Biological and Conservation Aspects of Otter Mortality: A Review

: The post mortem exam is important in diagnosing and investigating wildlife diseases. It is even more important to monitor the population of species that are not easily observed in the wild, such as otters. Of the 13 otter species, 11 are endangered due to many factors, such as climate change, pollution, or urbanisation. The authors present a review of the patterns of mortality of free-ranging otters worldwide, aiming to improve the knowledge of otter mortality and the role of mortality studies in their conservation. The main cause of death in aquatic otters is vehicle collision; hence, sea otter deaths are associated with shark attacks and imprisonment in fishing gear. It is possible to conclude that humans and human activity play a significant role in the mortality of these animals. In the future, a more standardised analysis of otter carcasses is necessary to understand their threats and diseases and design significant measures to protect these species.


Introduction
Otters, mammals from the order Carnivora, display remarkable diversity and adaptability across various environments, including rivers, lakes, coastal areas, wetlands, and aquatic environments around the globe.As semi-aquatic predators within the Mustelidae family, otters exhibit a range of physical and behavioural adaptations that allow them to thrive in freshwater and marine ecosystems.Otters exist on all continents except Australia and Antarctica [1,2].These animals exhibit diverse diets that vary significantly across species and habitats, reflecting their adaptability and role as top predators in aquatic environments [3].They primarily feed on fish, but their diet includes amphibians, crustaceans, and occasionally small mammals and birds [4,5].For instance, sea otters' diets (Enhydra lutris), are composed mainly of marine invertebrates, including sea urchins, crabs, shrimps, clamps, molluscs, and fish.Giant otters (Pteronura brasiliensis) hunt in groups, often preying on large fish species.The Neotropical otter (Lontra longicaudis) diet includes fish, crustaceans, invertebrates, and small vertebrates, and the Eurasian otter (Lutra lutra) has a diet that largely consists of fish but can also include birds, amphibians, and crustaceans [6].
There are 13 recognised species of otters belonging to the subfamily Lutrinae within the family Mustelidae [7].These species are distributed across various aquatic habitats worldwide, from freshwater rivers and lakes to coastal and marine environments.The Eurasian otter (Lutra lutra) is found across Europe, Asia, and North Africa.The North American River otter (Lontra canadensis) lives in North America.The Neotropical otter (Lontra longicaudis) is distributed throughout Central and South America.The Southern River otter (Lontra provocax) is found in Chile and Argentina.The Marine otter (Lontra felina) lives along the west coast of South America.The Giant otter (Pteronura brasiliensis) inhabits South America's Amazon, Orinoco, and La Plata river systems.The Smooth-coated otter (Lutrogale perspicillata) is found in the Indian subcontinent and Southeast Asia [8].
The Asian Small-clawed otter (Aonyx cinereus), the smallest otter species, is distributed in South and Southeast Asia.The African Clawless otter (Aonyx capensis) is found throughout much of sub-Saharan Africa.The Congo Clawless otter (Aonyx congicus) inhabits the Congo basin.The Hairy-nosed otter (Lutra sumatrana) is found in Southeast Asia and the Sea otter (Enhydra lutris) occupies the northern and eastern North Pacific Ocean and the spotted-necked otter (Hydrictis maculicollis) is in freshwater habitats across sub-Saharan Africa [8].
While otters are not typically known for long-distance migrations like some bird species or large mammals, there are instances where certain otter species exhibit seasonal movements or dispersal behaviours.Sea otters are known to move seasonally locally between coastal areas and offshore kelp forests.They follow the movement of their prey, such as sea urchins, and also seek out areas with more favourable environmental conditions [9].European otters may move between river systems or across land in search of suitable habitats or mates [6,10].Home ranges of otters vary in size according to species, location, and resource distribution, and are generally larger for males [11].For example, a female Alaska sea otter's home range may include 8 to 16 km of coastline.Eurasian otter home ranges can be around 15 km for males and around 7 km for females [12].
The necropsy exam is important in diagnosing and investigating wildlife diseases [16][17][18].It is even more important to monitor the population of species that are not easily seen in the wild, such as otters [3].Identifying the cause of death can reveal important information about the threats facing a species [3,19], including human-wildlife conflicts, such as vehicle collisions, habitat destruction, or illegal hunting [20,21].It also can play a crucial role in otter conservation strategy development [5,13] in several issues such as in disease surveillance monitoring, helping in the identification of diseases affecting otter populations [22]; in reproductive health assessment, helping to identify factors that may affect breeding success and population growth [2,23]; in the identification of exposure to environmental contaminants, pollutants, or toxins [21,23,24]; and monitoring population [13,25] and environmental health [26,27].In endangered species, it plays a crucial role in understanding health, diseases, and threats.Therefore, post mortem examinations can provide valuable insights into the causes of death, which are essential for conservation efforts aimed at protecting these vulnerable populations [13,25].
This work aims to improve the knowledge of otter mortality, reviewing the mortality pattern of free-ranging otters all around the world.

