Marine Mammals as Sentinel Species for Oceans and Human Health
TL;DR: The long-term consequences of climate change and potential environmental degradation are likely to include aspects of disease emergence in marine plants and animals, and the concept of marine sentinel organisms provides one approach to evaluating aquatic ecosystem health.
Abstract: The long-term consequences of climate change and potential environmental degradation are likely to include aspects of disease emergence in marine plants and animals. In turn, these emerging diseases may have epizootic potential, zoonotic implications, and a complex pathogenesis involving other cofactors such as anthropogenic contaminant burden, genetics, and immunologic dysfunction. The concept of marine sentinel organisms provides one approach to evaluating aquatic ecosystem health. Such sentinels are barometers for current or potential negative impacts on individual- and population-level animal health. In turn, using marine sentinels permits better characterization and management of impacts that ultimately affect animal and human health associated with the oceans. Marine mammals are prime sentinel species because many species have long life spans, are long-term coastal residents, feed at a high trophic level, and have unique fat stores that can serve as depots for anthropogenic toxins. Marine mammals may be exposed to environmental stressors such as chemical pollutants, harmful algal biotoxins, and emerging or resurging pathogens. Since many marine mammal species share the coastal environment with humans and consume the same food, they also may serve as effective sentinels for public health problems. Finally, marine mammals are charismatic megafauna that typically stimulate an exaggerated human behavioral response and are thus more likely to be observed.
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University of Montpellier1, University of La Réunion2, Claude Bernard University Lyon 13, Cheikh Anta Diop University4, Institut de recherche pour le développement5, Centre national de la recherche scientifique6, Institut Universitaire de France7, IFREMER8, University of Western Brittany9, University of Lyon10, University of Strasbourg11
TL;DR: It is discussed how crucial it is to consider ecological, evolutionary, and environmental sciences in understanding the emergence and re-emergence of infectious diseases and in facing the challenges of antimicrobial resistance.
Abstract: Over the past decade, a significant increase in the circulation of infectious agents was observed. With the spread and emergence of epizootics, zoonoses, and epidemics, the risks of pandemics became more and more critical. Human and animal health has also been threatened by antimicrobial resistance, environmental pollution, and the development of multifactorial and chronic diseases. This highlighted the increasing globalization of health risks and the importance of the human-animal-ecosystem interface in the evolution and emergence of pathogens. A better knowledge of causes and consequences of certain human activities, lifestyles, and behaviors in ecosystems is crucial for a rigorous interpretation of disease dynamics and to drive public policies. As a global good, health security must be understood on a global scale and from a global and crosscutting perspective, integrating human health, animal health, plant health, ecosystems health, and biodiversity. In this study, we discuss how crucial it is to consider ecological, evolutionary, and environmental sciences in understanding the emergence and re-emergence of infectious diseases and in facing the challenges of antimicrobial resistance. We also discuss the application of the "One Health" concept to non-communicable chronic diseases linked to exposure to multiple stresses, including toxic stress, and new lifestyles. Finally, we draw up a list of barriers that need removing and the ambitions that we must nurture for the effective application of the "One Health" concept. We conclude that the success of this One Health concept now requires breaking down the interdisciplinary barriers that still separate human and veterinary medicine from ecological, evolutionary, and environmental sciences. The development of integrative approaches should be promoted by linking the study of factors underlying stress responses to their consequences on ecosystem functioning and evolution. This knowledge is required for the development of novel control strategies inspired by environmental mechanisms leading to desired equilibrium and dynamics in healthy ecosystems and must provide in the near future a framework for more integrated operational initiatives.
346 citations
TL;DR: A possible relationship was found between the cause of death category and microplastic abundance, indicating that animals that died due to infectious diseases had a slightly higher number of particles than those that died of trauma and other drivers of mortality.
Abstract: Plastic pollution represents a pervasive and increasing threat to marine ecosystems worldwide and there is a need to better understand the extent to which microplastics (<5 mm) are ingested by high trophic-level taxa, such as marine mammals. Here, we perform a comprehensive assessment by examining whole digestive tracts of 50 individuals from 10 species whilst operating strict contamination controls. Microplastics were ubiquitous with particles detected in every animal examined. The relatively low number per animal (mean = 5.5) suggests these particles are transitory. Stomachs, however, were found to contain a greater number than intestines, indicating a potential site of temporary retention. The majority of particles were fibres (84%) while the remaining 16% was fragments. Particles were mainly blue and black (42.5% and 26.4%) in colour and Nylon was the most prevalent (60%) polymer type. A possible relationship was found between the cause of death category and microplastic abundance, indicating that animals that died due to infectious diseases had a slightly higher number of particles than those that died of trauma and other drivers of mortality. It is not possible, however, to draw any firm conclusions on the potential biological significance of this observation and further research is required to better understand the potential chronic effects of microplastic exposure on animal health, particularly as marine mammals are widely considered important sentinels for the implications of pollution for the marine environment.
