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Systematic Review

A Systematic Review of Global Marine Mammal Rehabilitation and Refloating, 2000–2023

by
Claire A. Simeone
1,*,
Estelle Rousselet
2,
Cathrine Atkin
3,
Mélodie De Trez
1,
Margot Delemotte
1 and
Shawn P. Johnson
1
1
Sea Change Health, Sunnyvale, CA 94086, USA
2
Wildlife Conservation Insights, 41700 Cour-Cheverny, France
3
Sea World Foundation, Gold Coast, QLD 4217, Australia
*
Author to whom correspondence should be addressed.
Sustainability 2024, 16(11), 4589; https://doi.org/10.3390/su16114589
Submission received: 15 April 2024 / Revised: 17 May 2024 / Accepted: 18 May 2024 / Published: 28 May 2024
(This article belongs to the Section Sustainable Oceans)
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Abstract

:
Rehabilitation of marine mammals is performed throughout the world, yet the impact of rehabilitation on individuals and populations is questionable given the lack of robust information on the rehabilitation process and post-release monitoring in most cases. The goals of this study were to perform a systematic review of existing literature on marine mammal rehabilitation between 2000–2023 to determine the current state of rehabilitation and to evaluate the rehabilitation and conservation factors that could be used to build a framework to assess the health of rehabilitation programs worldwide. A total of 418 publications encompassing 52 species of marine mammal were included in the systematic review. Rehabilitation efforts focused mostly on pinnipeds, and North America was the most represented region. Data are scarce for both short- and long-term post-release survival across species. Reports about species threatened with extinction were significantly more likely to include information about conservation parameters than those species of least concern. A meta-analysis demonstrated a fairly strong fit of the dimensions of the proposed framework for a rehabilitation health index. Further refinement would strengthen the utility of this tool for both rehabilitation and conservation programs.

1. Introduction

Rehabilitation of sick and injured marine mammals is performed to varying degrees throughout the world. It is defined as an attempt to return an animal to a state of health that allows for survival in the wild [1]. Concerns about the risks of rehabilitation to wild populations are well-documented [2,3,4], and the impact rehabilitated animals have in contributing positively to those populations is questionable given the lack of robust post-release information in most cases. For certain endangered species such as southern sea otters (Enhydra lutris nereis) and Hawaiian monk seals (Neomonachus schauinslandii), rehabilitation is utilized as a research component in comprehensive conservation programs [5,6]. This often involves collaboration with multiple stakeholders and close adherence to recovery plans. Apart from select cases, recommendations have been made for rehabilitators to enhance post-release monitoring, set wider objectives beyond release, and take steps to assess programs [7,8,9].
Without a proper evaluation system to assess the success and sustainability of rehabilitation programs, these programs risk being ineffective at best and detrimental at worst. Public health practitioners use health indices to measure health outcomes [10]. Inequities are unsustainable, and a broad variety of factors must be addressed and assessed when working toward equity [11]. Rehabilitation programs can be evaluated by (a) the factors that impact the individual animal during the rehabilitation process, such as the reason for stranding or admittance into rehabilitation, or the type of medical treatment given while in care; (b) the factors that impact the individual after its release, namely short- and long-term survival; (c) the factors that impact the population as a whole, such as epidemiology or population trends; (d) and the ability of a program to contribute to general conservation goals, such as conservation policy adherence or public awareness and engagement (Table 1). The goals of this study were to perform a systematic review of existing literature on global marine mammal rehabilitation to determine the current state of rehabilitation and to evaluate the rehabilitation and conservation factors that could be used to build a framework for assessing the health of rehabilitation programs worldwide.

2. Materials and Methods

A standard systematic search strategy was used to identify peer-reviewed and grey literature published between 2000 and 2023 reporting marine mammal rehabilitation around the world. All species of marine mammals were included (pinnipeds, cetaceans, sirenians, sea otters, and polar bears). Search results were recorded using a Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) flow diagram (Figure 1). Online databases Scopus and Web of Science were searched, along with relevant conference proceedings, reference lists of selected articles (reverse search), and Google Scholar. The literature search was completed by CS, ER, CA, MDT, MDLM, and SJ over a four-month period from December 2023 to March 2024. Search terms were related to the taxa (common and scientific names), rescue, rehabilitation or refloating, and location. Full manuscripts were reviewed against the following selection criteria: research was conducted on marine mammal species listed by the Taxonomy Committee of the Society of Marine Mammalogy that were stranded and determined to require intervention and entered rehabilitative care for any reason. Rapid in situ procedures such as beach disentanglement of pinnipeds were excluded; however, triage associated with cetacean refloating—returning a beach-cast animal to the sea—or mass stranding efforts were included if at least partial data was included about the management of the case.

