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Concept: Otter

179

The use of information provided by others to tackle life’s challenges is widespread, but should not be employed indiscriminately if it is to be adaptive. Evidence is accumulating that animals are indeed selective and adopt ‘social learning strategies’. However, studies have generally focused on fish, bird and primate species. Here we extend research on social learning strategies to a taxonomic group that has been neglected until now: otters (subfamily Lutrinae). We collected social association data on captive groups of two gregarious species: smooth-coated otters (Lutrogale perspicillata), known to hunt fish cooperatively in the wild, and Asian short-clawed otters (Aonyx cinereus), which feed individually on prey requiring extractive foraging behaviours. We then presented otter groups with a series of novel foraging tasks, and inferred social transmission of task solutions with network-based diffusion analysis. We show that smooth-coated otters can socially learn how to exploit novel food sources and may adopt a ‘copy when young’ strategy. We found no evidence for social learning in the Asian short-clawed otters. Otters are thus a promising model system for comparative research into social learning strategies, while conservation reintroduction programmes may benefit from facilitating the social transmission of survival skills in these vulnerable species.

Concepts: Otters, Mustelidae, Mammals of Asia, Otter, Social, Aonyx, Smooth-coated Otter, Lutrogale

166

The increase in Eurasian otter Lutra lutra populations in their natural range and recolonization processes are recently observed in several European countries. We address the process of otter recolonization and habitat utilization in Central Poland over 14 years. Field surveys in 1998 and 2007 documented increase in occurrence of the species. The frequency of positive sites denoted 15 % in 1993, 38 % in 1998, and 89 % in 2007. Otter occurrence at study sites was positively affected by river width while negatively affected by presence of buildings at the site and river regulation. During the most intensive colonization process in the 1990s, the habitat preferences of the otter did not change. However, the sites inhabited by otters after 1998 were characterized by lower river width and tree cover and were more often located on regulated river sections, suggesting change in habitat tolerance during expansion. The otter abundance in transformed habitats is a result of increasing population numbers and the necessity to inhabit suboptimal sections of watercourses. Thus, it seems that presence-absence data for otter populations cannot be considered a reliable indicator of habitat quality, being depended of the population density.

Concepts: Population, Population density, Otters, Mustelidae, Otter, European Otter

113

At 50 kg in estimated weight, the extinct Siamogale melilutra is larger than all living otters, and ranks among the largest fossil otters. The biomechanical capability of S. melilutra jaws as related to their large size is unknown but crucial to reconstructing the species' potentially unique ecological niche. Here we compare the mandibular biomechanics of S. melilutra using engineering-based performance measures against ten extant otter biomechanical models. Despite a wide range of feeding preferences from durophagy to piscivory, living otter species exhibit a linear relationship between mandible stiffness and volume, as expected in isometric model scaling. In contrast, S. melilutra models exhibit a six-fold increase in stiffness from expected stiffness-volume relationships calculated from extant species models. Unlike stiffness, mechanical efficiency of biting is conserved among living otters and in S. melilutra. These findings indicate that although similar to living bunodont otters in morphology and biting efficiency, jaw strength in S. melilutra far surpasses molluscivores such as sea otters and Cape clawless otters, even after accounting for size. Therefore, Siamogale represents a feeding ecomorphology with no living analog, and its giant size and high mandibular strength confer shell-crushing capability matched only by other extinct molluscivores such as the marine bear Kolponomos.

Concepts: Biomechanics, Extinction, Otters, Mustelidae, Sea otter, Otter, Extant taxon, Aonyx

28

Failure to account for interactions between endangered species may lead to unexpected population dynamics, inefficient management strategies, waste of scarce resources, and, at worst, increased extinction risk. The importance of species interactions is undisputed, yet recovery targets generally do not account for such interactions. This shortcoming is a consequence of species-centered legislation, but also of uncertainty surrounding the dynamics of species interactions and the complexity of modeling such interactions. The northern sea otter (Enhydra lutris kenyoni) and one of its preferred prey, northern abalone (Haliotis kamtschatkana), are endangered species for which recovery strategies have been developed without consideration of their strong predator-prey interactions. Using simulation-based optimization procedures from artificial intelligence, namely reinforcement learning and stochastic dynamic programming, we combined sea otter and northern abalone population models with functional-response models and examined how different management actions affect population dynamics and the likelihood of achieving recovery targets for each species through time. Recovery targets for these interacting species were difficult to achieve simultaneously in the absence of management. Although sea otters were predicted to recover, achieving abalone recovery targets failed even when threats to abalone such as predation and poaching were reduced. A management strategy entailing a 50% reduction in the poaching of northern abalone was a minimum requirement to reach short-term recovery goals for northern abalone when sea otters were present. Removing sea otters had a marginally positive effect on the abalone population but only when we assumed a functional response with strong predation pressure. Our optimization method could be applied more generally to any interacting threatened or invasive species for which there are multiple conservation objectives. Definición de Metas de Recuperación Realistas para Dos Especies en Peligro Interactuantes, Enhydra lutris y Haliotis kamtschatkana.