226 citations
TL;DR: There was sufficient evidence supporting an association between developmental PBDE exposure and reduced IQ, and the body of evidence was of “moderate” quality for ADHD with “limited” evidence for an association with PBDEs.
Abstract: Background: In the United States, one in six children are affected by neurodevelopmental disorders, and polybrominated diphenyl ethers (PBDEs) in flame-retardant chemicals are measured ubiquitously...
224 citations
TL;DR: A number of marine top predator species have been proposed as sentinel species to provide information about unobserved components of the ecosystem (Zacharias and Roff 2001).
Abstract: I an era of unprecedented environmental change, developing a suite of tools for ecosystem monitoring is critical. This need is particularly urgent in marine ecosystems, given the rapid, climatedriven changes in marine populations and communities (Poloczanska et al. 2013). Comprehensive monitoring in marine ecosystems presents a challenge due to difficulties inherent in observing the highly dynamic ocean environment at relevant timescales. Traditional shipbased surveys are expensive, autonomous floats and underwater vehicles are still sparsely distributed, and remote sensing fails to capture threedimensional ocean structure. Furthermore, ecological monitoring in the open ocean is largely extractive and often involves lethal sampling of animal communities. In the undersampled marine realm, innovative and costeffective tools that can rapidly assess ecosystem responses to environmental change are vital. “Sentinel” species have been proposed as a means to provide information about unobserved components of the ecosystem (Zacharias and Roff 2001). Classic examples of sentinels include a domesticated variety of the canary (Serinus canaria), which was formerly used to monitor air quality in coal mines, and invertebrates, whose diversity has been used as an indicator of aquatic ecosystem health (Wilhm and Dorris 1968; Barry 2013). More recent studies show that vertebrate species can serve as sentinels of human health and environmental pollution (Bossart 2006; Smits and Fernie 2013), as well as coupled climate–ecosystem processes (Moore 2008). Useful sentinel species should integrate broader processes into rapidly interpretable metrics that reflect underlying ecosystem processes. Marine top predators (including certain species of predatory fish, seabirds, sea turtles, and marine mammals) have been proposed as ecosystem sentinels based on their conspicuous nature and capacity to indicate or respond to changes in ecosystem structure and function that would otherwise be difficult to observe directly (Figure 1; Bossart 2006; Boersma 2008; Moore 2008). Many marine top predators possess key characteristics of sentinel species, including (1) exhibiting clear responses to environmental variability or change (Sydeman et al. 2015; Fleming et al. 2016), (2) playing important roles in shaping marine food webs (Estes et al. 2016), and (3) indicating anthropogenic impacts on ecosystems (Sergio et al. 2008). Given these characteristics, there is a strong argument for using marine predators as ecosystem sentinels. Despite the contemporary use of marine predators as sentinels (relevant examples are listed in WebTable 1), the absence of a standardized framework for identifying sentinel Marine top predators as climate and ecosystem sentinels
162 citations
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TL;DR: This review explores the nature of marine animal-microbiome relationships and interactions, and possible factors that may shift associations from symbiotic to dissociated states, and a brief review of current microbiome research and opportunities.
Abstract: All animals on Earth form associations with microorganisms, including protists, bacteria, archaea, fungi, and viruses. In the ocean, animal-microbial relationships have historically been explored in single host-symbiont systems. However, new explorations into the diversity of microorganisms associating with diverse marine animal hosts is moving the field into studies that address interactions between the animal host and a more diverse microbiome. The potential for microbiomes to influence the health, physiology, behavior and ecology of marine animals could alter current understandings of how marine animals adapt to change, and especially the growing climate-related and anthropogenic-induced changes already impacting the ocean environment. This review explores the nature of marine animal-microbiome relationships and interactions, and possible factors that may shift associations from symbiotic to dissociated states. I present a brief review of current microbiome research and opportunities, using examples of select marine animals that span diverse phyla within the Animalia, including systems that are more and less developed for symbiosis research, including two represented in my own research program. Lastly, I consider challenges and emerging solutions for moving these and other study systems into a more detailed understanding of host-microbiome interactions within a changing ocean.
143 citations
Cites background from "Marine Mammals as Sentinel Species ..."
...Marine mammals are often viewed as sentinel species of the ocean, because they appear to rapidly respond to ocean conditions, disturbances, and pathogens similarly to humans (Bossart, 2011)....
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TL;DR: It is concluded that global resources to counter disease emergence are poorly allocated, with the majority of the scientific and surveillance effort focused on countries from where the next important EID is least likely to originate.