2.1. Statistical Analyses

Definition of Variables

“Publication” refers to each unique published manuscript, and each publication was counted only once for the total publication count. Some publications included investigations of multiple species or pertained to multiple regions. These papers were counted separately when comparing different species or regions and are differentiated in the results as “reports”. As an example, one single publication may investigate both California sea lions (Zalophus californianus) and harbor seals (Phoca vitulina), while the report on California sea lions and the report on harbor seals were included separately in the statistical analysis. The region was assigned based on the geographical location of the rehabilitation in the relevant papers, as the natural and extralimital range of many marine mammals is not restricted to a single region.
The parameters were categorized into three groups, namely individual animal, population, and general conservation parameters. Individual animal parameters were divided into those encountered during rehabilitation, which included “rehabilitation numbers”, “cause of stranding”, “medicine”, “nutrition”, “welfare/enrichment”, “euthanasia”, and “cause of death”; and those encountered post-release, including “short-term survival” (<6 months) and “long-term survival” (>6 months). Population parameters included “epidemiology”, “research and monitoring”, and “population trends”. General conservation parameters included “conservation policy adherence”, “genetic diversity”, “habitat quality”, “threat assessment”, “public awareness and engagement”, “collaboration and partnerships”, and “climate change resilience”. Publications were reviewed for information relating to each category, and classified as either data if specific data were included in the publication, discussion only if the parameter was discussed but no specific data were included, or no if no data or discussion were found for the parameter.
Statistical methods. Statistical analyses were performed in jamovi [13]. A Chi-square test of independence and heat maps were performed for each parameter.
For the meta-analysis, a Principle Components Analysis (PCA) was used to reduce the parameters to a set of orthogonal variables (principle components; PC). All PC scores were saved as regression scores for components with eigenvalues > 1.

3. Results

A total of 418 publications were included (Supplementary Materials). Fifty-two species were included in the research, of which 18 were classified according to the 2023 IUCN Red List as critically endangered, endangered, vulnerable, or near threatened; the remaining 34 species were listed as least concern or data-deficient [14] (Table S1). Relevant publications documenting rehabilitation of the remaining 81 extant species listed by the Society of Marine Mammalogy [15] were not encountered in this review.
Eighteen publications included data that spanned multiple taxa or regions, so a total of 436 reports were included in the analysis. The reports that were most frequent concerned the rehabilitation of California sea lions (n = 113) and harbor seals (n = 112). Rehabilitation in the majority of other marine mammal species was not well represented in the literature within the timeframe of the review, with 38 species represented in fewer than 5 publications, and 20 of those species represented in only a single publication. Findings from the most frequently rehabilitated species from each taxon are reported below.

3.1. Taxa

3.1.1. Pinnipeds

Rehabilitation efforts focused mostly on pinnipeds, comprising 75% of reports (Table 2).

Otariids

Reports of California sea lions in rehabilitation were more numerous in the literature than those of any other species (n = 113). This is most likely due to the intense effort of rehabilitation of this species, particularly in California. In recent decades, this species has suffered numerous Unusual Mortality Events (UMEs), with increasing incidences of domoic acid toxicosis [16] and a prevalence of urogenital carcinoma [17]. These diseases and mortality processes have contributed to high numbers of strandings and rehabilitation admissions.
Rehabilitation of the northern fur seal (Callorhinus ursinus) was referred to in 16 reports during the study period. Much of the extensive range of the northern fur seal across the North Pacific occurs along coastlines with low human population densities [18,19]. Almost all studies were from North America, where this species is frequently admitted to rehabilitation centers. There was a single report on northern fur seal rehabilitation in the northwest Pacific, which discussed the rescue and treatment of four individuals in South Korea over a 10-year period [20]. Similarly, in Japan, individual fur seals have been rescued and placed in permanent care [21].
Rehabilitation of endangered otariids included the Galápagos fur seal (Arctocephalus galapagoensis) and Galápagos sea lion (Zalophus wollebaeki). Four of the five reports on the rehabilitation of these species reported on extra-limital occurrences of single individuals [22,23,24,25]. While the Galápagos species are vulnerable to climatic changes and anthropogenic activity, including entanglement in fishing gear and refuse, oil spills, and introduced pathogens, rehabilitation efforts currently appear to be limited to in situ responses [26]. Despite its endangered status, there was only one report on the rehabilitation of the endemic Australian sea lion (Neophoca cinerea) [27]. The species inhabits a vast area of largely unpopulated coastline from South to Western Australia [28], and rehabilitation efforts are only conducted on a small scale.

Phocids

A total of 176 reports focused on phocids in rehabilitation, including harbor seals (Phoca vitulina, both Atlantic and Pacific, n = 78), northern elephant seals (Mirounga angustirostris, n = 33); or both species together (n = 16). Other phocids studied included grey seals (Halichoerus grypus, n = 11); harp seals (Pagophilus groenlandicus; n = 4); spotted seals (Phoca largha; n = 1), grey and harbor seals together (n = 16) or reports including several phocid species such as harbor, elephant seal, harp, and hooded seals (Cystophora cristata) (n = 5). Publications focusing on endangered species included Caspian seals (Pusa capsica, n = 3) [29,30,31], Mediterranean monk seals (Monachus monachus) (n = 3) [32,33,34], and Hawaiian monk seals (Neomonachus schauinslandi) (n = 9) [35,36,37].
One hundred and twenty phocid reports originated from North America, including the North Atlantic coast of California and Vancouver, Canada. One report studied morbillivirus in a rehabilitated Mediterranean monk seal found in West Africa, three reports were from Asia (Caspian and spotted seals), and 53 reports were from Europe, primarily from the Netherlands.
Most phocid reports focused on infectious diseases (n = 59), with viral diseases, including phocid herpesvirus 1, phocine distemper virus, and avian influenza, studied in harbor seals and the elephant seal. Diagnostic (n = 24) research reports focusing mostly on clinical pathology, non-infectious diseases (n = 17), and physiology research (n = 18) were then the most frequent, including both individual and population research. Reports aiming at conservation strategies (n = 15; 8% of phocid literature) focusing on endangered species were published. Studies on toxicology (n = 13) assessed contaminant levels and health effects of organochlorine and mercury. Finally, reports focused on medical treatment (n = 13), such as pharmacokinetics studies, and behavior (n = 7), including diving movement and enrichment preferences, were published.