Materials and Methods
In this work, we present a review of the mortality pattern of free-ranging otters.The initial search included terms used in combination or isolated such as "otter", "Lutra", "Lontra", "aquatic otter", "aquatic mammal", "causes of death", "mortality", "sea otter", "morbidity", and "post-mortem", yielding 52 articles from digital databases ResearchGate and PubMed.Only articles providing detailed information on mortality causes or post mortem findings in free-ranging otters were considered as inclusion criteria.After screening abstracts, some articles were excluded because they did not focus on free-ranging or wild otters (7), there were limitations to access to the full article (4), there were language barriers (only manuscripts in English, Portuguese, Spanish, and French were included) (2), and there were duplicate studies (3) that were repeated.The final selection comprised 35 articles considered suitable for inclusion in this review [28].
Information regarding country, year, otter species, and mortality causes were extracted from the papers included in this review.Regarding the categories of mortality, the data available in the papers were very diverse.To simplify, the authors decided to divide into 12 categories as follows: shotgun (animals that died due to gun fires, and ammunition were found in the carcass), drowning and entrapment in fishing gear (animals that drowned where the cause of death was due to entrapment), vehicle collision, oil spill (cause of death was related to the effects of an oil spill), fight (death due to the wounds from other otter), train collision, nutritional disorders (juveniles or carcasses found in poor condition due to starvation without any disease or trauma associated), unknown (carcasses of animals that were found and no cause of death was identified), hunting (fur hunting), infectious diseases (diseases caused by viruses, bacteria, fungi, parasites, or other pathogenic agents), shark attack, and poisoning (pesticides, rodenticides, or other compounds).

Results
The 37 studies included in this review were published from 1968 to 2021.Studies on Lutra lutra were conducted over various periods spanning from the 1960s to 2017, with varying intervals, including observations in specific years such as 1979, 1990-2003, and 2009-2017, among others.Studies on Enhydra lutris kenyoni were primarily conducted between 2002 and 2015, with a specific observation interval within those years.Studies on Enhydra lutris nereis cover a broader period from 1968 to 2013, with several observations throughout these decades.Observations on Enhydra lutris were recorded from at least 1968 to 1999.Studies on Lontra canadensis were mainly conducted between 2002 and 2016, with some smaller intervals, including observations between 2003 and 2013.Studies on Pteronura brasiliensis were conducted between 2001 and 2015, with a few reports.

Distribution of Studies by Species
Our comprehensive literature review on otter mortality patterns has identified a distinct focus on several species across the included studies.Most studies focused on Lutra lutra, with 54.1% (n = 20) of the articles examining this species.The Southern Sea otter (Enhydra lutris nereis) was the second most studied species, representing 16.2% (n = 6) of the articles.Other studies included Lontra canadensis (8%, n = 3), Lutrogale perspicillata (8%, n = 3), and Lontra felina (2.7%, n = 1).Eight studies were conducted on endangered species.No other studies regarding mortality were found in the remaining 8 species of otters.

Geographical Distribution of the Studies
The geographical spread of studies demonstrates the global interest in otter mortality research, with significant contributions from North America and Europe.The United States of America (USA) leads the research about otter mortality, accounting for 32% of the studies (n = 12).The UK contributed to 18% of the studies (n = 7).The involvement of countries from other continents is less pronounced.Brazil was 8% (n = 3), and for Germany, France, and Sweden, each of these countries hosted 5% of the studies (n = 2 for each).Bulgaria, Czech Republic, Denmark, Hungary, Ireland, Israel, Italy, Peru, and Singapore were the locations for one study, making up 2.7% of the total each (n = 1 for each country).Figure 1 illustrates the worldwide distribution of mortality studies focused on various otter species, with colour coding representing each species.gapore were the locations for one study, making up 2.7% of the total each (n = 1 fo country).Figure 1 illustrates the worldwide distribution of mortality studies focus various otter species, with colour coding representing each species.

