Understanding the Environmental Risks of Unplanned Discharges – The Australian Context: Marine Mammals
Michelle Bejdera and Adam Gartnera
a BMT Oceanica Pty Ltd, PO Box 462, Wembley, WA 6913
September 2016
Document No. 1128_01_001/4_Rev1
Client: APPEA Document history
Distribution
No. copies Revision Author Recipients Organisation Date & format Rev A M Bejder R Harcourt Macquarie University 1 x docm 02/09/15 Rev B M Bejder K Hoefhamer BMT Oceanica 1 x docm 06/09/15 Technical Review Panel Rev C M Bejder K Lee 1 x docm 13/11/15 (CSIRO) M Bejder BMT Oceanica Project Rev D M Bailey 1 x docm 10/02/16 A Gartner Director D Hills M Bejder APPEA Project Steering 1 x docm Rev 0 L Smith 18/02/16 A Gartner Group 1 x pdf R Smith 1 x docm Rev 1 A Gartner A Taylor APPEA 30/08/16 1 x pdf
Review
Revision Reviewer Intent Date Rev A R Harcourt Technical Review 06/09/2015 Rev B K Hoefhamer Editorial Review 22/09/2015 Rev C K Lee Technical Review 17/12/2015 Rev D M Bailey Final sign-off for submission 17/02/2016 D Hills APPEA Project Steering Group Rev 0 L Smith 17/08/16 approval R Smith Rev 1 A Taylor Final submission 30/08/16
Contents
1. Introduction ...... 1 1.1 Behaviour and fate of crude oil in the marine environment...... 2 1.2 This review ...... 2 1.3 Environment Protection and Biodiversity Conservation Act ...... 3 2. Biological and/or Behavioural Vulnerabilities ...... 4 2.1 Cetaceans ...... 4 2.2 Pinnipeds ...... 6 2.3 Sirenians ...... 7 3. Impacts on Marine Mammals ...... 8 3.1 Toxicity associated with ingestion ...... 10 3.2 Toxicity associated with inhalation ...... 11 3.3 Ingestion of contaminated prey ...... 11 4. Capacity for Recovery ...... 12 5. Conclusions ...... 13 6. References ...... 14
List of Tables
Table 1.1 Key marine mammal species listed as a Matter of National Environmental Significance under the EPBC Act ...... 3
List of Figures
Figure 3.1 Conceptual impact pathways for hydrocarbon spills on marine mammals ...... 9
APPEA: Marine Mammals i
1. Introduction
Marine mammals are ubiquitous to most marine ecosystems. Many of these species are vulnerable to a range of natural disturbances and anthropogenic impacts, such as seismic activities, commercial exploitation, incidental shipping strikes, entanglement and reduced water quality from pollution (Nowacek et al 2004, Robbins et al 2004). Around the world, legislation governs the management and recovery of marine mammal species, ensuring their long-term protection and survival. Despite the legislative mechanisms put in place, anthropogenic activities can still pose a threat, and assessments on population, ecological relationships and anthropogenic impacts cannot always resolve actual risks from human activities. This includes risks associated with oil spill events, which can both directly and indirectly affect marine mammals, but because of their unplanned nature, are inherently difficult to control. According to AMSA (2015) there have been at least 44 large or notable oil spills in Australia since 1970 with the potential to impact marine ecosystems. Most of these were the result of shipping incidents, but they also include refinery and bulk storage spills, deliberate illegal dumping onshore and one oil platform wellhead blowout (Montara H1 well release starting on 21st August, 2009) (AMSA 2015). In light of such risk, this review provides a current state of knowledge examination of the consequences of oil spills on marine mammals, specific to the Australian context.
Coupled with anthropogenic pressures, marine mammals exhibit many defining characteristics that predispose individual populations to a delayed recovery once impacted, including large size, long life-spans, late reproductive age, few offspring, commercial value, distributions that cross international boundaries, and behaviours (Ehrenfeld 1970). Despite the vulnerability of marine mammals to human impacts, recent population trends in some species appear to have stabilized, or are showing strong signs of recovery (e.g. humpback whales (Bejder et al 2016) and southern right whales (Bannister 2001)). While for others, previously disturbed populations do not appear to have recovered (e.g. Australian sea-lions (DAFF 2007) and dugongs (Marsh et al 2005)), and therefore, smaller populations within these species remain highly vulnerable to impacts (Goldsworthy et al. 2010).
