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date: 19 September 2017

Sentinel Species of Marine Ecosystems

Summary and Keywords

A vigorous effort to identify and study sentinel species of marine ecosystem in the world’s oceans has developed over the past 50 years. The One Health concept recognizes that the health of humans is connected to the health of animals and the environment. Species ranging from invertebrate to large marine vertebrates have acted as “sentinels” of the exposure to environmental stressors and health impacts on the environment that may also affect human health. Sentinel species can signal warnings, at different levels, about the potential impacts on a specific ecosystem. These warnings can help manage the abiotic and anthropogenic stressors (e.g., climate change, chemical and microbial pollutants, marine litter) affecting ecosystems, biota, and human health.

The effects of exposure to multiple stressors, including pollutants, in the marine environment may be seen at multiple trophic levels of the ecosystem. Attention has focused on the large marine vertebrates, for several reasons. In the past, the use of large marine vertebrates in monitoring and assessing the marine ecosystem has been criticized. The fact that these species are pelagic and highly mobile has led to the suggestion that they are not useful indicators or sentinel species. In recent years, however, an alternative view has emerged: when we have a sufficient understanding of differences in species distribution and behavior in space and time, these species can be extremely valuable sentinels of environmental quality.

Knowledge of the status of large vertebrate populations is crucial for understanding the health of the ecosystem and instigating mitigation measures for the conservation of large vertebrates. For example, it is well known that the various cetacean species exhibit different home ranges and occupy different habitats. This knowledge can be used in “hot spot” areas, such as the Mediterranean Basin, where different species can serve as sentinels of marine environmental quality. Organisms that have relatively long life spans (such as cetaceans) allow for the study of chronic diseases, including reproductive alterations, abnormalities in growth and development, and cancer. As apex predators, marine mammals feed at or near the top of the food chain. As the result of biomagnification, the levels of anthropogenic contaminants found in the tissues of top predators and long-living species are typically high. Finally, the application of consistent examination procedures and biochemical, immunological, and microbiological techniques, combined with pathological examination and behavioral analysis, has led to the development of health assessment methods at the individual and population levels in wild marine mammals. With these tools in hand, investigators have begun to explore and understand the relationships between exposures to environmental stressors and a range of disease end points in sentinel species (ranging from invertebrates to marine mammals) as an indicator of ecosystem health and a harbinger of human health and well-being.

Keywords: sentinel species, One Health, biomonitoring, large marine vertebrate, marine mammals, anthropogenic contaminants, infectious diseases, climate change, biomarkers, human health

Introduction

The Origin and Evolution of the Sentinel Species Concept

Over the past 50 years, marine environmental research has focused on the identification of appropriate sentinel species of marine ecosystems in the world’s oceans and seas. The suitability and effectiveness of a sentinel species rely on the level of the investigation, the information that needs to be obtained, and the magnitude of the environmental stressor. “Bioindicator species” (a broader definition of sentinel species) were first defined in the 1980s as organisms or sets of organisms that enable the characterization of the state of an ecosystem and offer an early indication of its natural or provoked changes. Later, the definition shifted to “biological indicator of pollution” and “organisms which reveal the presence or absence of environmental conditions that cannot be revealed in other species or in the environment as a whole” (Blandin, 1986; O’Brien et al., 1993). Bioindicator species are organisms that can indicate the health of an environment or ecosystem by identifiable biochemical, physiological, and/or behavioral changes, and can provide information on the quality of the marine environment and human health (Lower & Kendall, 1990). “Sentinel species” were then defined as bioindicators with early alarm signals. The concept of sentinel species has been historically aligned with the concept of “the canary in the coal mine” as an early warning signal of exposure to environmental risk; dangerous gases in a mine would kill the canary before humans, thus providing a warning signal to abandon the mine.

Sentinel species can provide an early warning on the single or, more often, the cumulative effects of different environmental stressors and the extent to which these stressors can affect ecosystems and human health (Van der Schalie et al., 1999). In this regard, sentinel species can serve as sensitive indicators owing to their ability to integrate all responses to an exposure in an ecosystem (in particular in the trophic chain).

Organisms at the top level of the food chain (e.g., marine mammals and migratory birds), which constitute the lowest biomass but require a wide home range, can be considered as integrators of medium and large scales (Fossi et al., 2012). Marine organisms are at the same taxonomic level of mammals and, therefore, share similar physiology, pathology, diet (e.g., seafood consumers), and environment with humans. They may indicate the potential noxious effects on health at an early stage and may unravel the mechanisms of action of diverse environmental stressors (Schwacke et al., 2013). As part of the same ecosystem as humans, top marine predators and, in particular, marine mammals, are exposed to the same environmental changes on a global scale. Therefore, they are considered to be prime sentinels owing to their trophic position, long life span, and substantial ability to accumulate contaminants and become targets of emerging disease and algal toxin blooms. The use of sentinel species as “integrators” of the multiple stressors in the marine ecosystem is essential in establishing the definition of fitness for individuals, populations, and communities, since the simple measurement of threshold levels, for instance, of chemical contaminants, are difficult to establish for each species and do not reflect the overall health status of organisms and their ecosystems.

More recently, acknowledgment of the importance of the seas and oceans and the close connections among ecosystems, animals, and human health has led to the development of the One Ocean-One Health concept used as a paradigm to drive multidisciplinary research and encourage interdisciplinary collaborations (e.g., biologists, ecotoxicologists, veterinarians, and physicians). The One Health concept recognizes that human health is connected to the health of animals and the environment. The U.S. National Oceanographic and Atmospheric Administration (NOAA) Science Advisory Board Report (2010) stated: “The concept of the combined health of people and wildlife—one health—when combined with the concept of the ocean as an essential modulator/caregiver of all life on Earth, inexorably leads to the prime tenet that the health of the ‘one ocean’ is essential to the ‘one health’ of all life on earth, including that of humans.”