Causes of Mortality
The major causes of mortality described in the different papers were as follow lision with vehicle (n = 23) being in 2 cases a train collision, infectious diseases (n unknown causes (n = 15), drowning and entrapment in fishing gear (n = 14), fightin tween otters or with predators) (n = 11), shotgun injuries (n = 8), shark attacks (n poisoning (n = 7), nutritional disorders (n = 6), hunting (n = 4), and oil spills (n = 2).bly, 53% of otter mortality is connected to trauma, underscoring the significant imp both direct and indirect human activities on otter populations.Table 1 provides a de description of the different causes of death associated with the countries where these ies were conducted.

Causes of Mortality
The major causes of mortality described in the different papers were as follows: collision with vehicle (n = 23) being in 2 cases a train collision, infectious diseases (n = 20), unknown causes (n = 15), drowning and entrapment in fishing gear (n = 14), fighting (between otters or with predators) (n = 11), shotgun injuries (n = 8), shark attacks (n = 8), poisoning (n = 7), nutritional disorders (n = 6), hunting (n = 4), and oil spills (n = 2).Notably, 53% of otter mortality is connected to trauma, underscoring the significant impact of both direct and indirect human activities on otter populations.Table 1 provides a detailed description of the different causes of death associated with the countries where these studies were conducted.
The studies identify a high incidence of vehicle collisions.Countries like the UK and the USA report a high number of vehicle collision-related deaths.Drowning and entrapment in fishing gear is reported in Sweden and the USA.Regarding shotgun injuries and hunting, the USA reports the highest number of cases.The USA stands out for the highest number of deaths attributed to infectious diseases and shark attacks.Italy and the USA report deaths due to nutritional disorders, while a significant number of deaths in the USA are attributed to unknown causes.Some countries, like France and Ireland, report particular causes of mortality (e.g., drowning and entrapment in fishing gear in France).
Considering the mortality among otter species, for Lutra lutra, while specific causes such as shotgun injuries, roadkill, oil spills, fighting, train traffic, starvation/nutritional disorders, trauma unknown, and hunting/human intention were also documented, drowning, fishing gear, and infectious diseases stood out as the most prevalent mortality causes for this species.Among the mortality causes recorded for Enhydra lutris kenyoni, the most common were poisoning and starvation/nutritional disorders.For Enhydra lutris nereis, the most common causes varied, and included drowning, fishing gear, oil spills, fighting, and infectious diseases.The most common mortality causes for Lontra canadensis were fishing gear, intoxication, and shotgun incidents.For Lontra felina, the most common causes of death included drowning, fishing gear, fighting, and starvation/nutritional disorders.For Enhyrda lutris nereis, mortality causes most frequent were drowning, fishing gear, oil spills, and infectious diseases.The most common mortality causes for Lutrogale perspicillata were drowning, fighting, and starvation/nutritional disorders.The most common cause of death for Pteronura brasiliensis was unknown cause.Analysing the causes of mortality among otters in two distinct environments, aquatic and marine (Figure 2), it is possible to observe that the causes of mortality differ between marine and aquatic otters.The leading causes of death in aquatic species are collision with vehicles (n = 21) and drowning and entanglement in fishing gear (n = 9).In marine otters, the main causes of mortality are infectious diseases (n = 9) and shark attacks (n = 7).Both groups share several causes of mortality, including drowning and entrapment in fishing gear, unknown causes, infectious diseases, and fights.