This review attempts to consolidate what is known in general about the effects of oil spills on marine mammal populations. However, it should be stated that the broad volume of scientific data on marine mammals are limited to high-profile species, while many other species remain inadequately described with limited information on their biology and ecology from which status can be assessed. For this reason, it is difficult to undertake a systematic review or make comprehensive comparisons to better understand some key questions of ecological significance about exposure to petroleum oils. Despite these limitations, this white paper presents the most recent review of what has been learnt in the past two decades from laboratory studies, actual incidents and published literature on the effects of petroleum oils on marine mammals, and therefore, represents an accurate and detailed status update of what is known on the topic as relevant to the Australian context.
APPEA: Marine Mammals 1 1.1 Behaviour and fate of crude oil in the marine environment This review is concerned with the interaction between crude oils and marine mammals, which utilise both near-shore and off-shore coastal environments. As such, it is important to understand that the behaviour and fate of crude oils in the marine environment can vary in space and time (National Research Council (NRC) 2003), which in turn, influences the likelihood and type of interaction spilt oils may have on marine mammals.
Because crude oils contain a wide range of compounds, from light to heavy; they can be affected by many different fate processes (NRC 2003) including evaporation, emulsification and dissolution. It is expected that evaporation will generally remove about one-third of the volume of a medium crude oil slick within the first day, but there will always be a significant residue (NRC 2003). Up to 100% of a very light product such as a condensate, 75% of a light crude and 40% of a medium crude oil, can be removed via this process (Hook et al. 2016). Inhalation of evaporated of oil compounds and associated toxicity is relevant to marine mammals because of their breathing requirements at the sea surface.
Many crude oils will also emulsify readily, a process that can greatly reduce subsequent weathering rates (NRC 2003). Emulsification is the opposite of dispersion in that water is entrained within the slick to form a ‘chocolate mousse’ on the sea surface. Mousse formation tends to occur most readily in oils with a lower viscosity and when there is an energetic sea state (Hook et al. 2016). Emulsification of oils is also of relevance to many marine mammals because of vulnerability to external oiling, which in turn can effect capacity for thermoregulation, or interfere with surface feeding requirements.
Crude oils also have the potential to adsorb heavily onto intertidal sediments, with the risk of subsequent erosion of oiled sediments from the shoreline and deposition in near-shore habitats where some marine mammals, such as seals, inhabit (NRC 2003). Dissolution from slicks and stranded oil can persist for weeks to years (NRC 2003). Notwithstanding, while near-shore oil spills often pose a high risk to coastal dwelling fauna, an off-shore spill is much more likely to lose a significant portion of its toxic components before it reaches coastal waters (Haapkylä 2007). This process can be further accelerated with the use of dispersants. For example, within 24 hours of discharge, it is expected that the dispersed oil will mix into the top 10 m of the water column and be diluted to concentrations well below 10 ppm, with dilution continuing as time proceeds. As biodegradation takes place over the following weeks, dispersed oil concentrations could be expected to decline to less than 1 ppm (Lee et al 2013). 1.2 This review This white paper, which forms part of a boarder series of white papers examining the risks of oil spills on the marine environment, aims to provide an up-to-date review of the consequences of petroleum oil spills for Australian marine mammals. This information can be used to better plan for, and mitigate impacts associated with large scale hydrocarbon discharges.
It is important to highlight that marine mammals only represent one component of the marine environment, and the effects of hydrocarbons on other components of the ecosystem (e.g. fish, benthic macroinvertabrates, mangroves, corals) are addressed in separate white papers. It is also acknowledged that this white paper focuses on the effects of the unplanned discharges of crude and dispersed crude oil and condensate. There are numerous other forms of petroleum hydrocarbon
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contamination in the marine environment (e.g. shipping, produced formation water, drilling fluids). Accordingly, and where relevant, information on downstream products has been extrapolated to provide a better understanding of the potential implications of the large scale effects of crude oil exposure. However, while Australia is expected to become one of the world's chief exporters of gas, very little is known about the environmental fate or impacts of gas condensate on marine mammals within the Australian environment (Hook et al. 2016), and therefore this paper does not address this question. Nor does this paper address impacts associated with oil spill clean-up operations, which while also relevant, are planned to be addressed in other APPEA publications.
