Diet composition of the Eurasian otter Lutra lutra in different freshwater habitats of temperate Europe: a review and meta‐analysis

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Amphibians in Eurasian otter Lutra lutra diet: osteological identification unveils hidden prey richness and male‐biased predation on anurans

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Native European eels as a potential biological control for invasive crayfish

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A re‐evaluation of the role of killer whales Orcinus orca in a population decline of sea otters Enhydra lutris in the Aleutian Islands and a review of alternative hypotheses

• 1 During the past 15–20 years, sea otters Enhydra lutris in the Aleutian Islands, Alaska, USA, experienced a drastic decrease in population size. It has been hypothesized that an increase in killer whale Orcinus orca predation was the primary cause of this decline.
• 2 Causation of the decline by increased killer whale predation is now considered a textbook case of top‐down predator control. The purpose of this review is to re‐evaluate the evidence for killer whale predation and to review evidence for alternative causes.
• 3 The killer whale predation hypothesis is based on three lines of evidence: (i) there was an increase in the number of observed killer whale attacks on sea otters during the 1990s, coincident with a decline in sea otters, (ii) sea otter populations did not decline in areas considered inaccessible to killer whales, while they declined in adjacent areas considered accessible to killer whales, and (iii) the estimated number of attacks necessary to account for the rate of decline is similar to the observed number of attacks. Our re‐evaluation indicates that although the killer whale hypothesis is by no means disproved, the supporting data are limited and inconclusive.
• 4 Increases in shark populations in the Aleutian Islands concurrent with the sea otter population declines indicate the need for further research into the role of alternative marine predators in the population decline.
• 5 High contaminant levels observed in sea otters in the Aleutian Islands warrant further investigation into the impact of these toxins on sea otter health and vital rates, and their possible role on the population decline.
• 6 Disease has not been ruled out as a significant contributor to the population decline, particularly in the early stages of the decline.

     

Rethinking trophic niches: Speed and body mass colimit prey space of mammalian predators

1. Realized trophic niches of predators are often characterized along a one‐dimensional range in predator–prey body mass ratios. This prey range is constrained by an “energy limit” and a “subdue limit” toward small and large prey, respectively. Besides these body mass ratios, maximum speed is an additional key component in most predator–prey interactions.
2. Here, we extend the concept of a one‐dimensional prey range to a two‐dimensional prey space by incorporating a hump‐shaped speed‐body mass relation. This new “speed limit” additionally constrains trophic niches of predators toward fast prey.
3. To test this concept of two‐dimensional prey spaces for different hunting strategies (pursuit, group, and ambush predation), we synthesized data on 63 terrestrial mammalian predator–prey interactions, their body masses, and maximum speeds.
4. We found that pursuit predators hunt smaller and slower prey, whereas group hunters focus on larger but mostly slower prey and ambushers are more flexible. Group hunters and ambushers have evolved different strategies to occupy a similar trophic niche that avoids competition with pursuit predators. Moreover, our concept suggests energetic optima of these hunting strategies along a body mass axis and thereby provides mechanistic explanations for why there are no small group hunters (referred to as “micro‐lions”) or mega‐carnivores (referred to as “mega‐cheetahs”).
5. Our results demonstrate that advancing the concept of prey ranges to prey spaces by adding the new dimension of speed will foster a new and mechanistic understanding of predator trophic niches and improve our predictions of predator–prey interactions, food web structure, and ecosystem functions.

     

Trophic diversity of the otter (Lutra lutra L.) in temperate and Mediterranean freshwater habitats