Concepts: Predation, Lotka–Volterra equation, Endangered species, Extinction, Mustelidae, Sea otter, Otter, Biodiversity Action Plan

26

Color discrimination ability can be determined through anatomy or perceptual ability. In this study we tested perceptual ability. Three Asian small-clawed otters (Aonyx cinerea), one male and two females, were trained via operant conditioning to discriminate stimuli within a training task. If they passed criteria for this task, they were tested on as many as six delayed matching-to-sample experimental tasks. These experimental tasks involved comparing varying saturations of the colors blue, green, and red against varying shades of gray, as well as against each other. The male reached criterion on five of the experimental tasks, indicating an ability to discriminate the stimuli. One female participated in only two tasks and did not achieve the criteria as set. The second female did not pass the training task, and thus was not experimentally tested. This study overall showed some early evidence that Asian small-clawed otters may have the ability to learn to discriminate different stimuli on the basis of color cues. Sensory studies conducted on two other otter species and the results of this study indicate that color vision may be a common trait across Lutrinae species.

Concepts: Gender, Otters, Mammals of Asia, Otter, Aonyx, Oriental Small-clawed Otter

12

The Japanese otter lived throughout four main Japanese islands, but it has not been observed in the wild since 1979 and was declared extinct in 2012. Although recent taxonomic and molecular phylogenetic studies suggest that it should be treated as an independent species, International Union for Conservation of Nature Red List considers it as subspecies of Lutra lutra. Therefore, the taxonomic status of this species needs to be resolved. Here we determined the complete mitochondrial genome of two Japanese otters caught in Kanagawa and Kochi prefectures and five Eurasian otters (L. lutra). We reconstructed a molecular phylogenetic tree to estimate the phylogenetic position of the Japanese otter in Lutrinae using the Japanese otters and the other 11 Lutrinae species on the basis of ND5 (692 bp) and cytochrome b (1,140 bp) sequences. We observed that the two Japanese otters had close relationships with Eurasian otters, forming a monophyletic group (100% bootstrap probability). To elucidate detailed phylogenetic relationships among the Japanese and Eurasian otters, we reconstructed a maximum likelihood tree according to mitochondrial genome sequences (14,740 bp). The Japanese otter (JO1) collected in Kanagawa was deeply nested in the Eurasian otter clade, whereas the Japanese otter (JO2) collected in Kochi formed a distinct independent lineage in the Lutra clade. The estimated molecular divergences time for the ancestral lineages of the Japanese otters was 0.10 Ma (95%: 0.06-0.16 Ma) and 1.27 Ma (95%: 0.98-1.59 Ma) for JO1 and JO2 lineages, respectively. Thus, JO1 was identified as a member of L. lutra; JO2 represented the old Japanese otter lineage, which may be a distinct new species or subspecies of Lutra. We suggest that the ancestral population of the JO2 lineage migrated to Japan via the land bridge that existed between western Japanese islands and Asian continent at 1.27 Ma.

Concepts: Phylogenetics, Otters, Mustelidae, Otter

10

The northern sea otter inhabits coastal waters of the northern Pacific Ocean and is the largest member of the Mustelidae family. DNA sequencing methods that utilize microfluidic partitioned and non-partitioned library construction were used to establish the sea otter genome. The final assembly provided 2.426 Gbp of highly contiguous assembled genomic sequences with a scaffold N50 length of over 38 Mbp. We generated transcriptome data derived from a lymphoma to aid in the determination of functional elements. The assembled genome sequence and underlying sequence data are available at the National Center for Biotechnology Information (NCBI) under the BioProject accession number PRJNA388419.