To accomplish the One Health concept and to underline the need to identify appropriate sentinel species as indicators of ocean and human health, it is also essential to apply integrated monitoring tools to sentinel species that can properly identify diagnostic and prognostic marker responses.

Characteristics of a Sentinel Species

Some of the most important functions of a sentinel species are its use in monitoring the health of aquatic environments to provide early warning signals of environmental deterioration; identify biological responses to multiple environmental stressors; and assess the integrated responses of the organisms to environmental perturbations.

To determine what constitutes a good marine sentinel species, a series of criteria need to be defined. A sentinel species must be sensitive to environmental changes (e.g., chemical contamination, pathogens, biotoxins) and should accumulate the stressors in its tissues. It must have broad distribution in the area relevant to the agents of concern and the spatial scale to be analyzed. Its physiology, anatomy, and ecology should be well understood in order to identify any physiological signal that is not caused by exposure to the environmental stressors. Finally, it must have a key trophic and ecological role in its habitat so that it can provide relevant information, including a spatial and trophic niche.

Under the sentinel species concept and approach, several studies have been initiated around the world. One of the most representative studies is the Mussel Watch Program, which was initiated in 1976 (Goldberg et al., 1978) by the U.S. Environmental Protection Agency (EPA) and later taken over by NOAA in 1986 to monitor chemical contamination of bodies of waters (both oceans and lakes) in the United States. Over the years, the International Mussel Watch Program has been developed worldwide to measure the biological effects of pollution, from legacy persistent chemical to emerging issues (e.g., pharmaceuticals, nanoparticles). As with mussels, several fish species have been studied as sentinel species since the 1960s.

Although in recent decades many investigations have focused on the study of sentinel species for monitoring and risk assessment purposes, particularly with regard to chemical contaminants in marine environment, this topic is still scientifically challenging and debated because of the complex interactions of multiple stressors and their ecological consequences (Moore et al., 2004). For example, Bowen and Depledge (2006a) proposed a Rapid Assessment for Marine Pollution (RAMP), where sentinel species would serve as the integrators of pollution, evaluating diagnostic and laboratory-based tests and biomarkers with direct observation and contaminants analysis. This approach could provide assessment of health status at a range of scales, from individual to community and population, based on relatively small samples. This approach can also have a prognostic effect in evaluating long-term effects and can be used by policymakers for future mitigation activities.

In recent years, with the development of molecular biology techniques and the “omic” sciences (e.g., genomics, transcriptomics, proteomics, metabolomics), many species of invertebrates and fish can be useful models to study the effects of one or more compounds (e.g., DDTs, PBDEs, PFCs) or the mixture of environmental stressors (e.g., water temperature alterations, salinity, UV exposure, algal blooms) both in laboratory exposure studies and in the wild (Allen & Moore, 2004; Cossins & Crawford, 2005; Sedeño-Díaz & López-López, 2012).

Although the use of marine invertebrates and model fish species has a fundamental importance in monitoring programs, studying organisms at higher evolutionary levels (i.e., phylogenetically closer to humans) and with a broader home ranges may offer greater integration of the marine environment, enlarge the spatial and temporal scale, and offer a higher sensitivity.

Biomarkers in Sentinel Species

The concept of biomarkers represents an evolution of biomonitoring methodologies using sentinel species. Use of the biomarker approach in marine sentinel species to evaluate pollution hazards has noticeably increased in the past few decades, attracting the attention of international regulatory agencies as a powerful tool for detecting exposure to and the effects of environmental contamination. While various definitions of biomarkers have been proposed, we use the following broad definition: “taking into account all biological fluids, cells or tissues, a biomarker could be defined as any measurable molecular, biochemical, cellular variation in response to the presence and effect of one or more contaminants” (Depledge & Fossi, 1994; Livingstone et al., 2000). The methodological approach of biomarkers stems from this concept: the interactions between living organisms and contaminants can cause variations or damages at different biological levels of the individual, from the molecular to the cellular level, eventually affecting population viability and ecosystems. The organism reacts to environmental stressors with responses that can decrease the toxic effects of the compounds or induce endogenous systems that can amplify the effects of that stressor or stressors.

In the assessment of the ecotoxicological hazard, biomarkers were applied as powerful tools to indicate exposure to pollutants in several marine ecosystems (Bowen & Depledge, 2006b; Depledge et al., 1993; Rice, 2003). A wide spectrum of biomarkers have been evaluated in several sentinel marine species; in each case study, these methods of investigation were able to obtain reliable data in biomonitoring and risk-assessment studies (Dagnino et al., 2007; Galloway, 2006; Owen et al., 2008).

Biomarkers should provide information on the health status of both individuals and populations, but when it comes to evaluating eco-toxicological risk, complex issues are involved and a wide variety of factors should be considered. Biomarkers are a very important component of a “weight-of-evidence” approach in which the induction of biomarker response is suggestive of the presence of one or more known and/or unknown environmental stressors. Biomarker responses also integrate the impact of all the stressors, including natural stressors, that affect an organism, giving a more realistic scenario of the status of species in their environment. Different biomarker responses include the signals of metabolic toxicity, genotoxicity, immunotoxicity, disruption of endocrine systems, behavioral disturbance, and altered scope for growth and reproduction. Detection of any of these signals is a warning sign, even if it is not possible to establish accurate dose-response relationships for individual or mixtures of stressors. Conversely, the absence of biomarker signals of a stressor or pollution is compelling evidence of progress toward attaining good ecological status (although some allowance has to be made for the appearance of general “stress markers” that might signal periods of stress associated with natural seasonal cycles).

The sentinel species of marine ecosystems are subdivided here into two main categories: (1) sensitive indicators of marine ecosystems that can concentrate and integrate the exposure to marine pollutants within the food chain or ecosystem; and (2) sentinel organisms that can provide an early indication of the adverse effects on human health and ecosystems, owing to their physiology and diet similar to humans (Schwacke et al., 2013).

Sensitive Indicators of Marine Ecosystems

The species described here are characterized by differences in home range, spatial distribution, and trophic level (Figure 1); for example, highly mobile species are seen as sentinels of pelagic environments and less mobile invertebrate species as sentinels of coastal environments.