Aim To analyse the geographical patterns in the composition and diversity of otter's (Lutra lutra L.) diet and their relationship with climatic characteristics. Location European freshwater habitats under Mediterranean and temperate climatic regimes. Methods Thirty‐seven otter diet studies were reviewed, twenty‐one from temperate and sixteen from Mediterranean areas. All studies were based on spraint analysis and their results expressed as relative frequency of occurrence of seven main prey categories. Principal Component Analysis was performed to extract the main gradients of diet composition. Pearson's correlation and t‐tests were used to assess the relationship between diet characteristics (composition, diversity and taxonomic richness) and geographical and climatic variables. Results A clear latitudinal gradient in diet composition was observed. Otter diet was more diverse and featured more prey classes in southern localities, while the species was more piscivorous towards the north, where it predated upon a higher number of fish families. This pattern was similar when temperate and Mediterranean localities of Europe were compared. Mediterranean otters behaved as more generalist predators than temperate ones, relying less on fish, and more on aquatic invertebrates and reptiles. Main conclusions Geographical differences in otter feeding ecology in Europe seem to be related with the two contrasted climatic conditions affecting prey populations. The otter can act as a highly specialized piscivorous predator in temperate freshwater ecosystems, which do not suffer a dry season and have a comparatively stable water regime compared to Mediterranean ones. However, the unpredictable prey availability in Mediterranean areas, affected by strong spatial and temporal water shortages, favours a diversification of the otter's diet.     

Understanding the inter-specific dynamics of two co-existing predators in the Tierra del Fuego Archipelago: the native southern river otter and the exotic American mink

Knowledge about interactions between endangered native southern river otters (Lontra provocax) and introduced American mink (Neovison vison) is essential for effective management of both species. We evaluated competition for spatial and trophic niches between otter and mink in overlapping and non-overlapping areas, comparing distribution, habitat preference, diet and mink marking behavior. We surveyed otter and mink signs along 250 km of Beagle Channel coastline. Habitat suitability models were constructed based on species presence/absence and habitat characteristics, using generalized linear models. Feces were collected for diet analyses. Otters used forested coasts with 12°–32° shoreline slope and without human influence, and our evidence suggests they were not affected by mink presence. Mink preferred forested and shrubland coasts with 10°–28° shoreline slope. Neither human influence nor otter presence affected mink habitat occupation, but in the presence of otters, mink left fewer signs. Otters consumed more aquatic prey than mink, and mink modified their diet in the presence of otters, consuming more exotic small terrestrial mammals and less fish as well as shifting to smaller and shallower fish species that are less consumed by otters. Mink showed more plastic, generalist behavior than otters, being more tolerant of human presence, using more habitat types and having greater diet breadth. At the same time, otters apparently affect mink adversely and could help limit their invasion in sympatric areas. Conservation and recovery of otters, therefore, may produce a secondary benefit of simultaneously reducing the effect of mink, thereby providing an additional way to control this exotic predator’s population.     

Influence of occupation history and habitat on Washington sea otter diet

Habitat characteristics are primary determinants of nearshore marine communities. However, biological drivers like predation can also be important for community composition. Sea otters (Enhydra lutris ssp.) are a salient example of a keystone species exerting top‐down control on ecosystem community structure. The translocation and subsequent population growth and range expansion of the northern sea otter (Enhydra lutris kenyoni) in Washington State over the last five decades has created a spatio‐temporal gradient in sea otter occupation time and density, and acts as a natural experiment to quantify how sea otter population status and habitat type influence sea otter diet. We collected focal observations of sea otters foraging at sites across the gradient in varying habitat types between 2010 and 2017. We quantified sea otter diet composition and diversity, and long‐term rates of energy gain across the gradient. We found that sea otter diet diversity was positively correlated with cumulative sea otter density, while rate of energy gain was negatively correlated with cumulative density. Additionally, we found that habitat type explained 1.77 times more variance in sea otter diet composition than sea otter cumulative density. Long‐term diet studies can provide a broader picture of sea otter population status in Washington State.     

Feeding habits of the otter and the American mink in Bialowieza Primeval Forest (Poland) compared to other Eurasian populations