Discussion
Otters, a key indicator species for aquatic ecosystems, face various threats that impact their survival.Otter numbers in many countries are decreasing, and their populations are becoming threatened [25,57].Otter declines are primarily attributed to human-induced factors, habitat degradation, and pollution.Mortality studies in otters play a crucial role in understanding the factors influencing otter populations, identifying key threats, and understanding population dynamics, and are essential for conservation efforts to ensure the long-term survival of these vulnerable species [21,42].
The studies included in this review span a considerable temporal range from 1971 to 2021.This fifty-year span underscores the ongoing interest and research efforts directed

Discussion
Otters, a key indicator species for aquatic ecosystems, face various threats that impact their survival.Otter numbers in many countries are decreasing, and their populations are becoming threatened [24,56].Otter declines are primarily attributed to human-induced factors, habitat degradation, and pollution.Mortality studies in otters play a crucial role in understanding the factors influencing otter populations, identifying key threats, and understanding population dynamics, and are essential for conservation efforts to ensure the long-term survival of these vulnerable species [20,41].
The studies included in this review span a considerable temporal range from 1971 to 2021.This fifty-year span underscores the ongoing interest and research efforts directed towards understanding mortality patterns in otters, reflecting changes in research focus and conservation concerns over time.
The geographical analysis of the studies shows a wide distribution across various countries, indicating the global interest in otter mortality research.The countries with the most published works were the United Kingdom and the USA [1,52].Most of the mortality studies presented were performed on aquatic species (n = 23), particularly L. lutra (n = 19) [1,52].This distribution of studies highlights the varied interest in otter species across different habitats and geographical locations, reflecting the global concern for otter conservation and the need for a comprehensive understanding of mortality patterns to inform conservation strategies.This high percentage of papers about L. lutra mortality underscores the significant interest in and concern for the Eurasian otter's mortality patterns and conservation status.Pteronura brasiliensis, L. feline (South American river otter) [54,55] and L. perspicillata (Smooth-coated otter) [37] were the least represented in the literature, which may point to a need for increased research attention.The low number of studies on both species can be attributed to their status as threatened species, resulting from fewer individuals in the wild.Additionally, the difficulty in accessing carcasses for study is compounded by the otters' habitats, which often include deep forests and mangrove swamps [8,13].It is important to mention that it is also necessary to look at further studies on species that are not incorporated in the papers included in this review [47,55].
Across all species, traumatic events are a major cause of death, with a significant proportion linked to human actions, such as collisions with vehicles, fishing gear entanglement, shotgun wounds, poisoning, and oil spills.Natural factors, including infectious diseases and cancer, along with poorly understood causes, also contribute to mortality rates.The available literature reinforces that over half of otter deaths can be attributed to trauma, highlighting the considerable effect of human activities on these populations [19,48,49].
The published data also suggest a habitat-influenced distinction in the causes of mortality for marine and aquatic otters.Marine otters suffer more from drowning, entanglement in nets, and shark attacks, aligning with the threats in their oceanic environment.On the other hand, aquatic otters are more prone to vehicle collisions, which might indicate their closer interactions with human-modified landscapes, such as roads near freshwater habitats.Across both species, the prominent causes of death are traumatic and heavily linked to human activities, underlining the significant impact that human presence and development have on wildlife, even in less accessible habitats [20,47,52].Fishing activities present a considerable threat to otters, with accidental capture in nets, traps, and lines being too common.Such entanglements often result in drowning or debilitating injuries, adversely affecting otter survival and mobility [48,52].This study compiles evidence from 13 research cases, highlighting that marine and aquatic otters are vulnerable to these dangers associated with fishing practices [47,48].
Shark attacks on sea otters represent a severe threat in regions where their habitats intersect, such as coastal waters and estuarine areas.These encounters are sometimes fatal for the otters, particularly when sharks search for food and mistake the otters for their usual prey.In the United States, there are several documented instances (noted in seven studies) where marine otters have fallen victim to shark attacks.This indicates a notable risk for otter populations in shark-inhabited waters [47,48,52].A case of predation by a terrestrial predator was also described for Pteronura brasiliensis, an aquatic species, by a jaguar (Panthera onca) [54].Is possible that more cases of predation occur, but usually the carcass is devoured by the predators.
Due to the necessity of crossing roads, aquatic otters are more susceptible to vehicle collisions, with a noted incidence rate (n = 23) [35,42].Roads can fragment otter habitats, forcing otters to cross them in search of food, mates, or a suitable habitat [42].Roads near water bodies or wetlands can become barriers to otter movement, forcing them to navigate through traffic.Due to their nocturnal or crepuscular behaviour, there is an increased risk of being struck by vehicles, as drivers may have reduced visibility during these times [22,34,42].High-speed roads with limited visibility, inadequate signage, or lack of otter crossings pose greater risks to otters and other wildlife [45].In some regions, train lines crossing through their habitats pose an additional threat to aquatic otters, making them susceptible to being run over by trains.This situation highlights the impact of transportation infrastructure on wildlife, particularly for species that require extensive, uninterrupted territories to thrive [30].
In 10 studies, one of the causes of death was wounds from fights between otters [22,32,42,48].Otters are known for their social and tolerant nature, often engaging in playful behaviours and living in groups.However, it is important to recognise that they can exhibit aggression under specific circumstances.This aggressive behaviour is particularly observed during the breeding season when competition for mates can lead to confrontations or when resources are limited [4,8].In some instances, injuries can result from more aggressive interactions, especially when individuals are defending territories or asserting dominance within their social groups [33,48].Also, these injuries sustained during conflicts may increase vulnerability to other threats such as predation, disease, or environmental hazards.Mortality resulting directly from fights between otters is not very common, although, in our study, 10 studies reported a cause of death of wounds from fights [32,42,48].