Sentinel Species of Marine EcosystemsClick to view larger

Figure 1. Sensitive indicators of marine ecosystems at different home range (circles) and trophic level.

Invertebrates as Sentinels of the Coastal Environment

The biomarker approach in invertebrates for assessment of the toxicological effects of contaminants in the coastal environment was increasingly used in the 1990s for environmental hazard assessment. There are several reasons why invertebrates are preferable for ecotoxicological risk assessment in marine ecosystems. Invertebrates constitute 95% of all animal species, they are major components of all ecosystems, and their populations are often numerous, so that samples can be taken for analysis without significantly affecting population dynamics. Increasing knowledge of the biochemistry of invertebrates since the early 1990s allowed for the reasonable interpretation of biomarker responses in terms of ecological risk assessment (Depledge & Fossi, 1994).

After the success of the Mussel Watch Program in monitoring not only the concentration of contaminants in bivalves but also mussel health and, by extension, the health of their local and regional environment, several papers proposed the use of crabs as sentinel species of the coastal environment (Pie et al., 2015; Rodrigues et al., 2014; Rodrigues & Pardal, 2014). Fossi and collaborators in 2000 proposed a multitrial biomarker approach for evaluating toxicological risk due to polyaromatic hydrocarbons (PAHs) and particularly benzo(a)pyrene in the Mediterranean coastal environment. This multitrial approach, evaluating direct biological responses ranging from genetic to physiological alterations, was essential to determine the general health status of the sentinel organism. Moreover, it permitted the exploration of the relationship between responses at different levels of biological organization. The bioindicator organism chosen for this study was a benthic crustacean with low motility, the crab Carcinus aestuarii. The use of this sentinel species was successful in different Mediterranean estuarine scenarios related to different anthropogenic impacts, such as B(a)P, methylmercury (MeHg) and polychlorinated biphenyls (PCBs), both in experimentally exposed crabs and in the field (Fossi et al., 1998, 2000). Later, crabs were used as a model species in several studies and for many biomonitoring purposes, including the risk assessment of emerging contaminants (Rodrigues & Pardal, 2014). Because of their low motility and home range, polychaetes and several mussel species were also used as sentinels of the coastal environment.

Large Marine Vertebrates as Sentinels of the Pelagic Marine Environment

The effects of exposure to multiple stress and pollutants in the marine environment may be expressed at multiple trophic levels of the ecosystem; however, attention has focused recently on large marine vertebrates (including large pelagic fish, reptiles, birds and marine mammals). In the past, the use of large marine vertebrates in marine ecosystem monitoring and assessment has been criticized. The fact that these species are pelagic and highly mobile has led to the suggestion that they are not useful indicator or sentinel species. In recent years, however, an alternative view has emerged: with sufficient understanding of differences in species distribution and behavior in space and time, these species can be extremely valuable sentinels of overall environmental quality.

Knowing the status of large vertebrate populations is crucial to understanding ecosystem health and instigating measures for their conservation (Fossi et al., 2012). For example, it is well known that the various cetacean species exhibit different home ranges and occupy different habitats. The species that have relatively long life spans allow for the study of chronic diseases. As the result of biomagnification, the levels of anthropogenic contaminants found in the tissues of top predators and long-living species are typically high. As well as signaling many legacy environmental pollutants such as mercury, DDT, PCBs, and dioxins, large marine vertebrates can provide early warnings of newly emerging contaminants such as perfluorinated compounds, nanomaterials, and microplastics (Fossi & Depledge, 2014). The bodily burdens of environmental pollutants in the European and U.S. human populations is a growing cause for concern and may be associated with alterations in the frequency of occurrence of a range of diseases, including neurological disorders, cancers, diabetes, and cardiovascular disease (Lang et al., 2008; Melzer et al., 2010). Almost all the contaminants thought to be of concern in large marine vertebrates are also of concern to human health (Schwacke et al., 2013). Therefore, the relationship between the degree of chemical contamination and the health of large marine vertebrates is of great relevance to contaminant-related human diseases.

Large Pelagic Fish as Sentinels of Endocrine-Disrupting Chemicals

Endocrine disrupting chemicals (EDCs) are a structurally diverse group of compounds that may adversely affect the health of humans, wildlife, and fisheries, and/or their progenies, by interactions with the endocrine system (Colborn et al., 1993; Gillesby & Zacharewski, 1998). These include chemicals used heavily in the past in industry and agriculture, such as PCBs and organochlorine pesticides, as well as chemicals that are currently used, such as plasticizers and surfactants. Many of the known EDCs are estrogenic, particularly affecting reproductive functions. Because of the lipophilic and persistent nature of most xenobiotic estrogens and their metabolites, many bioaccumulate and biomagnify (Colborn et al., 1993; Matthiessen, 2003).

Contamination by human-made EDCs ranges across all continents and oceans. Some geographic areas, such as the Mediterranean Sea, are potentially more threatened than others. The Mediterranean Basin has limited exchange of water with the Atlantic Ocean and is surrounded by some of the most heavily populated and industrialized countries in the world. Levels of some xenobiotics are therefore much higher there than in other seas and oceans (Aguilar et al., 2002); therefore, the Mediterranean marine fauna are exposed to and can accumulate large concentrations of EDCs. For instance, the levels of organochlorines in a top predator of the Mediterranean, the striped dolphin (Stenella coeruleoalba), are one to two orders of magnitude higher than in Atlantic and Pacific dolphins of the same species (Borrell & Aguilar, 2005).