Diets of the otter Lutra lutra and the American mink Mustela vison were studied by scat analysis on five woodland rivers and streams in eastern Poland. Fish constituted 51% of food biomass consumed by otters in spring‐summer and 40% in autumn‐winter, with common fish (perch Perca fluviatilis, pike Esox lucius, and roach Rutilus rutilus) being captured most frequently by the otters. Amphibians (mainly Rana temporaria, which also dominated in the living community) made up 34% of otters’ food biomass in spring‐summer and 58% in autumn‐winter. American mink relied on three prey groups: fish (40% in spring‐summer, and 10% in autumn‐winter), frogs (32% and 51%, respectively), and small mammals (21% and 36%). Out of available Micromammalia, mink strongly selected the root vole Microtus oeconomus. The cold season diet of both otter and mink depended on river size. On small rivers with forested valleys, otters and mink fed nearly exclusively on amphibians (72–90% of food biomass). With size of a river increasing and riverside habitat becoming more open (sedge and reed marshes instead of forests), otters shifted to catching predominantly fish (up to 76% in diet) and mink to preying on small mammals (up to 65% in diet).
Review of literature on otter and mink in Eurasia showed that their diets did not change with latitude (as indicators of climate severity and duration of water freezing) but they depended on habitats. In otter diet, the mean share of fish declined from 94% (SE 1.7) on sea shores, to 71% (SE 2.9) on lakes and fish ponds, to 64% (SE 2.8) on rivers and streams. The roles of amphibians and crustaceans increased in the same gradient (from 0 to 15%, and from 3 to 7%, respectively). On inland waters, the abundance of crayfish was the essential factor differentiating otters’ diet composition. In Eurasia, the staple food types of American mink on rivers and streams were fish (on average, 27% in diet, SE 3.9), mammals (30%, SE 5.0), and amphibians (17%, SE 4.8), whereas on lakes and ponds mink fed predominantly on birds (on average, 33% in diet, SE 10.1) and fish (28%, SE 9.5). In the Palaearctic region, over a wide gradient of habitats, otters appeared strongly specialised on prey taken from water, whereas American mink was a typical generalist capable of utilising several prey groups originating from both water and land.     

Commensal association of the common kingfisher with foraging Eurasian otters

Positive interactions between birds and mammals are a fascinating aspect of animal behaviour. Feeding associations may consist of local enhancement or facilitation, and in the latter case, of commensalism or mutualism depending on the benefits received by the facilitator. We report here on a previously undescribed feeding association between piscivorous birds and Eurasian otters Lutra lutra. In Spain, common kingfisher Alcedo atthis and grey heron Ardea cinerea were observed closely following foraging otters and benefited from feeding opportunities provided by these. Behavioural observations of otters in central Spain (28.4 hr; 19 days) revealed that an association with kingfishers occurred in 33% of otter foraging events (n = 92). Simultaneous observations in northern Spain (14.2 hr; 16 days) showed an association between otters and kingfishers or grey herons in 41.6% and 11.7% of otter foraging events (n = 77), respectively. The association probability between kingfishers and otters increased significantly when otters foraged closer to the shore and on small fish rather than other prey (crayfish or large fish). Birds fed on prey remain left by the feeding otters, on small fish captured by otters when these were satiated and playing, or on prey displaced by otters. Our observations are consistent with facilitation and commensalism: piscivorous birds gained feeding opportunities provided by the otters, with no apparent costs or benefits to the latter. Similar feeding associations have been described between other species of otters and piscivorous birds (kingfishers, herons, egrets, storks) in Asia, South America and Southern Africa, but had not yet been described in Europe. The occurrence of piscivorous bird–otter associations in different species and regions suggests that this commensalism may be often overlooked but widespread. We have shown that the association can be frequent and is context‐dependent, with benefits for associating birds depending on otters´ behaviour and targeted prey.     

Flow‐mediated predator–prey dynamics influence fish populations in a tropical river

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Effects of prey abundance,distribution, visual contrast and morphology on selection by a pelagic piscivore

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Review and quantitative meta-analysis of diet suggests the Eurasian otter (Lutra lutra) is likely to be a poor bioindicator