Walrus

One publication was included in the study detailing an unsuccessful capture attempt for rehabilitation and the subsequent euthanasia of a walrus in Europe.

3.1.2. Cetaceans

This systematic review encompassed 33 reports on cetacean rehabilitation cases and 17 on refloating or relocation cases, with 23 odontocete species and only 1 mysticete species represented.
Distinct from other taxa, the majority of reports of cetacean rehabilitation (n = 22; 67%) provided robust detail on the rescue, rehabilitation, or post-release monitoring of cetaceans. In contrast, only 25% (n = 4) of refloating cases provided data and descriptions of the process. These reports frequently involved the first live rescue or rehabilitation attempt published for the species, such as the endangered Ganges river dolphin (Platanista gangetica) and the East Asian finless porpoise (Neophocaena phocaenoides sunameri), or involved a mass stranding event and subsequent monitoring, as with long-finned pilot whales (Globicephala melas) and rough-toothed dolphins (Steno bredanensis).
Both in rehabilitated and refloated cases, pathogens were frequently the subject of discussions on disease dynamics or prevalence in free-ranging populations, particularly if the presenting disease was an emerging pathogen, zoonosis, or of anthropogenic origin. Pathogens of interest included Brucella spp. [38], Aeromonas dhakensis [39], and Robiensoniella peroniensis with the probable origin from river contamination from swine farms in China [40]. Staphylococcus aureus has been reported as potentially shared with human stranding responders [41]. Toxoplasma gondii [42], Giardia spp. [43], Nasitrema spp. [44], and morbillivirus were also among the pathogens reported. Anthropogenic activities were a cause of death or stranding of cetaceans. Documented cases included vessel collisions resulting in severe injuries [45], microplastic ingestion inducing gastrointestinal obstruction [46], or fisheries interactions. Other anthropogenic causes of strandings are discussed in some articles, such as hearing loss induced by noise pollution or immune perturbation caused by chemical pollution, such as PCBs. Rare cases of congenital abnormalities were described in two P. phocoena, including hemihydranenphaly and a ventricular septal defect, observed for the first time in cetaceans [47,48]. Then, notably for river or estuarine dolphins, local threats are discussed, such as river pollution, accidental capture, hunting, river drying during the dry season, and the presence of dams [49,50,51].
Some studies delved into the hearing capabilities of cetaceans, which is a unique and crucial sense for these animals. Assessing hearing influences their ability to survive, interact normally with their environment, exhibit efficient predatory behavior, and engage in normal socialization behavior. These reports also explored environmental noise in rehabilitation pools [52].

3.1.3. Sea Otters

A total of 40 reports focused on endangered sea otters in rehabilitation, with 34 reports focused on the southern sea otter subspecies (Enhydra lutris nereis) and 8 focused on northern sea otters (Enhydra lutris kenyoni). No publications were found for the rehabilitation of the western sea otter (Enhydra lutris lutris).
Reports focused on the diverse threats and unique conservation challenges facing the species. Eighteen reports focused on major infectious and non-infectious causes of morbidity and mortality that affect sea otters, such as protozoal disease from Toxoplasma and Sarcocystis, cardiac disease, and both natural and anthropogenic trauma [53,54]. Five reports focused on oil spill response and preparedness, given the historical impact of the Exxon Valdez oil spill on northern sea otters and the risk of future oil spills on otters [55].
Six reports focused on conservation strategies employed by programs focused on species recovery, including surrogate rearing methods and rehabilitating live-stranded otters [56,57,58].

3.1.4. Sirenians

This study included 17 reports on sirenian rehabilitation cases. The majority of reports (n =13) focus on the Antillean manatee (Trichechus manatus manatus), Florida manatee (Trichechus manatus latirostris), and Amazonian manatee (Trichechus inunguis). There was limited documentation on the dugong (Dugong dugong) and no reports on the African manatee (Trichechus senegalensis).
While the total number of publications was comparatively small in contrast with other taxa, five reports focused on long-term datasets of several decades of sirenian stranding, rehabilitation, and post-release monitoring [59,60]. Several reports also discussed details of the rehabilitation process, such as hand-rearing and milk replacement formulas [61,62].

3.1.5. Polar Bears

No publications were located that met the criteria for inclusion in the study that would enable assessment of the sustainability of any rehabilitation project.

