possibly further north, as far as Sri Lanka. The Indian Ocean holds a greater diversity of blue whale populations than thought previously.

Evaluating the performance of the Bayesian mixing tool MixSIAR with fatty acid data for quantitative estimation of diet.

We test the performance of the Bayesian mixing model, MixSIAR, to quantitatively predict diets of consumers based on their fatty acids (FAs). The known diets of six species, undergoing controlled-feeding experiments, were compared with dietary predictions modelled from their FAs. Test subjects included fish, birds and mammals, and represent consumers with disparate FA compositions. We show that MixSIAR with FA data accurately identifies a consumer's diet, the contribution of major prey items, when they change their diet (diet switching) and can detect an absent prey. Results were impacted if the consumer had a low-fat diet due to physiological constraints. Incorporating prior information on the potential prey species into the model improves model performance. Dietary predictions were reasonable even when using trophic modification values (calibration coefficients, CCs) derived from different prey. Models performed well when using CCs derived from consumers fed a varied diet or when using CC values averaged across diets. We demonstrate that MixSIAR with FAs is a powerful approach to correctly estimate diet, in particular if used to complement other methods.

Foraging behaviour of the South American sea lion (Otaria byronia) in two disparate ecosystems assessed through blubber fatty acid analysis.

Fatty acids have been widely used as trophic biomarkers in marine mammals. However, for the South American sea lion, the most abundant otariid in the eastern South Pacific, there is no information about blubber fatty acids and their link to diet. Here, we compare fatty acid profiles of sea lions from two distinct oceanographic regions in northern and southern Chile. Their fatty acids vary greatly between regions, suggesting dietary differences at a spatial scale. The fatty acid C22:6ω3 was more abundant in sea lions from the northern region, likely associated with consumption of anchovy, cephalopods, and crustaceans, which are rich in that fatty acid, and have been reported as their main prey items. Sea lions from the southern region were richer in C22:1 and C20:1, characteristic of teleost fish, suggesting a piscivorous diet. Males displayed a more diverse fatty acid composition than females, suggesting a wider trophic niche. Few individual sea lions within the southern region had unusually high levels of C18:2ω6, commonly found in terrestrial environments. This suggests consumption of farmed salmon, whose diet is usually based on terrestrial sources. This demonstrates how human intervention is being reflected in the tissues of a top predator in a natural environment.

Age-related differences in the acoustic characteristics of male leopard seals, Hydrurga leptonyx.

During the breeding season, the underwater vocalizations and calling rates of adult male leopard seals are highly stereotyped. In contrast, sub-adult males have more variable acoustic behavior. Although adult males produce only five stereotyped broadcast calls as part of their long-range underwater breeding displays the sub-adults have a greater repertoire including the adult-like broadcast calls, as well as variants of these. Whether this extended repertoire has a social function is unknown due to the paucity of behavioral data for this species. The broadcast calls of the sub-adults are less stereotyped in their acoustic characteristics and they have a more variable calling rate. These age-related differences have major implications for geographic variation studies, where the acoustic behavior of different populations are compared, as well as for acoustic surveying studies, where numbers of calls are used to indicate numbers of individuals present. Sampling regimes which unknowingly include recordings from sub-adult animals will artificially exaggerate differences between populations and numbers of calling animals. The acoustic behavior of sub-adult and adult male leopard seals were significantly different and although this study does not show evidence that these differences reflect vocal learning in the male leopard seal it does suggest that contextual learning may be present.

Calling underwater is a costly signal: size-related differences in the call rates of Antarctic leopard seals.