Otters, like many other animals, can be susceptible to a variety of infectious diseases.These diseases can be caused by bacteria, viruses, parasites, and fungi, and they can have significant impacts on otter populations [47,50].Although in most papers the mortality cause is only described as infectious diseases or natural causes, in some there is a description of the agents observed.Regarding viruses, some of the most described are distemper virus (CDV) and parvovirus (CPV) [15,47].Parasites that are common in otters are Ascaridae, Strongylidae, Angiostrongylus vasorum, Cestodae, Dirofilaria immitis, Metastrongyloid Toxoplasma gondii, Corynosoma spp., Isthmiophora melis, Oswaldocruzia filiformis, Sarcocystis lutrae, and S. neurona are, as some examples [14,57].A large variety of bacteria have been isolated from pneumonia, wounds, abscesses, and other infections [48,57].
Poisoning is also a significant cause of death, indicating the threat of environmental contaminants.A review of seven studies identified instances where otters died of poisoning.In some cases, humans may deliberately poison otters.This can occur in contexts with conflicts with fisheries or due to poaching activities.Fishermen may use poisons to eliminate perceived competitors or predators, inadvertently harming otters and other wildlife.Otters living in urban or industrialised areas are at risk of exposure to pollutants from industrial activities, including manufacturing, mining, and wastewater discharge.Chemicals such as heavy metals (e.g., mercury, lead, and cadmium) and industrial solvents can accumulate in the tissues of otters over time.This accumulation can lead to poisoning and various health issues [45].Also, otters residing in or near agricultural areas may come into contact with pesticides and fertilizers used in farming practices [36,58].Runoff of farm fields can transport these chemicals into waterways, affecting the prey and habitat of otters.If ingested directly or through contaminated prey, pesticides like organophosphates and rodenticides can be particularly toxic to otters [13].The discharge of untreated sewage and wastewater into otter habitats is another source of contamination by pathogens, pharmaceuticals, heavy metals, and other pollutants into the environment [12].Plastic pollution, particularly microplastics and macroplastics, poses a growing threat to otters and other marine mammals.Otters may inadvertently ingest plastic debris while foraging for food, leading to intestinal blockages, digestive issues, and nutrient deficiencies [54,55].
Otters primarily feed on fish, but their diet can also include amphibians, crustaceans, and occasionally small mammals and birds.This varied diet allows them to thrive in a wide range of freshwater and marine environments but is also dangerous.Chemical contaminants from industrial runoff, agricultural pesticides, and urban waste can accumulate in otter habitats and prey species.Otters are vulnerable to the bioaccumulation of toxins through their diet.Contaminants accumulated in prey species can concentrate in otter tissues, leading to health and reproductive problems.Monitoring otter health can provide insights into the presence and impact of environmental toxins [10,23,58].
Oil spills are a significant threat to otters and their habitats, as described in two studies from the United Kingdom and the USA [24,59].These incidents, unfortunately common, primarily endanger otters due to the toxic effects of oil on the animals and their environment.The consequences of oil spills include fur matting, which impairs otters' ability to regulate body temperature, and the ingestion of toxins, leading to internal damage.Additionally, habitat contamination from oil spills reduces prey availability, impacting the otter population [24].Even when the visible signs of oil have dissipated, the lingering effects can persist in otter habitats for years.Chronic exposure to residual oil and its associated contaminants can lead to long-term declines in otter populations' health and reproductive success [24,60,61].
Historically, otters have been hunted for various reasons, including the fur trade, traditional medicine, meat, and superstitions [61].Countries where otter hunting may be allowed or permitted under specific circumstances include Alaska (USDA), Canada, Siberia (Russia), Norway, Estonia, Sweden, and Latvia [61].In the present study, hunting was described in the Czech Republic, Germany, Hungary, and the USA (n = 4) [3,30,48].It is possible that in most cases it was illegal hunting, since except for the USA no other countries permit otter hunting.It is important to note that hunting otters for fur or other purposes has led to population declines and conservation concerns for many otter species worldwide [60].Today, the hunting of otters is often regulated or prohibited by laws and regulations aimed at protecting these animals from overexploitation and ensuring their conservation and welfare [14].
In 11 cases, the exact cause of death could not be determined, highlighting the challenges in conducting a post mortem analysis of wildlife.This examination requires experience, a standardised methodology, and extensive anatomical, physiological, and pathological knowledge.Additionally, it should be performed as early as possible.Often, access to the body is delayed, and putrefactive phenomena complicate the interpretation of macroscopic observations and hinder histopathological examination, resulting in the loss of valuable data.In many cases, wildlife carcasses are not readily accessible or may go undiscovered, particularly in remote or inaccessible areas.Species such as Pteronura brasiliensis live in the depths of the Amazonas (Brazil), which can be one of the reasons for the almost non-existent mortality descriptions due to the difficulty in retrieving the carcasses [54].
Nevertheless, post mortem examination serves as a crucial instrument in wildlife medicine and conservation, offering valuable insights into the health status of individual animals and broader information about the population and ecosystem [57,62].The identification of mortality causes could uncover human activities' effects on ecosystems and wildlife populations and identify the most significant anthropogenic pressures within a particular region or on a specific species.By providing essential information on the challenges wildlife faces, this examination can guide conservation strategies aimed at reducing the impact of human actions on natural habitats [48,63].
On the one hand, necropsy enables the collection of samples for further examinations, such as histopathology, microbiology, and toxicology, allowing for an etiological diagnosis beyond a morphological one [43,48].
The geographical distribution of studies on otter mortality demonstrates the global interest in researching otter mortality, with notable contributions from North America and Europe.While less pronounced, participation from countries on other continents indicates a global acknowledgement of the significance of otter conservation.The diverse locations of these studies mirror the wide ecological range of otters and highlight the universal demand for data on their mortality to devise effective conservation strategies.