Abstract: Emerging infectious diseases (EIDs) are a significant burden on global economies and public health. Their emergence is thought to be driven largely by socio-economic, environmental and ecological factors, but no comparative study has explicitly analysed these linkages to understand global temporal and spatial patterns of EIDs. Here we analyse a database of 335 EID 'events' (origins of EIDs) between 1940 and 2004, and demonstrate non-random global patterns. EID events have risen significantly over time after controlling for reporting bias, with their peak incidence (in the 1980s) concomitant with the HIV pandemic. EID events are dominated by zoonoses (60.3% of EIDs): the majority of these (71.8%) originate in wildlife (for example, severe acute respiratory virus, Ebola virus), and are increasing significantly over time. We find that 54.3% of EID events are caused by bacteria or rickettsia, reflecting a large number of drug-resistant microbes in our database. Our results confirm that EID origins are significantly correlated with socio-economic, environmental and ecological factors, and provide a basis for identifying regions where new EIDs are most likely to originate (emerging disease 'hotspots'). They also reveal a substantial risk of wildlife zoonotic and vector-borne EIDs originating at lower latitudes where reporting effort is low. We conclude that global resources to counter disease emergence are poorly allocated, with the majority of the scientific and surveillance effort focused on countries from where the next important EID is least likely to originate.
5,992 citations
"Marine Mammals as Sentinel Species ..." refers background in this paper
...Ultimately, it is in our own best interest to investigate all wildlife health patterns that could potentially affect our own well-being since three-fourths of all emerging infectious diseases of humans are zoonotic, most originate in wildlife, and their incidence is increasing.(114,145,192,218)...
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TL;DR: This study represents the first quantitative analysis identifying risk factors for human disease emergence, with protozoa and viruses particularly likely to emerge, and helminths particularly unlikely to do so, irrespective of their zoonotic status.
Abstract: A comprehensive literature review identifies 1415 species of infectious organism known to be pathogenic to humans, including 217 viruses and prions, 538 bacteria and rickettsia, 307 fungi, 66 protozoa and 287 helminths. Out of these, 868 (61%) are zoonotic, that is, they can be transmitted between humans and animals, and 175 pathogenic species are associated with diseases considered to be 'emerging'. We test the hypothesis that zoonotic pathogens are more likely to be associated with emerging diseases than non-emerging ones. Out of the emerging pathogens, 132 (75%) are zoonotic, and overall, zoonotic pathogens are twice as likely to be associated with emerging diseases than non-zoonotic pathogens. However, the result varies among taxa, with protozoa and viruses particularly likely to emerge, and helminths particularly unlikely to do so, irrespective of their zoonotic status. No association between transmission route and emergence was found. This study represents the first quantitative analysis identifying risk factors for human disease emergence.
2,331 citations
TL;DR: An overview of the recent advances in the toxicology and mode of action for PFAAs, and of the monitoring data now available for the environment, wildlife, and humans is provided.
2,175 citations
"Marine Mammals as Sentinel Species ..." refers background in this paper
...In toxicology testing in laboratory species, convincing evidence exists for the toxicopathologic effects of many of these contaminants on endocrine, neurologic, reproductive, developmental, immunologic, and cellular systems.(13,41,45,53,67,79,104,125,126,170,193,229) Beluga whales (Delphinapterus leucas) from the St....
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TL;DR: The completion of the genome sequence of Leptospira interrogans serovar lai, and other continuing leptospiral genome sequencing projects, promise to guide future work on the disease.
Abstract: In the past decade, leptospirosis has emerged as a globally important infectious disease. It occurs in urban environments of industrialised and developing countries, as well as in rural regions worldwide. Mortality remains significant, related both to delays in diagnosis due to lack of infrastructure and adequate clinical suspicion, and to other poorly understood reasons that may include inherent pathogenicity of some leptospiral strains or genetically determined host immunopathological responses. Pulmonary haemorrhage is recognised increasingly as a major, often lethal, manifestation of leptospirosis, the pathogenesis of which remains unclear. The completion of the genome sequence of Leptospira interrogans serovar lai, and other continuing leptospiral genome sequencing projects, promise to guide future work on the disease. Mainstays of treatment are still tetracyclines and beta-lactam/cephalosporins. No vaccine is available. Prevention is largely dependent on sanitation measures that may be difficult to implement, especially in developing countries.
2,055 citations
"Marine Mammals as Sentinel Species ..." refers background in this paper
...Leptospirosis is a zoonotic disease infecting a broad range of mammalian hosts and is reemerging globally.(12) California sea lions (Zalophus californianus) have experienced recurrent outbreaks of leptospirosis since 1970, and the infection is thought to be enzootic....
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