It is proposed that where sexually selected vocal communication is an honest signal, the call production rate is predicted to change throughout the breeding season. Male leopard seals call underwater for many hours each day over their three- to four-month breeding season, and it is hypothesized that a decrease in calling rate would be associated with the declining body condition of smaller males. The calling rates of leopard seals were measured (N = 49 recordings) and compared between seals of different size classes throughout the breeding season. Male leopard seals produce their calls at more stable rates as they become larger. In this study, larger male leopard seals adopted a strategy of consistent underwater calling throughout the breeding season, whereas there was a breakdown in the calling stereotypy of the smaller males at its height. Toward the end of the breeding season, the smaller seals produced fewer calls in shortened calling bouts, and they took more rest periods. Therefore, underwater calling may represent an honest signal in the leopard seal. For marine mammals that call underwater, the production of repetitive sequences advertises the breath-holding ability of the caller to the listeners, and this ability may be related to male stamina and endurance, thus representing an honest signal that could be widespread in other species.

Does size matter? Examining the drivers of mammalian vocalizations.

Previous studies of the vocalization frequencies of mammals have suggested that it is either body mass or environment that drives these frequencies. Using 193 species across the globe from the terrestrial and aquatic environments and a model selection approach, we identified that the best-supported model for minimum and maximum frequencies for vocalization included both body mass and environment. The minimum frequencies of vocalizations of species from all environments retained the influence of body mass. For maximum frequency however, aquatic species are released from such a trend with body mass having little constraint on frequencies. Surprisingly, phylogeny did not have a strong impact on the evolution of the maximum frequency of mammal vocalizations, largely due to the pinniped species divergence of frequency from their carnivoran relatives. We demonstrate that the divergence of signal frequencies in mammals has arisen from the need to adapt to their environment.

Temporal segregation of the Australian and Antarctic blue whale call types (Balaenoptera musculus spp.).

We examined recordings from a 15-month (May 2009-July 2010) continuous acoustic data set collected from a bottom-mounted passive acoustic recorder at a sample frequency of 6kHz off Portland, Victoria, Australia (38°33'01″S, 141°15'13″E) off southern Australia. Analysis revealed that calls from both subspecies were recorded at this site, and general additive modeling revealed that the number of calls varied significantly across seasons. Antarctic blue whales were detected more frequently from July to October 2009 and June to July 2010, corresponding to the suspected breeding season, while Australian blue whales were recorded more frequently from March to June 2010, coinciding with the feeding season. In both subspecies, the number of calls varied with time of day; Antarctic blue whale calls were more prevalent in the night to early morning, while Australian blue whale calls were detected more often from midday to early evening. Using passive acoustic monitoring, we show that each subspecies adopts different seasonal and daily call patterns which may be related to the ecological strategies of these subspecies. This study demonstrates the importance of passive acoustics in enabling us to understand and monitor subtle differences in the behavior and ecology of cryptic sympatric marine mammals.

Calls reveal population structure of blue whales across the southeast Indian Ocean and the southwest Pacific Ocean.

For effective species management, understanding population structure and distribution is critical. However, quantifying population structure is not always straightforward. Within the Southern Hemisphere, the blue whale (Balaenoptera musculus) complex is extremely diverse but difficult to study. Using automated detector methods, we identified "acoustic populations" of whales producing region-specific call types. We examined blue whale call types in passive acoustic data at sites spanning over 7,370 km across the southeast Indian Ocean and southwest Pacific Ocean (SWPO) from 2009 to 2012. In the absence of genetic resolution, these acoustic populations offer unique information about the blue whale population complex. We found that the Australian continent acts as a geographic boundary, separating Australia and New Zealand blue whale acoustic populations at the junction of the Indian and Pacific Ocean basins. We located blue whales in previously undocumented locations, including the far SWPO, in the Tasman Sea off the east coast of Australia, and along the Lau Basin near Tonga. Our understanding of population dynamics across this broad scale has significant implications to recovery and conservation management for this endangered species, at a regional and global scale.

Examining the prey mass of terrestrial and aquatic carnivorous mammals: minimum, maximum and range.