Finally, it is important to highlight that each uncontrolled oil release represents a unique set of physical, chemical, and biological conditions. As such, the information presented here is intended to serve as a guide and not an absolute outcome, especially given the paucity of regional information in the Australian context. 1.3 Environment Protection and Biodiversity Conservation Act The Environment Protection and Biodiversity Conservation Act 1999 (EPBC Act) requires government approval for any action that is likely to have a significant impact on a ‘Matter of National Environmental Significance’ (MNES), which include listed threatened species as well as migratory species, many of which are marine mammals. While it is not the aim of this review to identify all EPBC Act listed species, it is important to recognise that petroleum exploration/development is generally regarded as a controlled action under the EPBC Act (DoE 2013). Some key species which are commonly considered in most offshore oil and gas environmental approvals are listed in Table 1.1.
Table 1 .1 Key marine mammal species listed as a Matter of National Environmental Significance under the EPBC Act
Marine Fauna Common Name Scientific Name Listing Status Group Blue or pygmy blue whale Balaenoptera musculus Endangered; Migratory Southern right whale Eubalaena australis Endangered; Migratory Humpback whale Megaptera novaeangilae Vulnerable; Migratory Fin whale Balaenoptera physalus Vulnerable; Migratory Sei whale Balaenoptera borealis Vulnerable; Migratory Antarctic minke whale Balaenoptera bonaerensis Migratory Cetacean Bryde's whale Balaenoptera edeni Migratory Sperm whale Physeter macrocephalus Migratory Killer whale Orcinus orca Migratory Indo-Pacific bottlenose dolphin Tursiops aduncus Migratory Australian snubfin dolphin Orcaella heinsoni Migratory Indo-Pacific humpback dolphin Sousa sahulensis Migratory Pinniped Australian sea lion Neophoca cinerea Vulnerable Sirenian Dugong Dugong dugon Migratory
APPEA: Marine Mammals 3 2. Biological and/or Behavioural Vulnerabilities
In excess of 100 mammal species rely on the ocean for survival globally and represent a diverse collection of biological and behavioural adaptations to the aquatic lifestyle. The extensive range of marine mammal habitat preferences, sensory capabilities and ecological vulnerabilities requires diverse management and conservation conditions to effectively protect an area and the various species that use that area. In Australia, marine mammal species occupy offshore pelagic areas, coastal shallow waters and terrestrial landscapes. Each species inhabits preferred habitats that are biologically important for breeding, foraging, resting, migrating and ultimately, their survival. Some of their life history parameters constrain their potential for recovery and growth, including long life- spans, low reproductive rates and high offspring investment. An unplanned discharge in a biologically important area may potentially result in habitat loss and degradation, displacement, reduced foraging or mating success, and at its most extreme, death and population loss. However, the impacts to each species will vary based on anatomy, physiology, behaviour, life history parameters and environmental conditions. Therefore, the environmental risks of unplanned discharges to marine mammals are contingent on the distinct biological and behavioural vulnerabilities of each species or population, and interspecific differences in vulnerability will generally be lower than those between populations of the same species. 2.1 Cetaceans The Australian cetacean species include mysticetes (baleen whales) and odontocetes (toothed whales), and both groups display a continuum of biological and behavioural vulnerabilities to oil pollution. The characteristics that would put a species or population most at risk are: 1) being rare (low abundance); 2) limited geographic range; 3) strong habitat preferences (site fidelity); and/or 4) behave in such a way that increases direct exposure to potential oil spills.
In Australia, 47 odontocete species are distributed in both offshore pelagic and inshore coastal areas, and the most vulnerable would be rare species that show strong site fidelity within limited distribution ranges. The northern, inshore coastal dolphins (such as the Australian snubfin or Indo- Pacific humpback dolphins) have disjunct distributions, tend to aggregate in bays and estuaries where they show strong site fidelity and occur in relatively low numbers. These include dolphin species occurring in shallow, coastal waters with low population abundances, (DSEWPaC 2012, Allen et al. 2012, Cagnazzi et al. 2011, Parra et al. 2006). Their isolated distributions generally consist of small group sizes (<10 individuals per group) with little evidence of migration. In Cleveland Bay, northeast Queensland, populations of Australian snubfin and Indo-Pacific humpback dolphins were estimated at less than 100 individuals for each species (Parra et al. 2006). In north-western Australia, field surveys documented similarly small group sightings for these same species, also highlighting their isolated and rare distribution along coastal habitats (Allen et al. 2012). Their recurrent use of specific bays suggests strong site fidelity and further increases their vulnerability to habitat degradation or loss. Based on these biological characteristics, the recovery potential of coastal dolphin species is limited, rendering them extremely vulnerable to severe, local impacts. If an unplanned discharge occurred in one of these coastal, biologically important areas, potential impacts may include habitat loss and fragmentation, displacement, reduced foraging and reproductive success and ultimately, localised population extinctions.