The potential estrogenic effects of PAHs was investigated in Mediterranean top predators, focusing on gender differences in biochemical responses and contaminant bioaccumulation (Fossi et al., 2001, 2007). Sensitive biomarkers were used, such as Vitellogenin (Vtg) and Zona Radiata proteins (Zrp), for the evaluation of toxicological risks due to EDCs in one of the top predator fish species: the swordfish (Xiphias gladius). Induction of vitellogenin and zona radiata protein transcription and translation is a well-established major response to estrogens in fish (Arukwe & Goksøyr, 2003). Swordfish is a large migratory fish found worldwide in temperate and tropical waters, which grows reasonably fast and matures quickly. The swordfish in the Mediterranean Sea is thought to have been overfished, with the population becoming less abundant. The fishery industry traditionally catches many juveniles and prereproductive fish, which is a major cause of concern for population stability.

The significant introduction of these typically female proteins was detected by enzyme-linked immunosorbent assay (ELISA) and western blot in adult males in a 10-year survey of the Mediterranean swordfish population. Several male Mediterranean swordfish specimens showed values of Zrp and Vtg protein, which were higher than male average values and/or in the same range as those of reproductive females; this finding suggests that this species is exposed to xenoestrogens in the Mediterranean Sea. Interestingly, an increasing induction of Vtg in male specimens was related to the aging of the fish analyzed, confirming the bioaccumulation of persistent organic pollutants (POPs) with ED potency during the aging process (age/PCBs liver—p = 0.0002; age/DDTs liver—p = 0.009) (Figure 2). Moreover, Vtg and Zrp were induced in the Mediterranean adult males in comparison with the Atlantic ones.

Sentinel Species of Marine EcosystemsClick to view larger

Figure 2. Trend of Vtg in male specimens of swordfish in relation to the increasing of age (Class A: 0–2 years, Class B: 3–5 years, Class C: 6–9 years, Class D: more than 9 years, according to the Von Bertalanffy growth factor).

An interesting temporal trend was highlighted during a 10-year survey of the Mediterranean population. A reduction in blood levels of Zrp was found in the male specimens from 1999 to 2009, suggesting a decrease of EDCs in the basin. These findings indicate that this species is a potential temporal and regional sentinel of the health status of the entire basin with respect to contamination by EDCs (Figure 3), in addition to confirming the benefits of monitoring for evaluating the health of the swordfish fishery.

Sentinel Species of Marine EcosystemsClick to view larger

Figure 3. Levels of Zrp in male specimens of swordfish (Xiphias gladius) in relation to the temporal trend.

The final outcomes of this study confirm that top predator pelagic fish can be considered a sentinel of the impacts of the EDCs in highly impacted semi-enclosed sea basins on long-term scales and, because of their role in the diet of humans, can provide a warning of the impacts of these EDC compounds on the food chain.

Seabirds and Sea Turtles as Indicators of Marine Litter Ingestion

Anthropogenic marine litter is pervading the ocean surface, coastal environments, and the seafloor and has increased over the last century. Marine litter and the products deriving from the breakdown processes can travel long distances from one region to another, even reaching remote areas. Marine litter, and in particular the accumulation of plastic debris, has been identified as a global problem, alongside other key issues such as climate change, ocean acidification, and loss of biodiversity. During the 2015 G7 Science Ministers meeting (in Germany, October 2015), marine litter was acknowledged as a global risk to marine and coastal life ecosystems and, potentially, to human health.

According to ocean-based sources (such as shipping, fishing, and maritime activities) and land-based sources (such as tourism, ocean-adjacent industries, and river inputs), these plastics are entering our seas and oceans, “posing a complex and multi-dimensional challenge with significant implications for the marine and coastal environment and human activities all over the world” (UNEP, 2009). In particular, the occurrence of microplastics (generally defined as fragments less than 5 mm in dimension) in seas and oceans is an emerging worldwide concern. Because of the high sorption capacity of plastics for hydrophobic organic chemicals, the adherent chemicals can also be transported by microplastics which function as carriers, traveling long distances in marine ecosystems (Lee et al., 2013). In addition, small plastic particles in the environment are of particular concern as a wide range of organisms, from plankton, to fish (consumed by humans), to larger vertebrates such as turtles or whales, may ingest them (Romeo et al., 2015; Wright et al., 2013).

Currently, there is a significant gap in establishing the presence and effects of marine litter on marine organisms and the potential effects on human health and seafood consumers. This gap must be covered using sentinel species to determine their presence and effects, and to implement future mitigation actions worldwide (Galgani et al., 2014, 2015).

Seabirds

Ingestion of plastics is documented in many marine organisms, in particular sea turtles and marine birds. Seabirds are long-lived top predators that conduct long migrations and forage extensively offshore. These characteristics make them potentially sensitive indicators of the health of the marine ecosystem. In birds, plastic is present in the stomachs of an estimated 90% of individuals, with a prediction that plastic ingestion will be present in 99% of all seabird species by 2050 (Wilcox et al., 2015).

Northern Fulmars (Fulmarus glacialis) is the best studied organism as a sentinel for marine debris ingestion; it is, therefore, used as an indicator of the state of the North Sea ecosystem (van Franeker et al., 2011) and as a model for bird plastic ingestion worldwide (e.g., British Columbia, Alaska, the Canadian Arctic, the western North Atlantic; Bond et al., 2014). The Ecological Quality Objective (EcoQO), established by the Oslo-Paris Convention (OSPAR, 2008), identifies a target of no more than 10% of fulmars having >0.1 g of plastic in their systems. Currently, the only standardized methodology for indicators of marine litter within the European Marine Strategy Framework Directive (MSFD) is the OSPAR EcoQO for litter particles in stomachs of Northern fulmars.

Nevertheless, it is clear that this species cannot represent the whole body of water in Europe and worldwide, owing to the diversity of oceans. Thus, a range of other marine sentinels for marine litter ingestion need to be selected for monitoring this emerging issue at different scales and habitats to elucidate the effects on biota.