The Eurasian otter (Lutra lutra L.) is a top predator in aquatic systems and plays an important role in ecosystem functioning. However, it has undergone dramatic declines throughout Europe as a result of environmental degradation. We examine the putative role of the otter as a bioindicator in Ireland which remains a stronghold for the species and affords a unique opportunity to examine variation in its ecological niche. We describe diet, using spraint contents, along rivers during 2010 and conduct a review and quantitative meta-analysis of the results of a further 21 studies. We aimed to assess variation in otter diet in relation to river productivity, a proxy for natural nutrification and anthropogenic eutrophication, and availability of salmonid prey (Salmo trutta and Salmo salar), to test the hypothesis that otter diet is related to environmental quality. Otter diet did not vary with levels of productivity or availability of salmonids whilst Compositional Analysis suggested there was no selection of salmonid over non-salmonid fish. There was a distinct niche separation between riverine and lacustrine systems, the latter being dominated by Atlantic eel (Anguilla anguilla). Otters are opportunistic and may take insects, freshwater mussels, birds, mammals and even fruit. Otters living along coasts have a greatest niche breath than those in freshwater systems which encompasses a wide variety of intertidal prey though pelagic fish are rarely taken. It is concluded that the ability of the otter to feed on a wide diversity of prey taxa and the strong influence of habitat type, renders it a poor bioindicator of environmental water quality. It seems likely that the plasticity of the habitat and dietary niche of otters, and the extent of suitable habitat, may have sustained populations in Ireland despite intensification of agriculture during the 20th century.     

Density-dependent prey behaviours and mutable predator foraging modes induce Allee effects and over-prediction of prey mortality rates

1. Predator–prey models are often used to represent consumptive interactions between species but, typically, are derived using simple experimental systems with little plasticity in prey or predator behaviours. However, many prey and predators exhibit a broad suite of behaviours. Here, we experimentally tested the effect of density-dependent prey and predator behaviours on per capita relative mortality rates using Florida bass (Micropterus floridanus) consuming juvenile Bluegill (Lepomis macrochirus).
2. Experimental ponds were stocked with a factorial design of low, medium, and high prey and predator densities. Prey mortality, prey–predator behaviours, and predator stomach contents were recorded over or after 7 days. We assumed the mortality dynamics followed foraging arena theory. This pathologically flexible predator–prey model separates prey into invulnerable and vulnerable pools where predators can consume prey in the latter. As this approach can represent classic Lotka–Volterra and ratio-dependent dynamics, we fit a foraging arena predator–prey model to the number of surviving prey.
3. We found that prey exhibited density-dependent prey behaviours, hiding at low densities, shoaling at medium densities, and using a provided refuge at high densities. Predators exhibited ratio-dependent behaviours, using an ambush foraging mode when one predator was present, hiding in the shadows at low prey–high predator densities, and shoaling at medium and high prey–high predator densities. The foraging arena model predicted the mortality rates well until the high prey–high predator treatment where group vigilance prey behaviours occurred and predators probably interfered with one another resulting in the model predicting higher mortality than observed.
4. This is concerning given the ubiquity of predator–prey models in ecology and natural resource management. Furthermore, as Allee effects engender instability in population regulation, it could lead to inaccurate predictions of conservation status, population rebuilding or harvest rates.

     

Body mass relationships affect the age structure of predation across carnivore–ungulate systems: a review and synthesis

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Do non‐native fish as prey favour the conservation of the threatened indigenous Eurasian otter?

1. Biological invasions are considered a major threat to biodiversity. Most research has focused on the distribution, biology and impacts of non‐native species on native fauna and flora. However, few studies have explored their role as prey for native predators of conservation concern. 2. To assess the incidence and intensity of predation by the Eurasian otter Lutra lutra on established non‐native fish species, data were collated from the published literature. To be selected, studies had to cover at least 1 year, analyse more than 100 spraints and report the study period and percentage relative frequency (%RF) of all prey fish species. 3. To permit reliable, time‐related comparisons with %RF of non‐native fishes in otter diet, we also reviewed available information about both the distribution of non‐native fishes and history of their introductions to European countries, revealing a decrease with longitude in the number of naturalised non‐native fishes taken (ranging between 5 and 34) and their percentage in each fish assemblage. 4. Our selective criteria were met by 30 dietary studies from 44 study areas in 15 European countries during 1970–2010. The extent to which otters rely on non‐native fishes was almost negligible (mean %RF = 4.8), with the number of non‐native fishes preyed upon by otters decreasing with both latitude and longitude. 5. The %RF of non‐native fish in the diet increased slightly with time, with otters preying significantly more on non‐native fish in study areas where alterations of the fish assemblage had been highlighted in the reference papers. No relationship was found between otter diet breadth and the occurrence of non‐native fishes in their diet. 6. The current role of non‐native species in otter diet suggests that effective otter conservation management plans should focus on the maintenance and/or enhancement of native fish assemblages.     