Mysticete feeding strategies expose them to negative impacts from oil pollution through direct contact with the contaminants. The three mysticete foraging strategies (suction feeding, skimming and engulfing) exploit prey found in different depths throughout the water column. At the surface of
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the water, Southern right whales feed by swimming slowly with open mouths while “skimming” for prey (Kenney 2002). Their numerous (250–390 plates) and extremely long (3 m) baleen is finely textured to filter prey as water moves through (Rice 2002). The larger and more streamlined mysticetes of the Balaenopteridae family (i.e. rorquals) forage by swimming rapidly through prey while engulfing large volumes of water by expanding their pleated throat grooves (Berta et al. 2006). Blue whales may engulf up to 70 tons of water in a single attempt and strain prey through their shorter and coarser baleen. While primarily feeding in the Antarctic, humpback whales may opportunistically feed while migrating through Australian waters (DSEWPAC 2012). Therefore, foraging mysticetes may directly contact hydrocarbon compounds if an unplanned discharge occurred within a feeding area.
Evidence suggests that many cetacean species are unlikely to detect and avoid spilled oil (Harvey & Dahlheim 1994, Matkin et al. 2008) and it is thought that the lack of an olfactory system likely contributes to the difficulty cetaceans have in its detection (Matkin et al. 2008). There are numerous examples where cetaceans have appeared to incidentally come into contact with oil and/or not demonstrated any obvious avoidance behaviour. Following the Exxon oil spill, Matkin et al. (2008) reported killer whales in slicks of oil as early as 24 hours after the spill. The slick resulting from the spill was several hundred kilometres long and moved southwest from its origin over several months, allowing an extended time and large geographic area for many cetaceans to come into contact with the oil. According to Harvey & Dahlheim (1994), in the months following the spill, there were also numerous observations of gray whales, harbor porpoises Phocoena phocoena, Dall’s porpoises and killer whales swimming through light-to-heavy crude-oil sheens. Evans (1982) observed that gray whales Eschrichtius robustus typically swam through oil seeps off California; although the gray whales modified their swim speeds and breathing rates, there was no consistent pattern of behaviour in regard the presence of the oil. In controlled experiments, Smith et al. (1983) found that captive bottlenose dolphins Tursiops truncatus initially avoided oiled areas in their tanks, but all eventually contacted the oil. Geraci & St. Aubin (1985) provided evidence that although captive bottlenose dolphins relied on vision to detect thick oil, tactile response was the primary factor in avoidance, while Smultea & Wursig (1995) found that dolphins apparently did not detect sheen oil and that although they detected slick oil, they did not avoid travelling through it.
The geographic ranges and distributions of all mysticetes occurring in Australia waters are very large. All extend beyond the Australian Exclusive Economic Zone, thus increasing the potential exposure to potential unplanned discharges (Harcourt et al 2014). Some mysticete whales, particularly those with coastal migration and reproduction, display strong site fidelity to specific resting, breeding and feeding habitats, as well as to their migratory paths. This natural propensity to return to the same breeding and feeding areas made these species particularly vulnerable to commercial exploitation during the whaling era (Taylor 2002). A number of species of mysticetes congregate predictably in high numbers thereby maximising resources that are only seasonally available, such as food and mates (Stern 2002). High-latitude foraging habitats are most productive during summer months, and low-latitude breeding and resting areas likely provide thermoregulatory benefits and protection from predators. For example, approximately 19,200 humpback whales reliably and consistently migrate to Camden Sound and Pender Bay, Western Australia, to breed and calve each year (IWC 2014, Jenner et al. 2001). Blue and pygmy blue whales may aggregate at Australian feeding areas, which may include but are not limited to the Bonney upwelling and Duntroon Basin, South Australia (November to April) and Perth Canyon, Western Australia (December to April; McCauley & Jenner 2010, McCauley et al. 2004, DEH 2005). Furthermore, Australian Southern right whales exhibit varying degrees of site fidelity, with the majority of females