Sea Turtles

The loggerhead sea turtle was recently proposed by the European MSFD Technical Subgroup of Marine Litter (Descriptor 10) as an indicator species to detect the ingestion of marine litter by biota in the Mediterranean Sea and nearby Atlantic areas (Galgani et al., 2013). The “sea turtle tool” is classified as “under development,” indicating that enough information exists to be able to suggest a monitoring approach for this species. The loggerhead sea turtle (Caretta caretta) is one of the most common and widespread marine turtle species and the most abundant in the entire Mediterranean Basin. Because of its distribution, the habitat use and migration movements can serve as bioindicators of marine litter at subbasin and basin scale. As an omnivore, this turtle ingests a large amount of debris, mistaking the debris for food, causing, in the worst case scenario, death due to entanglement in marine debris or occlusion of the gastrointestinal tract.

Campani et al. (2013) investigated the presence and frequency of occurrence of marine litter in the gastrointestinal tract of the Caretta caretta found stranded or accidentally caught in the North Mediterranean Sea. Marine debris were present in 71% of specimens; when the debris was subdivided into different categories according to the Fulmar Protocol (van Franeker et al., 2011), the main type of marine debris found was plastic, with the most frequent occurrence being sheet-like plastic. The adult specimens showed higher values of marine litter ingested than juveniles. The presence of marine debris observed in this research confirms the high impact of marine debris in the Mediterranean Sea compared to other seas and oceans, and highlights the importance of Caretta caretta as a good indicator for Descriptor 10 (marine litter) in the MSFD.

To support the recommendation of the sea turtle as a sentinel species and to look beyond European needs to find an indicator to reach the “good environmental status” proposed by the MSFD by 2020, several studies have demonstrated the occurrence of marine litter and plastic debris in the gastrointestinal tract of several species of sea turtles worldwide. Marine litter has been observed to have lethal and sublethal effects on five species globally, in particular in the green turtle (Chelonia mydas) and leatherback turtle (Dermochelys coriacea) (Schuyler et al., 2013). For most species, the oceanic phase of sea turtles (corresponding to the juvenile stage in most reptile species) is the phase most threatened by the risk of plastic ingestion (Schuyler et al., 2013; Santos et al., 2015), representing a severe threat for the fitness of vulnerable turtle populations worldwide.

Although researchers have reported on ingestion of anthropogenic debris by marine turtles and implied incidences of debris ingestion have increased over time, there has not been a global synthesis of the phenomenon since 1985. Thus, we analyzed 37 studies published from 1985 to 2012 that report on data collected from before 1900 through 2011. Specifically, we investigated whether the prevalence of ingestion has changed over time, what types of debris are most commonly ingested, the geographic distribution of debris ingestion by marine turtles relative to global debris distribution, and which species and life-history stages are most likely to ingest debris. The probability of green (Chelonia mydas) and leatherback turtles (Dermochelys coriacea) ingesting debris increased significantly over time, and plastic was the most commonly ingested debris. Turtles in nearly all regions studied ingest debris, but the probability of ingestion was not related to modeled debris densities. Furthermore, smaller, oceanic-stage turtles were more likely to ingest debris than coastal foragers, whereas carnivorous species were less likely to ingest debris than herbivores or gelatinovores. Our results indicate that oceanic leatherback turtles and green turtles are at the greatest risk of both lethal and sublethal effects from ingested marine debris. To reduce this risk, anthropogenic debris must be managed at a global level.

The evaluation of the plastic ingestion rate by long-living organisms that feed predominantly in marine environments, travel long distances across the sea and oceans, and cross different environments can represent a warning signal.

Marine Mammals as Sentinels of Ocean Health

Sentinel species with physiology and/or diets similar enough to those of humans, such as marine mammals, may provide an early indication of potential adverse health effects and provide insight into the toxic mechanisms of a given hazardous agent (Schwacke et al., 2013).

Multiple stress factors stemming from the bioaccumulation of anthropogenic contaminants combined with infectious diseases, food depletion, and climate change pose potential hazards to marine mammal populations worldwide (Figure 4). For this reason, attention is focusing on marine mammals as charismatic sentinels of ocean change.

Marine mammals have similar mammalian physiology to humans and are long-living top predators, so they can be effective indicators for chronic or slow developing pathologies that are more difficult to detect in human populations exposed to lower levels of the same hazard (Bossart, 2011). A wide variety of diseases have been observed in marine mammals worldwide that have heightened the scientific community and public awareness of their risk of environmental exposure to contaminants, biotoxins, and pathogens (Schwacke et al., 2013).

In the past, marine mammals were not generally considered to be useful sentinel species because of their protected status and the difficulty of obtaining tissue samples. However, after several large-scale mortality events of marine mammals worldwide, concern from the scientific community has led to the establishment of a global biomonitoring program to collect data to help elucidate temporal and geographic trends. To this end, marine mammal tissue banks (such as the U.S. National Marine Mammal Tissue Bank and the Mediterranean Marine Mammal Tissue Bank) and marine mammal stranding networks were established worldwide. The tissue banks and stranding networks have proven to be very useful tools for evaluating temporal and geographic trends of environmental exposure to contaminants, biotoxins, and pathogens, standardizing collection, banking, and analyzing marine mammal tissues (Schwacke et al., 2013).

An alternative option to monitoring the health status of marine mammals is the remote sampling of skin biopsies from free-ranging animals, a method confirmed to be a powerful, relatively noninvasive method of sampling (Fossi & Marsili, 1997). Since the 2000s, several research groups have been using a nonlethal biomarker approach through skin biopsies and “in vitro” models using fibroblast cell cultures and organotypic cell lines exposed to different doses of contaminants obtained from the biopsies (Godard-Codding et al., 2011; Fossi & Marsili, 1997). The classic approach applied to skin biopsies has been the quantification of Cytochromes P450 (CYP1A and CYP2B) protein induction, immunofluorescence assays, and the quantification of POPs. Besides this classic biomarker, the use of gene-expression biomarkers was appropriate for this kind of tissue to investigate at the molecular level early warning on the molecular pathway of toxification or detoxification systems (Panti et al., 2011).

The following section describes several key studies that diagnose toxicological stress syndromes related to multiple human pressures in marine mammals (e.g., bioaccumulation of anthropogenic contaminants combined with infectious diseases, food depletion, and climate change). These studies underline the role of these organisms as sentinels of ocean health (Figure 4).