Concepts: DNA, Human Genome Project, Genome, Sequence, Pacific Ocean, Mustelidae, Sea otter, Otter

9

Variation in terrestrial mammalian skull morphology is known to constrain feeding performance, which in turn influences dietary habits and ultimately fitness. Among mustelids, otters have evolved two feeding specializations: underwater raptorial capture of prey (mouth-oriented) and capture of prey by hand (hand-oriented), both of which have likely associations with morphology and bite performance. However, feeding biomechanics and performance data for otters are sparse. The first goal of this study was to investigate the relationships between feeding morphology and bite performance among two mouth-oriented piscivores (Pteronura brasiliensis and Lontra canadensis) and two hand-oriented invertebrate specialists (Enhydra lutris and Aonyx cinerea). Since other vertebrate taxa that are mouth-oriented piscivores tend to possess longer skulls and mandibles, with jaws designed for increased velocity at the expense of biting capability, we hypothesized that mouth-oriented otters would also possess long, narrow skulls indicative of high velocity jaws. Conversely, hand-oriented otters were expected to possess short, blunt skulls with adaptations to increase bite force and crushing capability. Concomitant with these skull shapes we hypothesized that sea otters would possess a greater mandibular bluntness index, providing for a greater mechanical advantage compared to other otter species investigated. A second goal was to examine morphological variation at a finer scale by assessing variation in cranial morphology among three sea otter subspecies. Since diet varies among these subspecies, and their populations are isolated, we hypothesized that the magnitude of mandibular bluntness and concomitant mechanical advantage, as well as occlusal surface area would also vary within species according to their primary food source (fish versus hard invertebrates). Functional expectations were met for comparisons among and within species. Among species the phylogeny suggests a deeply rooted transition to alternative foraging types. Yet within foraging types alternative species were also strongly variable, suggesting either selective differences in the extent or nature of realized foraging mode, or an accumulation of non-adaptive changes during the long independent evolutionary history. At the finest scale, variation among subspecies indicates that trophic adaptation occurred rapidly, making it interesting that we happened to find both deeply and shallowly-rooted transformations associated with diet type in otter species and subspecies.

Concepts: Evolution, Species, Otters, Mustelidae, Sea otter, Otter, Lontra, Aonyx

8

Cooperative problem solving has gained a lot of attention over the past two decades, but the range of species studied is still small. This limits the possibility of understanding the evolution of the socio-cognitive underpinnings of cooperation. Lutrinae show significant variations in socio-ecology, but their cognitive abilities are not well studied. In the first experimental study of otter social cognition, we presented two species-giant otters and Asian small-clawed otters-with a cooperative problem-solving task. The loose string task requires two individuals to simultaneously pull on either end of a rope in order to access food. This task has been used with a larger number of species (for the most part primates and birds) and thus allows for wider cross-species comparison. We found no differences in performance between species. Both giant otters and Asian small-clawed otters were able to solve the task successfully when the coordination requirements were minimal. However, when the temporal coordination demands were increased, performance decreased either due to a lack of understanding of the role of a partner or due to difficulty inhibiting action. In conclusion, two species of otters show some ability to cooperate, quite similar to most other species presented with the same task. However, to draw further conclusions and more nuanced comparisons between the two otter species, further studies with varied methodologies will be necessary.

Concepts: Psychology, Problem solving, Otters, Mustelidae, Mammals of Asia, Otter, Aonyx, Oriental Small-clawed Otter

7

Commercial hunting for the international trade in animal hides in the 20th century decimated many populations of aquatic wildlife in Amazonia. However, impacts varied significantly between different species and regions, depending upon hunting intensity, accessibility of habitat, and the inherent resilience of various species and their habitats. We investigated the differential responses of two Amazonian Mustelid species, the neotropical otter and giant otter, to commercial hunting pressure along the upper Rio Negro in Brazil, and examined historical factors that influenced spatial and temporal variation in commercial exploitation. We analyzed previously unanalyzed data from historical records of hide shipments to track changes in hide sales and prices for the two species in the late 20th century. We also gathered oral histories from older Baniwa people who had witnessed or participated in commercial otter hunting. These complimentary data sources reveal how intrinsic biological and social characteristics of the two otter species interacted with market forces and regional history. Whereas giant otter populations were driven to local or regional extinction during the late 20th century by commercial hunting, neotropical otters persisted. In recent decades, giant otter populations have returned to some parts of the upper Rio Negro, a development which local people welcome as part of a generalized recovery of the ecosystems in their territory as a result of the banning of animal pelt exports and indigenous land demarcation. This paper expands the scope of the field historical ecology and reflects on the role of local knowledge in biodiversity conservation.

Concepts: Conservation biology, 20th century, Brazil, History, Otters, Mustelidae, Otter, Hides