APPEA: Marine Mammals 5 and calves returning to the same birthing location, while some also travel long distances between breeding grounds within a season (DSEWPaC 2013). If spilled oil reaches these biologically important habitats, the pollution may disrupt natural behaviours, displace animals to less optimal areas, reduce foraging or reproductive success rates and increase mortality. If sufficiently high numbers are impacted, the greater population may experience reduced recovery and survival rates. Site fidelity is accordingly a major risk factor for mysticetes to any unplanned discharge in a biologically important area. 2.2 Pinnipeds Three pinniped species breed in mainland Australasian waters and nearshore islands (the endemic Australian sea lion, the New Zealand fur seal and the Australian fur seal), and seven other species are likely to occur, three of which breed on Australia’s subantarctic islands (leopard seal, southern elephant seal and subantarctic fur seal; Shaughnessy 1999). Pinnipeds forage in the marine environment but return to land or ice to mate, give birth, care for offspring and moult (Bowen et al. 2002, Boyd 2002). There are temporal and spatial constraints on foraging and reproduction which vary seasonally. The distance between oceanic foraging areas and terrestrial breeding grounds vary depending on body size, diving capabilities and energy storage. Pinniped foraging is function of habitat, with Australian fur seals and Australian sea lions primarily feeding on the benthic shelf, while New Zealand fur seals are epi-pelagic feeders and venture beyond the continental shelf. All females of the Otariidae family (i.e. eared seals) are constrained to return to their breeding site year-round, while males show greater flexibility and may feed far from breeding areas outside of breeding seasons. However, male sea lions are more constrained due to the species’ protracted breeding season, which is further complicated by breeding asynchronicity between colonies. Therefore, in the event of an unplanned discharge, Australian pinnipeds are most vulnerable to negative impacts based on their abundance and reproductive constraints.
Australian pinniped colonies are occupied all year, and some have seasonal peaks in abundance for breeding (Shaughnessy 1999). The terrestrial breeding aggregations (i.e. rookery) and resting or haul-out sites are essential for pinniped reproductive success, particularly for females and young pups (Antonellis 2002). Some pinnipeds exhibit strong site fidelity to return to their coastal natal rookeries (philopatry) and haul-out sites, thereby increasing their vulnerability to habitat pressures and degradation. Australian sea lions exhibit extreme philopatry, which significantly influences the greater population structure and restricts recruitment to small, isolated colonies, thus increasing the population’s vulnerability to localised extinctions (Lowther et al. 2012, Campbell et al. 2008). Over relatively short distances (some colonies <20 km apart), distinct Australian sea lion populations may not show any evidence of genetic mixing or recolonising, emphasising how their limited movements and highly-structured populations are a unique characteristic of this rare species. This is exacerbated by the fact that Australian sea lions breed at numerous, small colonies, many with < 10 pups recruited per breeding cycle, each colony therefore extremely vulnerable to stochastic events (Goldsworthy et al. 2014). Furthermore, female Australian sea lions have geographically- fixed foraging specialisations that vary among individuals within the same colony, and both females and males will return repeatedly to the same foraging location (Lowther et al. 2011, 2012, 2013). The extreme, long-term site fidelity for natal rookeries as well as foraging areas is a significant vulnerability for Australian sea lions to habitat loss caused by unplanned discharges in the marine environment. Female dispersal, immigration or recolonisation is very unlikely (DSEWPaC 2013). Therefore, any negative impact to a female Australian sea lion that results in a loss or mortality could potentially lead to significant risk of extinction to already compromised and rare populations.
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Thermoregulation requirements for pinniped survival present a significant biological vulnerability to oil contamination. Marine mammals must adapt to the challenge of maintaining constant body temperature (i.e. thermoregulation) in a significantly colder aquatic environment and rely on blubber (matrix of collagen fibres) or fur for insulation (Castellini 2002). Fur not only traps dry air on the skin but also repels water and cold air away. While subcutaneous, thick blubber is most commonly used for thermal protection in adult seals (e.g. Australian sea lions), fur seals require high-quality, clean fur for insulation (Jenssen 1996). If their external fur is covered with spilled oil, their thermoregulation and diving capabilities may be compromised, and toxic hydrocarbons may be ingested or inhaled, potentially leading to hypothermia, reduced foraging ability and death.