3.2. Conservation Status

Data on other conservation parameters, including climate change resilience, conservation policy adherence, genetic diversity, habitat quality, public awareness and engagement, and threat assessment were infrequently reported, with each conservation parameter included in fewer than 7% of reports.
Reports about species threatened with extinction (listed either as critically endangered, endangered, threatened, or near threatened) were significantly more likely to include information about population trends (p < 0.0001), genetic diversity (p < 0.0001), habitat quality (p < 0.0001), threat assessment (p < 0.0001), conservation policy adherence (p < 0.0001), and public awareness and engagement (p < 0.0001). No significant differences were observed for epidemiology (p = 0.28), research and monitoring (p = 0.16), collaboration and partnerships (p = 0.9), and climate change resilience (p = 0.07).

3.3. Region

Rehabilitation efforts for marine mammals were reported on every continent except for Antarctica (Figure 2). North America was the most represented region among the marine mammal rehabilitation reports identified (p < 0.001), with 71% (n = 303) originating in the region. The abundance of reports on the rehabilitation of California sea lions, harbor seals, and northern elephant seals contributed to the dominance of North America among published reports (Table 2).
Reports from Europe were dominated by phocid rehabilitation in the Netherlands and, to a lesser extent, individual cetacean cases.
South America was the most represented region for sirenian rehabilitation reports. It was also the only region with an included report involving a mysticete [63]. Otariids and a variety of odontocete species are distributed along the Pacific and Atlantic coasts of South America, and rehabilitation is occasionally reported for these species in this region.
Reports from Asia were predominately focused on single odontocete strandings [45]. Three reports focused on the unusual mortality event involving endangered Caspian seals [29,30,34].
Reports of rehabilitation in the Australia/Oceania region were scarce (n = 13). All reports on rehabilitated otariids and odontocetes in the region were from Australian facilities. The majority of reports were of endemic individuals within their normal range. Extralimital subantarctic fur seals (Arctocephalus tropicalis) were rehabilitated in small numbers [64].
Reports originating from Africa were limited to Cape fur seals (Arctocephalus pusillus pusillus) in South Africa [65] and a report on a Mediterranean monk seal on the Atlantic coast of West Africa [66].

3.4. Rehabilitation Parameters

Reports most frequently reported data about stranding and rehabilitation numbers, with 70% (n = 301) of all reports including these data and 41% (n = 176) sharing data on the causes of stranding. Sirenian reports frequently included rehabilitation datasets over several decades, while in comparison only 20% (n = 30) of otariid reports included periodic data over a 1-year period or longer, while the rest reported on smaller subsets of the population of animals entering rehabilitation. Although 32% (n = 49) of otariid reports presented research on between 1 and 10 individuals, in some cases, this did represent the total number of rehabilitation admissions for a given region or time period [64]. Many of the reports involving 10 or fewer cases described vagrant individuals who were stranded beyond their normal distribution [67], while others discussed unusual or novel pathological findings [68,69]. Cetacean reports most frequently described one or few individuals, and the data on these stranding events were typically comprehensive, and in cases of mass stranding events, the outcome for each animal was indicated (rehabilitation, refloating attempt, euthanasia) [70,71].
Data on topics occurring while animals were in rehabilitation varied across taxa, likely due in part to the varied approaches used to rehabilitate different species. Data on rehabilitation were reported in particular detail when unique or novel techniques were used, such as surrogacy programs or point-of-care diagnostic tests [57,72]. Gaps in data reporting, particularly about nutrition, welfare, and enrichment, were observed. Nutrition during the rehabilitation process exhibited heterogeneity among different articles. Twenty-five % of reports included nutrition information. Most of these gave few details on the nature of the food provided or the feeding method used. A subset of reports, particularly in cases of neonate or young cetaceans and sirenians, did describe a comprehensive nutrition plan (e.g., whole fish, squid, mash, milk formula, supplements), providing extensive details during the rehabilitation process [61]. Welfare was indirectly assessed in several studies [73,74], however in most cases, welfare discussions were limited to brief statements regarding the physical or social environment, the effects of stress during rehabilitation, or the reasons for euthanasia [27]. The impact of environmental enrichment to enhance welfare during rehabilitation was also reported in three species including northern elephant seals, California sea lions, and harbor seals [75,76].
Sparse data on euthanasia were included in 11% (n = 48) of reports. Methods employed to conduct euthanasia were included in several reports [77]. A small number of reports provided data on the length of time in care prior to euthanasia.
Discussion of medical protocols and data were included in 44% (n = 190) of reports. Most reports focused on clinical pathology, treatment during infectious or non-infectious disease, or advanced diagnostics.
All of the individual animal rehabilitation parameters evaluated were statistically different when combining data and data found in discussion only (p > 0.05), except for medicine, cause of death, euthanasia, and nutrition (Table 3).
Data on short-term and long-term survival after rehabilitation were statistically different (p < 0.05). Short-term survival data were included in 14% of reports (n = 58), and data on long-term survival were included in 6% (n = 26).
Parameters assessing general science included epidemiology and disease dynamics (for which data were reported in 50%), science research and monitoring (data reported in 48%), and collaboration and partnerships (data reported in 50%). There were no statistical differences (p = 0.9) between these parameters when compared to whether data or information in discussion was present or not.
Population-wide parameters included epidemiology and disease dynamics, scientific research and monitoring, population trends, and genetic diversity. No statistical differences existed between epidemiology (49% of papers with data or discussion) and science (48%) when compared to whether data or information in discussion was present or not (p = 0.67). There were statistical differences between population trends (18%), genetic diversity (5%), and the above-mentioned parameters (p < 0.05).