Sentinel Species of Marine EcosystemsClick to view larger

Figure 4. Concurrence of human-made pressures on marine mammals.

This section also outlines the concept of different marine mammal species as sentinels of ocean health in relation to their different home ranges (Figure 5).

Sentinel Species of Marine EcosystemsClick to view larger

Figure 5. Marine mammals species as indicators of ocean health in relation to their different spatial distribution.

Bottlenose Dolphin and Pinnipeds: Sentinels of the Coastal Environment

The environmental forces exerting pressure on the coastal environment can affect the health of the entire coastal ecosystem, causing long-term consequences for organisms. The cumulative anthropogenic stress can lead to a complex plethora of effects, which can be monitored by coastal sentinel species under the One Ocean-One Health concept.

Marine mammals living in coastal and estuarine environments, such as the bottlenose dolphin (Tursiops truncatus), are considered to be early sentinels of coastal ecosystems owing to their status as long-living top predators, their large amount of fat tissues, and their chronic exposure to persistent pollutants and environmental changes (Wells et al., 2004; Kucklick et al., 2011; Mancia et al., 2015).

As an apex predator, the bottlenose dolphin is particularly exposed to the accumulation of persistent contaminants and mercury. It has been proposed as a sentinel for exposure to mercury in cetaceans and humans (Reif et al., 2015). Mercury is a global contaminant, released by industrial sewage, mining activities, and natural causes (Tewalt et al., 2001). Organic mercury, methylmercury (MeHg), is bioaccumulated and biomagnified along the food web. Several studies have reported high concentrations of mercury in the tissues sampled from stranded organisms and free-ranging bottlenose dolphins, including the well-studied bottlenose dolphin populations inhabiting Saratosa Bay and Indian River Lagoon in Florida (Stavros et al., 2011; Reif et al., 2015), which can serve as long-term sentinels.

In addition to the measurement of total mercury burden in different tissues, organisms with increased blood and skin mercury concentrations presented evidence of endocrine disruption, including alteration of several hormone levels, liver damages, and immune system depression (Reif et al., 2015). Historically, mercury is known to cause adverse health effects in human endocrine, immune, and nervous systems. The most iconic syndrome related to mercury exposure in humans is “Minamata Disease,” discovered in consumers of methyl mercury-contaminated fish and shellfish in the Minamata Bay (Japan) in the 1960s (Harada, 1995). Since bottlenose dolphins share similar habitats, diets, and physiologies with humans, they can be considered sentinels for chronic exposure to mercury as well as a complex mixture of other threats including xenobiotic compounds, natural biotoxins, and pathogens.

Several studies have been carried out on the exposures and effects of oil spill-associated stress over the long term in cetaceans like killer whales, particularly after the Exxon Valdez oil spill in Alaska in 1989 when a population decline was observed (Matkin et al., 2008). Studies on bottlenose dolphins inhabiting bays and sounds were recently carried out to assess the potential impact of the severe oil spill in the Gulf of Mexico in 2010 (Deepwater Horizon oil spill). Low survival rates and high rates of reproductive failure, unusual strandings, reproductive impairment, hematologic abnormalities, lung disease (Lane et al., 2015; Schwacke et al., 2014), and immunotoxicity (Barron, 2012) in bottlenose dolphins were found. The integration of all the data collected on long-term monitoring of both live and dead bottlenose dolphins could help researchers fully understand the impacts of oil spills and other stressors at the population level, including possible threats to humans.

Marine mammals living in coastal and estuarine environments can also be sentinels of emerging infectious disease, providing important evidence on the coastal ecosystem and public health. This is the case of viral (e.g., Morbillivirus), bacterial (e.g., Brucella), protozoan (e.g., Toxoplasma), and mycotic (e.g., Lobomycosis) diseases (Bossart, 2011). Several studies have shown that increasing environmental pressure can cause more frequent and severe zoonosis and that marine mammals can be infected with pathogens from both marine and terrestrial origin (particularly from sewage municipal wastewater treatment or runoff from agricultural land). Antimicrobial-resistant strains of the bacteria, Escherichia coli, have been isolated from several marine mammals, including free-ranging bottlenose dolphins in South Carolina and Florida (Greig et al., 2015). The parasite, Toxoplasma gondii, usually transmitted from terrestrial mammals’ feces, is currently one of the major cause of pathology and mortality in California sea lions (Zalophus californianus) (Carlson-Bremer et al., 2015). Zoonotic gastrointestinal bacterial pathogens, such as Salmonella, have also been detected in stranded elephant seals (Mirounga angustirostris) in California (Stoddard et al., 2005).

Similarly, harbor seals (Phoca vitulina), which use urbanized coastal habitats, are opportunistic feeders, and have a strong site fidelity, can acquire enteric bacteria from the environment and food. Vibrio infection has been found in free-ranging and stranded harbor seals in the waters off California (Hughes et al., 2013). Not only pathogens, but also harmful algal bloom biotoxins (e.g., Domoic acid) have caused severe outbreaks in sea lions inhabiting California coasts (Goldstein et al., 2008), while harbor seal populations have declined in Scottish waters owing to several cumulative factors, including toxins from harmful algae (such as domoic acid and saxitoxins) resulting from the consumption of contaminated prey (Jensen et al., 2015).

Considering that humans share the environment and food resources with seals and other marine mammals, the spread of pathogens and biotoxins observed in sentinel marine mammals also may be of concern to human health and may have strong implications for understanding how human pathogens can be spread in coastal environments (Baily et al., 2015) and the extent of coastal habitat degradation.