New Zealand and Australian fur seals are particularly vulnerable to oil contamination and have previously been ill affected by oil spills in Western Australia. In 1991, New Zealand fur seal pups were contaminated by heavy fuel oil spilled from a bulk carrier (Shaughnessy 1999). These pups were captured and rehabilitated immediately, and their rocky coastal habitat was cleaned prior to returning the pups to the wild. Additionally, oil spilled from wrecked ships off the Tasmanian and Western Australian coasts were within close proximity to sensitive pinniped habitats. However, the spilled oil was not observed ashore, and impacts to pinnipeds are unknown (Gales 1991). 2.3 Sirenians The dugong distribution range extends from coastal to inland waters in tropical and subtropical environments and includes international regions of approximately 40 countries (Marsh et al. 1999). However, dugong populations are in a constant and global risk of decline resulting from habitat loss, disease, hunting and fisheries by-catch. The species’ extinction risk remains high and hindered by low natural growth rates (<5% annually) even under ideal circumstances of low mortality and no anthropogenic impacts (Marsh et al. 1999). Furthermore, any possible habitat reduction or degradation that negatively impacts their highly specialised dietary reliance on seagrass could be significantly detrimental to their recovery and survival.
Herbivorous dugongs have highly specialised diets for specific seagrass meadows and may selectively forage for resources with high nitrogen and starch content (Sheppard et al. 2010, Marsh et al. 1999). Significant changes in seagrass availability documented two primary types of dugong responses: displacement to less optimal areas or reduction in reproductive potential. In Queensland, two floods and a cyclone caused significant loss of seagrass habitats (>1000 km2) and forced a mass exodus of displaced dugongs and damaging consequences for the regional population, including emaciation, reduced calf sightings and death (Preen & Marsh 1995). Some dugongs unsuccessfully relocated up to 900 km away before eventually dying, and population recovery was estimated to take more than 25 years. Similarly, in Western Australia, a large-scale movement of dugongs (40% population increase) occurred in response to reductions in prey availability caused by a tropical cyclone, although the impacts of this abundance shift were not as detrimental to the population (Gales et al. 2004). Dugong populations that were not displaced following seagrass diebacks experienced reductions in life history and reproduction rate of females, including low birth rate, high calf mortality, later age of first parturition and less frequent births (Marsh & Kwan 2008). Signs of recovery and improvements in reproductive success were documented up to 15 years later. Therefore, dugongs are highly vulnerable to reductions in habitat quality, and an unplanned discharge in an important seagrass habitat could have severe and long- term impacts.
APPEA: Marine Mammals 7 3. Impacts on Marine Mammals
Marine mammals may come into direct contact with floating oil as they swim through water and surface to breathe. For mysticete whales, oil can adhere to barnacles, callouses on their skin or their baleen plates during filter feeding. For pinniped species, surface fouling may reduce insulation properties of fur and potentially lead to hypothermia, drowning and ingestion of toxic hydrocarbons (Peterson et al. 2003). Chemical contact may cause a variety of harmful injuries: skin and eye irritation; inflammation; burns to mucous membranes, mouth and nares; or increased susceptibility to infection (Marine Mammal Commission 2011). The following sections will summarise recently available scientific data, based on known cause-effect pathways for marine mammals (Figure 3.1). However, for a comprehensive review of physiological and toxic effects of marine mammals, please refer to Geraci and St Aubin (1990).
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Note: Cause-effect pathways identify conceivable outcomes of oiling of marine mammals in general; actual effects and long-term consequences will vary between species
Figure 3 .1 Conceptual impact pathways for hydrocarbon spills on marine mammals
APPEA: Marine Mammals 9 3.1 Toxicity associated with ingestion When marine mammals are exposed to oil at sea, toxic polycyclic aromatic hydrocarbon (PAH) compounds may be ingested. It has been suggested that from the intestines, these compounds may be absorbed rapidly into the blood and transferred to muscle, liver and blubber (Jenssen 1996). Ingestion of oil may cause gastrointestinal inflammation, ulcers, bleeding, diarrhoea and maldigestion by damaging organs (e.g. the liver, kidney, adrenal glands, spleen or brain), anaemia, cancer, congenital defects, immune system suppression and reproductive failure (Marine Mammal Commission 2011).