3.5. Meta-Analysis

Data were utilized from 428 reports representing 418 unique manuscripts published between 2000 and 2023. The PCA variable reduction was summarized into five orthogonal PCs (Table 4) explaining 53.8% of the cumulative variance (Table 5). For PC 1, population trends, habitat quality, threat assessment, conservation policy adherence, public awareness and engagement, collaboration and partnerships, and climate change resilience, all loaded positively. For PC 2, genetic diversity and short- and long-term survival loaded positively. For PC 3, termed Individual Health Parameter-1, stranding/rehabilitation numbers and causes of stranding, medicine, nutrition, and welfare loaded positively. For PC 4, termed Individual Health Parameter-2, euthanasia, cause of death, and life history loaded positively. Finally, for PC 5, termed General Science, epidemiology and research/monitoring loaded positively.
Correlations exist between PC 1 and 2 (0.479), PC 1 and 5 (0.440), and PC 2 and 5 (0.426).

4. Discussion

The scope of this review provides a global view of marine mammal rehabilitation efforts over more than two decades, although notable exceptions were excluded, given the search parameters. For sea otters, reports about the southern sea otter were more frequent than northern sea otters, although excluding research prior to 2000 meant excluding literature from rehabilitated northern sea otters following the Exxon Valdez oil spill [78]. Critics of marine mammal rehabilitation frequently cite the inordinately high cost of rehabilitating oiled otters during this oil spill as a sign of its ineffectiveness, reported as more than $80,000 per otter [79]. Supporters of rehabilitation highlight that these cited costs often include capital costs over a single use, while models in some areas have shifted towards multipurpose facilities that can be used for a variety of rehabilitative efforts over decades and note that oiled wildlife rehabilitation is complementary to, and not a substitute for, wildlife restoration [80].
Ex situ conservation efforts, such as that of the vaquita (Phocoena sinus) [81], were also excluded in this study as the individuals handled briefly during that effort were technically not stranded or in need of rehabilitation, although the species itself could be accurately described as in need of rehabilitation [82].
While this review does capture rehabilitation efforts throughout the world, the published literature does not accurately reflect the total rehabilitative efforts, of which some remain unpublished. Some regions, such as North America, had a strong focus on scientific data across most parameters in contrast to others, where rehabilitation is known to occur but data are not published. For example, although many pinnipeds are rehabilitated in France each year, peer-reviewed literature was nonexistent in this review. Also, despite multiple facilities in Australia and New Zealand treating stranded and rescued otariids, publications in this review originated only from Australian facilities.
The limited literature on rehabilitation efforts for the African manatee may be attributed to the species’ endangered status, small population size, and the challenging political and social context of its geographic distribution. Similarly, the scarcity of data on the dugong can be explained by the few observed individuals in recent years and the ineffective enforcement of conservation regulations in many regions due to poverty, lack of resources, and personnel constraints, all of which have the ability to impact rehabilitation priorities across regions; otherwise, as above, rehabilitation efforts may yet go unpublished.
For this study, the refloating or mass stranding response of cetaceans was included in the search criteria, even though best practices of rehabilitation of marine mammals do not include these triage procedures where release follows immediately [83]. Given the lack of logistical capabilities for cetacean rehabilitation in many regions and the infrequent nature of these events, the data gained from this handful of reports was seen as a valuable addition, although the definition of rehabilitation—when an animal is transported to a secondary location for temporary care—traditionally excludes these cases.
While a determination of non-releasability and transition into permanent managed care is a viable outcome of rehabilitation, papers were excluded if the animals were in permanent care at the time of the research and the data did not pertain to their time in rehabilitation. For species such as walruses or polar bears, this led to few to zero records being included for review. Most walrus strandings are typically young calves that have been separated from their mother, who are extremely underweight and sick. Because of their extended period of maternal dependency, the U.S. Fish and Wildlife Service generally considers walrus calves to be non-releasable and considers all stranded walruses on a case-by-case basis for permanent placement [83]. Sub-adult and adult walruses are generally not suitable candidates for rehabilitation because of their large size, aggressive nature, difficulty to physically and chemically immobilize, and lack of specialized facilities suitable for extended care. The most likely course of action for an injured sub-adult or adult walrus is euthanasia [84]. With the rapid decline of arctic sea ice and loss of habitat for arctic species, the need for improved walrus rescue and rehabilitation techniques and policies must be evaluated. Walruses and other marine mammals that are currently deemed non-releasable and held in long-term care should be further studied to help refine rescue and rehabilitation techniques and to improve knowledge of marine mammal health.
Concerns about rehabilitation may influence regulations regionally. In Alaska, USA, the government has a policy of not returning rescued arctic pinnipeds to the wild due to concerns of introducing new diseases into the wild populations that are used by local populations for subsistence [4]. Similarly, the Scientific Committee on Antarctic Research (SCAR) 1997 recommendations discourage the release of rehabilitated Antarctic and Subantarctic seals, due to the potential threat of introduction of disease to free-ranging populations [85]. In an investigation of the pathology of rehabilitating fur seals, the authors reported the in situ treatment of a Subantarctic fur seal, in compliance with the SCAR recommendations [86]. Rehabilitated animals have the potential to become vectors of disease to wild populations, and treatments during rehabilitation can alter pathogens. Other reports included in this study demonstrated that sea otters with a history of rehabilitation were more likely to be infested with nasal mites than those without a rehabilitation history [87] and reported on a novel serotype of Salmonella in elephant seals in rehabilitation [88], highlighting the potential risks both to wild populations and potential zoonotic risk to humans. At the same time, rehabilitation facilities that perform robust science have the opportunity to identify novel pathogens or investigate the epidemiology of known pathogens [89].
Post-rehabilitation survival was not widely reported, despite its value as a measure of rehabilitation success [3]. A lack of resources has been identified in rehabilitation facilities as a hindrance to conducting post-release monitoring [9]. Restranding could be used as an index of short-term survival post-rehabilitation; however, restranding data is rarely quantified in the literature. While restranding may be an indicator of an individual’s physical or behavioral inadequacies or decline following rehabilitation, it may also reflect an element of the natural environment that is impacting fitness, or the cause may differ to that of the original stranding event. Restranding data could therefore be a useful tool for assessing the health of rehabilitation programs and highlighting environmental challenges to survival.