Striped Dolphin: Subbasin Sentinel Species

In the Mediterranean Sea, the striped dolphin (Stenella coeruleoalba) is very frequent; it is distributed in a gradient from east to west in both inshore and offshore waters, suggesting subpopulations in western and eastern basins (Gaspari et al., 2007). Since it is a cosmopolitan species, it is abundant at a global scale as well. Nevertheless, the large Mediterranean population is believed to be resident, and it does not mix with the eastern Atlantic population. Since striped dolphins have a pelagic distribution throughout the basin, feed on pelagic and bathypelagic species, have abundant fatty tissue and a limited capacity to metabolize certain PCB congeners, these dolphins show the highest levels of Organochlorine Compounds of all marine mammals sharing the same habitat (Borrell & Aguilar, 2005).

Anthropogenic pressures on cetaceans in the Mediterranean Sea are potentially affecting population stability and marine biodiversity (Figure 4). This effect was demonstrated for the only pelagic marine-protected area in the Mediterranean Sea, the Pelagos Sanctuary for Mediterranean Marine Mammals. A multidisciplinary tool using diagnostic markers elaborated in a statistical model to rank toxicological stress in Mediterranean cetaceans was applied to the analysis of persistent bioaccumulative and toxic (PBT) chemicals. These data were correlated to a wide range of diagnostic markers of exposure to anthropogenic contaminants and the genetic variation by analysis of nuclear markers (microsatellite) was performed as a marker of genetic erosion in striped dolphin skin biopsies (Panti et al., 2011; Fossi et al., 2013). For this particular sentinel species, the statistical model was applied to obtain a complete toxicological profile of the striped dolphin in pelagic areas across the Mediterranean Sea. The proposed set of diagnostic tools in skin biopsies provided evidence of toxicological stress in striped dolphin living in the Pelagos Sanctuary, emphasizing differences in the PBT chemicals and molecular biomarker responses in the three striped dolphin populations investigated. The highest toxicological impact in the Pelagos population was highlighted by high PBT chemical levels, combined with associated biomarker responses (Fossi et al., 2013).

The results support an association between genetic diversity and toxicological stress, confirming that genetic variability is linked to resilience. Individuals with lower heterozygosis reported significantly higher contaminant loads (50% of the dolphins of the Pelagos Sanctuary). A statistical model was applied to obtain a complete toxicological profile of the striped dolphin in the Pelagos Sanctuary and other Mediterranean areas (i.e., the Ionian Sea and the Strait of Gibraltar). Application of the classification model provided an outline of the toxicological status of striped dolphin populations and represented a potential tool for the monitoring and conservation of cetacean biodiversity and their habitats (Figure 6). Particular concern arises from the evidence that 50% of the striped dolphins from the Pelagos Sanctuary were classified in the high toxicological hazard group (Figure 6), suggesting that other top predator species are exposed to the same hazards.

Sentinel Species of Marine EcosystemsClick to view larger

Figure 6. Canonical discriminant weights for ranking toxicological risk in striped dolphin in the Mediterranean Sea in three different sampling areas: Pelagos Sanctuary (I), the Ionian Sea (C), and the Strait of Gibraltar (G) (Fossi et al., 2013).

Evidence of toxicological stress in cetaceans living in the Pelagos Sanctuary confirms the use of small cetacean species as useful sentinels at the subbasin scale and underscores the high toxicological pressures in this region, with potential consequences for the food chain and human health.

Fin Whale: Basin Sentinel Species

As discussed earlier, there is increasing concern that a wide range of marine organisms are affected by plastic wastes in the sea (see Seabirds and Sea Turtles as Indicators of Marine Litter Ingestion). The interactions between cetaceans and microplastics have been investigated recently in the free-ranging fin whales (Balaenoptera physalus), comparing populations living in two semienclosed basins, the Mediterranean Sea and the Sea of Cortez (in the Gulf of California, Mexico; Fossi et al., 2016). Fin whales, the only resident mysticete in the Mediterranean, aggregate during summer in the feeding grounds of the Pelagos Sanctuary and migrate to the southern Mediterranean Sea during winter. In the Sea of Cortez, fin whales are resident and genetically isolated from other Pacific populations. Fin whales forage on the dense aggregations of krill in the water column and near the surface, engulfing an average of 71 m3 of water per mouthful (Goldbogen et al., 2007). As a result, fin whales are exposed to a high potential risk of microplastic ingestion in their feeding grounds owing to the ingestion of contaminated prey and to the direct ingestion of floating microplastics. This species can represent a critical indicator of the microplastic contamination in a whole basin.

In this case study, considerable abundance of microplastics and plastic additives was demonstrated in the superficial zooplankton samples from the Pelagos Sanctuary of the Mediterranean Sea (compared to those detected in Sea of Cortez). In addition, pelagic areas containing high densities of microplastics overlapped with whale feeding grounds, suggesting that whales are exposed to microplastics during foraging (Figure 7).

Sentinel Species of Marine EcosystemsClick to view larger

Figure 7. Cluster dendrogram on phthalates, OCs, and biomarkers responses in skin biopsies of fin whales resident in the Mediterranean Sea and Sea of Cortez. The two populations of whales are statistically different. Abundance of microplastics in neustonic samples collected in the Mediterranean Sea (red) and Sea of Cortez (blue) (Fossi et al., 2016).

Given the abundance of microplastics in the Mediterranean environment, along with the high concentrations of PBT chemicals, plastic additives, and biomarker responses detected in the biopsies of Mediterranean whales as compared to those in whales inhabiting the Sea of Cortez, the exposure to microplastics because of direct ingestion and consumption of contaminated prey poses a major threat to the health of fin whales in the Mediterranean Sea. The temporal and regional ecotoxicological differences support the hypothesis that the fin whale is a large-scale indicator of the impact of microplastics and related contaminants in pelagic environments as well as a charismatic sentinel of the integrity of the marine food chain on the basin scale.

Sperm Whale: World-Ocean Sentinel Species

While coastal and pelagic dolphins and baleen whales can serve as sentinel species from coastal to basin scale, the sperm whale (Physeter macrocephalus) can be considered a worldwide sentinel of ocean pollution and health. Among the cetaceans, the sperm whales are the most cosmopolitan species. They prefer ice-free waters over 1000 meters deep. Although both sexes range through temperate and tropical oceans and seas, only the adult males populate the higher latitudes. Populations are denser close to continental shelves and canyons.