For whales, however, actual evidence of the acute effects of hydrocarbon ingestion is scarce because of limited opportunities to complete controlled testing (i.e. under experimental conditions), or to collect biological tissue samples from exposed individuals. It can be assumed that if an individual swallows sufficiently large volumes of oil, any metabolic capacity to break down and pass the oil is likely to be overwhelmed (Geraci & St. Aubin 1990). However, specific thresholds for concentrations and volumes are presently unknown. While many marine mammals appear to have the necessary liver enzymes to metabolise hydrocarbons and excrete them as polar derivatives, chronic ingestion of sub-toxic quantities of oil may have subtle effects which would only become apparent through long-term monitoring (Geraci & St. Aubin 1990). For example, the transfer of petroleum hydrocarbons through the mother’s milk to suckling young is a possible pathway.
For bottlenose dolphins, recent evidence identified adrenal gland dysfunction in the Gulf of Mexico. Following the Deepwater Horizon (DWH) oil spill, a large, multi-year unusual mortality event for cetaceans occurred in areas which also showed overlap with dispersion of the DWH petroleum hydrocarbon plume (Venn-Watson et al. 2015). A histological evaluation assessed the factors that contributed to the cause of deaths for 46 fresh dead carcasses of bottlenose dolphins (Venn-Watson et al. 2015). The results indicated 33% of dolphins had a high prevalence of thin adrenal gland cortices, which was hypothesized to be the result of direct exposure to and ingestion of high levels of PAHs (Venn-Watson et al. 2015). Adrenal gland injury may have led to chronic adrenal insufficiency, a life-threatening disease that causes adrenal crisis and death in mammals, especially when the animal's condition is further compromised by pregnancy, cold temperatures and infections. The observed chronic adrenal gland injury was significantly higher than 106 samples of reference dolphin carcasses that were not exposed to the oil spill (Venn-Watson et al. 2015).
The limited evidence for biological impacts from ingested oil varies among pinniped species. In the North Sea, ingestion of oil was the primary cause of death for grey seals found with oil in their mouths, stomachs and intestines (Jenssen 1996). Following the Exxon Valdez oil spill, brain lesions in harbour seal carcasses were caused by oil exposure and lead to observed disorientation and lethargy (Loughlin 1994), apparently due to damaged nerve cells caused by C5–C8 hydrocarbon toxicity. It was suggested that in the days immediately following the Exxon Valdez oil spill, concentrations of volatile hydrocarbon compounds in the air over the slick were ~9 ppm (Frost et al., 1994).
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3.2 Toxicity associated with inhalation Inhalation of specific volatile organics is known to cause respiratory irritation, inflammation or emphysema in marine mammals (Marine Mammal Commission 2011). In other mammals, PAH inhalation irritates airways, causes peribronchial inflammation and systemic toxicity and damages epithelium and cilia, which can then severely impair immune defences (Venn-Watson et al. 2015). However, the severity of volatile hydrocarbon vapour inhalation is particularly concerning for marine mammals based on their respiratory anatomy and functions. The proportion of total lung capacity of marine mammals is substantially larger than terrestrial mammals. In one breath of a terrestrial mammal, the volume of air inhaled and exhaled is approximately 10–15% of the animal's total lung capacity, which is remarkably smaller than the 75–90% volume of air exchanged in one breath of a marine mammal (Wartzok 2002). Furthermore, adaptations to their deep-diving, aquatic behaviours increase the potential for prolonged and amplified exchange between air-borne contaminants and circulatory systems, particularly: 1) the lack of nasal cilia to filter air prior to reaching the lungs; and 2) long breath holds following deep inhalations, which increase injuries and infections to deeper lung tissues (Venn-Watson et al. 2015).
From a histological evaluation of 46 fresh dead bottlenose dolphin carcasses linked to Deepwater Horizon oil spill, 10 dolphins had primary bacterial pneumonia, which either caused or contributed to the animal's death (Venn-Watson et al. 2015). The primary bacterial pneumonia found was significantly more prevalent and more severe than pneumonia found in reference dolphin samples collected elsewhere. Scientific evidence confirmed that high levels of PAHs associated with the oil spill were found in the visibly-oiled marine environment in which bottlenose dolphins were observed swimming and feeding, thus increasing the likelihood that volatile PAHs were inhaled (Venn-Watson et al. 2015). Therefore, the bottlenose dolphins' inhalation of PAHs likely compromised their immune responses and increased the risk of acquiring primary bacterial pneumonia.