The challenges of measuring long-term survival (>6 months) of rehabilitated marine mammals most likely have contributed to the paucity of published studies on this aspect of rehabilitation. The duration of monitoring of otariids post-rehabilitation, beyond 12 months, is often limited by the technique and technology. Paint markings on the pelage and tracking devices attached to the fur will be lost due to the annual molt in most species [90]. Branding or natural markings, combined with resighting or photographic and video surveillance, have been used to determine survival in many species, but these techniques usually require significant research effort and are only valuable in species with high site fidelity. Flipper tags are relatively inexpensive compared to satellite tags but are prone to loss or may become unreadable over time [91]. The recent development and application of intra-peritoneal tags have the potential to greatly extend the period of post-release monitoring from months to years [92].
The post-release phase is described in some rehabilitated cetacean cases using different types of tagging: satellite-linked transmitters or radio-tracking transmitters attached to the dorsal fin. For cetaceans, studies estimate the minimal time required to define a successful rehabilitated case as 6 weeks. This period allows for the observation of potential re-acclimatization into the wild, particularly concerning diving patterns, travel rates, social behavior patterns, and foraging behavior patterns. Monitoring with satellite tags allows for the improvement of current knowledge, notably on the diurnal cycle of dive patterns and ocean area preferences according to species. To evaluate the real impact of rehabilitation on conservation, a long-term study over several years is required, which exceeds the length of current tag lives. This can be organized through surveys and studies of wild populations, photo identification and genetic sampling campaigns, whale-watching activities, sighting observation of individuals, and, in the case of females, monitoring whether they give birth [63,93,94].
The reasons to undertake rehabilitation are diverse and vary by species, country, and region. Definitions of rehabilitation success also vary among stakeholders, ranging from an individual animal’s release into the wild, to long-term survival and successful reproduction, to contributing to the successful recovery of a species. Indeed, supporters of rehabilitation may point to the potential positive impact rehabilitated animals could have on a population. For example, an analysis indicated that up to 24% of the 2012 population of endangered Hawaiian monk seals was comprised of seals or descendants of seals saved by small-scale interventions such as dehookings and disentanglements; when rehabilitation efforts were included in the analysis, the proportion increased to 32% [5]. For the southern sea otter, intensive rehabilitation efforts focused on a surrogate program increased the population in Elkhorn Slough from 20 individuals to nearly 150 in less than 15 years, with 55% of the overall population growth attributed to surrogate-reared animals and their offspring [57]. Over four decades of coordinated rehabilitation efforts for the Florida manatee resulted in more than 500 rehabilitated animals being released back to the wild; that, combined with other conservation efforts, contributed to the subspecies downlisting from endangered to threatened under the US Endangered Species Act [95].
The knowledge and experience gained while rehabilitating non-threatened species can help support the care of similar, endangered species. Regardless of the reason rehabilitation is undertaken, critics argue that evidence-based, species-specific, and context-specific protocols are frequently lacking, particularly in post-release monitoring and analysis of the population and ecosystem impacts of release [56,96]. This study found similar gaps, and ongoing development of strengthened protocols supported by science is key to ensuring survival after release and successful integration into the wild population.
Contribution to conservation is not always a primary goal for marine mammal rehabilitation, but this study showed that there was a significantly greater focus on conservation parameters such as conservation policy adherence, public awareness and engagement, and threat assessment for those studies focused on species threatened with extinction when compared with species of least concern. This disparity can be attributed to the endangered status of these species, and the fact that rehabilitation of high-profile endangered species is often one prong in a multifaceted conservation program that typically features multi-agency stakeholders, public-private partnerships, and robust scientific evaluation. Conversely, this study showed no significant difference in the inclusion of discussion of parameters such as epidemiology, research and monitoring, or collaboration between publications focused on threatened and endangered species versus those of least concern. This suggests that these more general scientific topics are existing priorities for many rehabilitation programs: for instance, the strength of collaborations is essential to the logistical operations associated with marine mammal rehabilitation and is vital to ensuring limited resources are efficiently and sustainably utilized. This study confirms that research is a tool that is utilized in many rehabilitation facilities to improve the care of rehabilitated animals or better understand the species. Where a gap exists, and rehabilitative efforts are not being published, there is an opportunity for rehabilitation programs to contribute meaningfully to the scientific process.
The meta-analysis of this study demonstrated a fairly strong fit of the dimensions in the proposed framework for a rehabilitation health index, divided into individual animal parameters both during and post-rehabilitation, population-wide parameters, and conservation parameters (Table 1). The principal component analysis suggested that further refining these categories may strengthen the utility of this tool (Table 6). Instead of “during rehabilitation” and “post rehabilitation”, individual animal parameters were split into live and dead animal parameters. Population-level parameters were subdivided into those focused on an individual animal’s impact on the population and broader population-level impacts. This is reflected in the fact that rehabilitation programs may be likely to focus on the parameters in one of these dimensions, with certain programs having excellence in medicine or nutrition, while others might focus on necropsy and causes of death.
Nearly universally, parameters in the conservation dimension were the least reported. Publications occasionally discussed these conservation parameters, but actual data were lacking. Additionally, there was a nearly complete absence of collaboration between regions. There is an opportunity for rehabilitation programs to both develop data collection on conservation parameters and build broader, global collaboration.
Given the desire for robust, evidence-based rehabilitation protocols across taxa, rehabilitators can emulate the comprehensive conservation programs that incorporate rehabilitation as part of their strategies. Assessing rehabilitation programs and the data strengths and gaps that exist for parameters during rehabilitation, post-release, and associated with larger population-wide impacts and human-social factors allows rehabilitation programs to work to close the gap between conservation goals and actual impact. Health indices are tools that measure a broad variety of health factors to compare the health of large groups or organizations and have been implemented for public health, global health, and ocean health [10,97,98]. There is a need to identify evidence-based priorities for both research and conservation needs across marine mammal taxa [99]. The development of a standardized conservation health index, a tool that could provide objective measures of the ability of a program to effectively perform its work, could benefit both rehabilitation programs and all stakeholders working towards species conservation.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/su16114589/s1, Table S1: Species featured in publications included in systematic review. Table S2: Complete dataset of publications included in systematic review. Figure S1: PRISMA Checklist. Figure S2: Statistical analysis. References [100,101,102,103,104,105,106] are citied in the Supplementary Materials.