Biomarker and contaminant analyses in the skin biopsies of the threatened sperm whale collected worldwide could reveal geographical trends in exposure on an oceanwide scale (Godard-Codding et al., 2011). The Intergovernmental Oceanographic Commission (IOC) (2001) recommended that ocean health monitoring programs investigate the presence of marine contaminants and the health of threatened species as well as the use of multiple and early-warning biomarker approaches. Godard-Codding and collaborators (2011) analyzed CYP1A1 expression (by immunohistochemistry), stable nitrogen and carbon isotope ratios (as general indicators of trophic position and latitude, respectively), and contaminant burdens (e.g., POPs) in skin biopsies to explore regional trends in the Pacific Ocean. Biomarker analyses revealed significant regional differences in exposures and effects within the Pacific Ocean. For example, the large-scale monitoring study was successful in identifying regional differences in CYP1A1 expression, providing a baseline for this known biomarker of exposure to aryl hydrocarbon receptor agonists.

More recently, Savery and collaborators (2015) established a global baseline of oceanic lead (Pb) concentrations using free-ranging sperm whales as an indicator species. Lead is an oceanic pollutant of global concern. Skin biopsies were collected during the voyage of the Odyssey (2000–2005) from 17 regions taking into account whale gender and age. This research, the first global toxicological dataset for lead in cetaceans, confirmed that lead is widely distributed, with hot spots in some regions. Future oceanwide CYP1A1 expression profiles and pollutant data in sperm whale skin biopsies are desirable and could reveal whether globally distributed chemicals occur at biochemically relevant concentrations on a global basis. Such a study could provide a measure of ocean integrity and clarify the long-term effects on the food chain and human health.

Marine Mammals as Sentinels to Impacts of Climate Change

The earth is experiencing a rapid shift in environmental stability, which challenges the adaptive capacity of Arctic marine mammals. The polar bear (Ursus maritimus), walrus (Odobenus rosmarus), bearded seal (Erignathus barbatus), and ringed seal (Phoca hispida) may be especially vulnerable due to life histories reliant on sea ice (Moore & Huntington, 2008). Reductions in Arctic sea ice extent and thickness have become a hallmark of climate change, but impacts to marine ecosystems are poorly understood. In particular, the polar bear, as an apex predator of the Arctic marine ecosystem, receives increased attention in the climate change discussion. Declines in polar bear abundance and sea ice habitat by the end of the 21st century support the listing of this species as threatened under the Endangered Species Act (Hunter et al., 2010).

As top predators, marine mammals also must adapt to environmental changes that result from biophysical and anthropogenic forcing; thereby they can act as sentinels to ecosystem variability and reorganization (Moore, 2015). Marine mammals can act as ecosystem sentinels because they respond to climate change through shifts in the distribution, timing of their movements, and feeding habits and locations. Data from decades-long studies, many conducted in partnership with indigenous people, provide a foundation for evaluating the impacts of climate change on marine mammals in the Pacific Arctic Sector. Synthesis of the Arctic Research (SOAR) Project reported on changes in ice seal diets and the divergent trends in seal and whale body condition at local and regional scales due to climate change (Moore, 2015; Laidre et al., 2015).

If polar bears can reflect global climate changes related to the arctic ecosystems, migratory species, such as the humpback whale (Megaptera novaeangliae), can reflect climate variability and changes in ecosystem dynamics worldwide. Analysis of the humpback’s diet over 20 years has demonstrated a shift of prey from krill to schooling fish from cooler to warmer waters due to the delay of upwelling phenomena (Fleming et al., 2016). Thus, the changes in the feeding habit of humpback whales could represent a sentinel of the impacts of water temperature variation across the food web, and, therefore, of plankton and fish abundance, as well as trophic chain biodiversity and ecosystem stability, in relation to global climate change.

Finally, marine mammals are fundamental to the nutrition and cultural heritage of Arctic indigenous people, thereby providing a vital link between the ocean and human health. In this context, Sue Moore, a NOAA oceanographer says that “[m]arine mammals connect people to ecosystem research by making it relevant to those who live in the Arctic and depend on these mammals for diet and cultural heritage and people around the world who look to these animals as symbols of our planet’s health” (NOAA, 2014).

Concluding Remarks

The rapid changes in the marine environment and the continuous evolution of human impacts and emerging threats support the need for in-depth study of the connection between the health of marine species and humans. Researchers from different areas of expertise have begun to unravel the relationships between exposures to environmental stressors (e.g., climate change, pollutants, marine waste) and a range of endpoints in sentinel species as an indicator of ecosystem health and a harbinger of human health and well-being.

Specifically, there is an urgent need to improve early warning diagnostic biomarkers in sentinel species that occur shortly after exposure to negative stressors and that could prevent chronic exposure and, subsequently, long-term effects at both the individual and community level, thus affecting population viability. The novel system biology and omics-approach need to be further improved in the area of environmental and life sciences as a whole, and the resulting enormous amount of data need to be comprehensively analyzed in the interest of providing a more accurate diagnosis of a multiple risk assessment.

Finally, marine organisms, in particular marine mammals, can serve as sentinels for ocean perturbation that can affect wildlife and human health. This strong linkage constitutes the basis for the One Health approach, which should drive the environmental research in a multidisciplinary perspective. International cooperation, including researchers, stakeholders, and policymakers, will pave the way to a common methodological approach to face emerging environmental issues on global scale, ranging from nanomaterials to climate change.

Acknowledgments

Sincere thanks are due to Letizia Marsili, Silvia Casini, Ilaria Caliani, Matteo Baini, Daniele Coppola, Teresa Romeo, Roberta Minutoli, Giancarlo Lauriano, Maria Grazia Finoia, Simone Panigada, Claudio Leonzio, Jorge Urban, and Michael H. Depledge for their invaluable scientific support during the research activities related to some of the data presented in this article.

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