Predator-prey body mass relationships are a vital part of food webs across ecosystems and provide key information for predicting the susceptibility of carnivore populations to extinction. Despite this, there has been limited research on the minimum and maximum prey size of mammalian carnivores. Without information on large-scale patterns of prey mass, we limit our understanding of predation pressure, trophic cascades and susceptibility of carnivores to decreasing prey populations. The majority of studies that examine predator-prey body mass relationships focus on either a single or a subset of mammalian species, which limits the strength of our models as well as their broader application. We examine the relationship between predator body mass and the minimum, maximum and range of their prey's body mass across 108 mammalian carnivores, from weasels to baleen whales (Carnivora and Cetacea). We test whether mammals show a positive relationship between prey and predator body mass, as in reptiles and birds, as well as examine how environment (aquatic and terrestrial) and phylogenetic relatedness play a role in this relationship. We found that phylogenetic relatedness is a strong driver of predator-prey mass patterns in carnivorous mammals and accounts for a higher proportion of variance compared with the biological drivers of body mass and environment. We show a positive predator-prey body mass pattern for terrestrial mammals as found in reptiles and birds, but no relationship for aquatic mammals. Our results will benefit our understanding of trophic interactions, the susceptibility of carnivores to population declines and the role of carnivores within ecosystems.

Virtual reconstruction and prey size preference in the mid Cenozoic thylacinid, Nimbacinus dicksoni (Thylacinidae, Marsupialia).

Thylacinidae is an extinct family of Australian and New Guinean marsupial carnivores, comprizing 12 known species, the oldest of which are late Oligocene (∼24 Ma) in age. Except for the recently extinct thylacine (Thylacinus cynocephalus), most are known from fragmentary craniodental material only, limiting the scope of biomechanical and ecological studies. However, a particularly well-preserved skull of the fossil species Nimbacinus dicksoni, has been recovered from middle Miocene (∼16-11.6 Ma) deposits in the Riversleigh World Heritage Area, northwestern Queensland. Here, we ask whether N. dicksoni was more similar to its recently extinct relative or to several large living marsupials in a key aspect of feeding ecology, i.e., was N. dicksoni a relatively small or large prey specialist. To address this question we have digitally reconstructed its skull and applied three-dimensional Finite Element Analysis to compare its mechanical performance with that of three extant marsupial carnivores and T. cynocephalus. Under loadings adjusted for differences in size that simulated forces generated by both jaw closing musculature and struggling prey, we found that stress distributions and magnitudes in the skull of N. dicksoni were more similar to those of the living spotted-tailed quoll (Dasyurus maculatus) than to its recently extinct relative. Considering the Finite Element Analysis results and dental morphology, we predict that N. dicksoni likely occupied a broadly similar ecological niche to that of D. maculatus, and was likely capable of hunting vertebrate prey that may have exceeded its own body mass.

The gut bacterial community of mammals from marine and terrestrial habitats.

After birth, mammals acquire a community of bacteria in their gastro-intestinal tract, which harvests energy and provides nutrients for the host. Comparative studies of numerous terrestrial mammal hosts have identified host phylogeny, diet and gut morphology as primary drivers of the gut bacterial community composition. To date, marine mammals have been excluded from these comparative studies, yet they represent distinct examples of evolutionary history, diet and lifestyle traits. To provide an updated understanding of the gut bacterial community of mammals, we compared bacterial 16S rRNA gene sequence data generated from faecal material of 151 marine and terrestrial mammal hosts. This included 42 hosts from a marine habitat. When compared to terrestrial mammals, marine mammals clustered separately and displayed a significantly greater average relative abundance of the phylum Fusobacteria. The marine carnivores (Antarctic and Arctic seals) and the marine herbivore (dugong) possessed significantly richer gut bacterial community than terrestrial carnivores and terrestrial herbivores, respectively. This suggests that evolutionary history and dietary items specific to the marine environment may have resulted in a gut bacterial community distinct to that identified in terrestrial mammals. Finally we hypothesize that reduced marine trophic webs, whereby marine carnivores (and herbivores) feed directly on lower trophic levels, may expose this group to high levels of secondary metabolites and influence gut microbial community richness.