Author Contributions

Conceptualization, C.A.S.; methodology, C.A.S.; validation, C.A.S. and S.P.J.; formal analysis, C.A.S. and E.R.; investigation, C.A.S., E.R., C.A., M.D.T., M.D. and S.P.J.; data curation, C.A.S., E.R., C.A., M.D.T., M.D. and S.P.J.; writing—original draft preparation, C.A.S.; writing—review and editing, C.A.S., E.R., C.A., M.D.T., M.D. and S.P.J.; visualization, C.A.S., E.R. and M.D.; supervision, C.A.S.; project administration, C.A.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Complete dataset of publications included in the systematic review can be found in Supplementary Materials.

Acknowledgments

The authors acknowledge the tireless efforts of stranding responders and rehabilitation providers globally to document and make freely available the data included in this analysis. Additionally, the authors thank the anonymous reviewers for their constructive feedback, which strengthened the manuscript.

Conflicts of Interest

Authors Claire A. Simeone, Mélodie De Trez, Margot Delemotte and Shawn P. Johnson was employed by the company Sea Change Health. Author Estelle Rousselet was employed by the company Wildlife Conservation Insights. Author Cathrine Atkin was employed by the company Sea World Foundation. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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Sustainability 16 04589 g001
Figure 1. PRISMA flow diagram of systematic search strategy and results [12].
Figure 1. PRISMA flow diagram of systematic search strategy and results [12].
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Sustainability 16 04589 g002
Figure 2. Proportion of reports on marine mammal rehabilitation for each taxon and global region where rehabilitation was performed. Symbol sizes represent the total number of reports that originated from that region, which ranged from 2 reports from Africa to 307 reports from North America.
Figure 2. Proportion of reports on marine mammal rehabilitation for each taxon and global region where rehabilitation was performed. Symbol sizes represent the total number of reports that originated from that region, which ranged from 2 reports from Africa to 307 reports from North America.
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Table 1. Proposed health dimensions that contribute to the robust assessment of a marine mammal rehabilitation program.
Table 1. Proposed health dimensions that contribute to the robust assessment of a marine mammal rehabilitation program.
Individual Animal DimensionPopulation DimensionConservation Dimension
During RehabilitationPost-Rehabilitation
Stranding/rehabilitation numbersShort-term survivalEpidemiologyConservation policy adherence
Causes of strandingLong-term survivalScience and researchPublic awareness and engagement
Medicine Population trendsCollaboration and partnerships
Nutrition Genetic diversityClimate change resilience
Welfare and enrichment Habitat quality
Euthanasia Threat assessment
Cause of death
Life history
Table 2. Number of reports of marine mammal rehabilitation from each region, listed by taxon.
Table 2. Number of reports of marine mammal rehabilitation from each region, listed by taxon.
# of SpeciesReports by RegionTotal
Reports *
AfricaAsiaAustralia/
Oceania		EuropeNorth AmericaSouth America
CetaceansOdontocetes2301041116849 (11.2)
Mysticetes10000011 (0.2)
PinnipedsOtariids13119012813152 (34.9)
Phocids10130531190176 (40.4)
Walrus10001001 (0.2)
SireniansManatee, Dugong3020041117 (3.9)
MustelidsSea Otters1000040040 (9.2)
UrsidsPolar Bears00000000 (0)
Grand Total *522 (0.5)16 (3.7)13 (3.0)65 (15.4)307 (70.4)33 (7.6)436 (100)
* Values presented as total (percentage of total).
Table 3. Frequencies table of individual animal rehabilitation parameters. A value of “0” represents no data or discussion of the parameter in reports, while a value of “1” represents data or discussion included in the report.