Temperature and prey density jointly influence trophic and non‐trophic interactions in multiple predator communities

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Determinants of dietary specialization: a comparison of two sympatric species of sea snakes

Why do some predator species specialize on only a single type of prey whereas others take a broad range? One critical determinant may be the ontogenetic range of body sizes of the predator compared to that of its prey. If any single prey taxon spans only part of the range of prey sizes ingestible by the predator, then the predator will be more likely to take multiple prey taxa. We exploit a model system that provides a robust opportunity to test this hypothesis. We studied two sympatric species of predatory sea snakes, similar in size and general ecology that feed on anguilliform fishes from different habitats in the Great Lagoon of New Caledonia. Eel species from soft‐bottom habitats must construct their own burrows, and thus tend to be more slender‐bodied and less variable in body size than eel species that inhabit variable‐sized crevices among hard coral. As a result, a laticaudine sea snake species (Laticauda saintgironsi) that feeds on hard‐coral‐dwelling eels relies primarily on a single prey species: juveniles take young eels whereas adults consume adult eels of the same species. In contrast, a laticaudine species (L. laticaudata) that forages on soft‐bottom eels switches its prey ontogenetically: juveniles take small eel species whereas adults consume large eel species. Thus, habitat‐imposed constraints on the range of body sizes within each prey taxon generate a striking difference in the degree of dietary specialization of two closely related, sympatric predator species.     

Habitat heterogeneity and mammalian predator–prey interactions

• 1 In predator–prey theory, habitat heterogeneity can affect the relationship between kill rates and prey or predator density through its effect on the predator's ability to search for, encounter, kill and consume its prey. Many studies of predator–prey interactions include the effect of spatial heterogeneity, but these are mostly based on species with restricted mobility or conducted in experimental settings.
• 2 Here, we aim to identify the patterns through which spatial heterogeneity affects predator–prey dynamics and to review the literature on the effect of spatial heterogeneity on predator–prey interactions in terrestrial mammalian systems, i.e. in freely moving species with high mobility, in non‐experimental settings. We also review current methodologies that allow the study of the predation process within a spatial context.
• 3 When the functional response includes the effect of spatial heterogeneity, it usually takes the form of predator‐dependent or ratio‐dependent models and has wide applicability.
• 4 The analysis of the predation process through its different stages may further contribute towards identifying the spatial scale of interest and the specific spatial mechanism affecting predator–prey interactions.
• 5 Analyzing the predation process based on the functional response theory, but separating the stages of predation and applying a multiscale approach, is likely to increase our insight into how spatial heterogeneity affects predator–prey dynamics. This may increase our ability to forecast the consequences of landscape transformations on predator–prey dynamics.

     

Disturbance cues as a source of risk assessment information under natural conditions

1. Disturbance cues are released by stressed or disturbed prey prior to a predator attack and convey useful risk assessment information regarding local threats. While studies have shown that disturbance cues may be important early on within the predation sequence (prior to an attack), their role in predator–prey interactions remains relatively overlooked by ecologists. Critically, experimental studies examining disturbance cues, especially among prey fishes, have been conducted primarily under laboratory or semi-natural conditions.
2. Here, we tested the prediction that disturbance cues function as sources of risk assessment information in situ. We exposed Trinidadian guppies, in two natural populations differing in predation risk, to a model predator paired with stream water or the disturbance cue collected from guppies from either a high- or low-predation risk population.
3. We found that the predator inspection response of guppies to disturbance cues depends on the level of risk of both the focal and the cue source population. Guppies from both populations exhibited increased latencies to inspect, lower inspection rates and reduced inspecting group sizes towards the model paired with conspecific disturbance cues versus a stream water control. Interestingly, guppies of both populations showed evidence of higher perceived predation risk towards the disturbance cues collected from high-predation risk donors compared to low-predation risk donors.
4. Our results support the hypothesis that disturbance cues function as a source of information used by prey fish in the assessment of predation risk and provide the first evidence of disturbance cue function under fully natural conditions.