Conclusions
Post mortem analyses provide valuable data to assess the conservation status of threatened mammals such as otters and the efficacy of conservation measures.Based on the data supplied from the review and the post mortem findings, humans may play a significant role in the mortality of these animals.Post mortem examinations are valuable in wildlife conservation as they provide critical information about the health, threats, and challenges facing wildlife populations.This knowledge informs conservation strategies, helps prevent disease outbreaks, and contributes to ecosystems' overall well-being and sustainability.In the future, it will be necessary to implement an efficient system of collection and examination of otter carcasses.This network will help us understand the main threats to otter populations and develop more efficient measures to protect these already threatened species.In the future, conservation efforts focused on habitat protection and restoration, pollution control, sustainable fisheries management, and reducing human disturbances are essential for mitigating otter declines and ensuring the long-term survival of these charismatic and ecologically important mammals.Collaboration between governments, conservation organizations, local communities, and stakeholders is crucial for implementing effective conservation strategies to address the complex challenges facing otter populations worldwide.

Figure 1 .
Figure 1.Distribution of mortality studies worldwide by otter species (author: Andreia Garc

Table 1 .
Distribution of the causes of mortality among otters across the different countries, de the total number of animals (N) reported in the papers.

Table 1 .
Distribution of the causes of mortality among otters across the different countries, detailing the total number of animals (N) reported in the papers.