Table 3. Frequencies table of individual animal rehabilitation parameters. A value of “0” represents no data or discussion of the parameter in reports, while a value of “1” represents data or discussion included in the report.
VariableValueProportion (%)
01
Causes of Death27416237.16
Causes of Stranding16427262.39
Euthanasia3508619.72
Medicine24619043.58
Nutrition32810824.77
Stranding & Rehab Numbers7735982.34
Table 4. Principal component analysis for five rehabilitation categories obtained from 428 reports on marine mammal rehabilitation.
Table 4. Principal component analysis for five rehabilitation categories obtained from 428 reports on marine mammal rehabilitation.
Component LoadingsComponentUniqueness
12345
Stranding and Rehab Numbers 0.464 0.725
Causes of Stranding 0.720 0.427
Medicine 0.697 0.449
Nutrition 0.619 0.564
Welfare 0.719 0.470
Euthanasia 0.733 0.519
Cause of Death 0.824 0.354
Life History 0.420 0.634
Short-term Survival 0.942 0.296
Long-term Survival 0.925 0.300
Epidemiology −0.440 0.8860.336
Research and Monitoring −0.3490.7490.391
Population Trends0.314 0.495
Genetic Diversity 0.573 0.588
Habitat Quality0.3110.392 0.439
Threat Assessment0.450 0.364
Conservation Policy Adherence0.896 0.373
Public Awareness and Engagement0.837 0.350
Collaboration and Partnerships0.815 0.452
Climate Change Resilience0.513 −0.321 0.706
Table 5. Eigenvalues and the variance explained for extracted principal component scores for five rehabilitation categories obtained from 428 reports on marine mammal rehabilitation.
Table 5. Eigenvalues and the variance explained for extracted principal component scores for five rehabilitation categories obtained from 428 reports on marine mammal rehabilitation.
ComponentEigenvalue% of VarianceCumulative %
14.37221.8621.9
22.20511.0232.9
31.6368.1841.1
41.3446.7247.8
51.2126.0653.8
60.9884.9458.8
70.9744.8763.7
80.8834.4168.1
90.7983.9972.1
100.7283.6475.7
110.6713.3579.1
120.6353.1882.2
130.5792.9085.1
140.5292.6587.8
150.5072.5490.3
160.4992.5092.8
170.4442.2295.0
180.3851.9397.0
190.3361.6898.6
200.2741.37100.0
Table 6. Revised health dimensions that contribute to the robust assessment of a marine mammal rehabilitation program, based on principal component analysis of the systematic review of 428 marine mammal rehabilitation reports.
Table 6. Revised health dimensions that contribute to the robust assessment of a marine mammal rehabilitation program, based on principal component analysis of the systematic review of 428 marine mammal rehabilitation reports.
Individual Animal DimensionPopulation DimensionConservation Dimension
Live AnimalDead Animal/HistoricalIndividual Impact on PopulationPopulation-Level Impact
Stranding/rehabilitation numbersEuthanasiaShort-term survivalEpidemiologyPopulation trends
Causes of strandingCause of deathLong-term survivalScience and researchThreat assessment
MedicineLife historyGenetic diversity Conservation policy adherence
Nutrition Habitat quality Public awareness and engagement
Welfare and enrichment Collaboration and partnerships
Climate change resilience
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Simeone, C.A.; Rousselet, E.; Atkin, C.; De Trez, M.; Delemotte, M.; Johnson, S.P. A Systematic Review of Global Marine Mammal Rehabilitation and Refloating, 2000–2023. Sustainability 2024, 16, 4589. https://doi.org/10.3390/su16114589

AMA Style

Simeone CA, Rousselet E, Atkin C, De Trez M, Delemotte M, Johnson SP. A Systematic Review of Global Marine Mammal Rehabilitation and Refloating, 2000–2023. Sustainability. 2024; 16(11):4589. https://doi.org/10.3390/su16114589

Chicago/Turabian Style

Simeone, Claire A., Estelle Rousselet, Cathrine Atkin, Mélodie De Trez, Margot Delemotte, and Shawn P. Johnson. 2024. "A Systematic Review of Global Marine Mammal Rehabilitation and Refloating, 2000–2023" Sustainability 16, no. 11: 4589. https://doi.org/10.3390/su16114589

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