Both physiological and behavioural effects result from inhalation of toxic compounds by pinniped species. Following the Exxon Valdez oil spill, concentrations of volatile hydrocarbons over the oil slick contained sufficient levels to cause narcosis and death (Jenssen 1996). Inhalation of toxic fumes resulted in brain lesions, stress and disorientation, which killed 302 harbour seals (Peterson et al. 2003). Additionally, the harbour seals exhibited abnormal behaviour resulting directly from caused by hydrocarbon toxicity (Jenssen 1996). 3.3 Ingestion of contaminated prey Chronic exposure to toxic hydrocarbon may result from ingesting prey with hydrocarbon bioaccumulation. Following the Exxon Valdez oil spill, toxic oil persisted in intertidal zones with coarse gravel and rocks, which also inhibited degradation and weathering processes from wave exposure (Peterson et al. 2003). Mussel beds trapped oil and presumably provided a consistent entry point for oil into the marine tropic system, and abnormal development was observed in herring and salmon, both common marine mammal prey species in that region. Marine mammals are capable of detoxifying and eliminating petroleum hydrocarbons (Fair et al. 2010). However, PAHs may escape metabolisation and persist in low concentrations in marine mammals, presumably from consuming contaminated prey (Holsbeek et al. 1999). Thus, effects of chronic and low levels of oil contamination by consuming prey with accumulated toxic compounds vary depending on the toxic levels within the contaminated prey, as well as the species' ability to metabolize the compounds (Jenssen 1996).
APPEA: Marine Mammals 11 4. Capacity for Recovery
On an ecosystem level, the evidence for recovery from an oil spill exposure is controversial and conflicting. Seventeen years following the Exxon Valdez oil spill, a literature review of over 20 valued ecosystem components included primary producers, filter feeders, fish, birds, mammals, biogeochemical processes and habitat mosaic and wilderness quality (Harwell & Gentile 2006). The authors assessed the ecological significance of changes to structure, function and health of the system and determined that the ecosystem effectively recovered from oil spill impacts, except for one killer whale pod and one sea otter subpopulation, the decline of which was most likely influenced by long-term population dynamics and the species’ intrinsic, slow recovery rate. However, this is in stark disagreement with other published scientific data confirming postponed recovery from persistence of toxic oil, chronic exposure to wildlife, delayed population reductions and cascades of indirect effects (Peterson et al. 2003).
For marine mammal species, one challenge in determining the consequences and recovery from an oil spill is understanding that observed deaths may represent only a fraction of the total mortality. The appropriate spatial and temporal scales to assess the impacts of acute events (e.g. direct contact with oil) are further complicated by long-term, chronic effects (e.g. habitat degradation) and a lack of population-specific information (Williams et al. 2011). Impacts observed immediately following a spill event may deceptively underestimate true consequences, and marine mammal carcasses may decay, sink (i.e. whale fall), drift away or be preyed and scavenged upon by other fauna species. Following the Deepwater Horizon oil spill, 140 dead marine mammals were found as well as numerous dolphin stranding events (Barron 2012). Based on historical carcass-detection rates for 14 cetacean species in the northern Gulf of Mexico, preliminary estimates suggested that the actual marine mammal mortality was potentially up to 50 times greater than the number of carcasses actually recovered (Williams et al. 2011). Similarly, the large number of observed deaths from the Exxon Valdez oil spill most likely represented a fraction of the actual mortality that occurred (Estes 1991).
Recovery from exposure to an oil spill will vary among different species, different populations of the same species and even different individuals within the same population. For killer whales in Alaska, population decline was observed within the first few years following exposure to the 1989 oil spill of the Exxon Valdez, and recovery has not since achieved pre-spill population abundance levels, in part due to the loss of reproductive and/or juvenile females, long life spans and social organisation of discrete pods without genetic mixing (Matkin et al. 2008). Suggested contamination routes in that case were acute exposure to and toxicity from crude oil and chronic exposure from consumption of oiled harbor seals (their preferred prey species). Up to six months following the spill, killer whales were photographed swimming in oil slicks. Although there was no biological evidence that directly linked toxic oil exposure to the unprecedented and timely population decline, long-term population declines are complex and may persist several years after an unplanned discharge event.
Marine mammal recovery thresholds from exposure to oil spills do not exist, and it is impossible to determine the long-term, sub-lethal impacts with which surviving animals are burdened. PAHs are ubiquitous environmental contaminants that may enter the marine environment from both natural (e.g. fires, petroleum seeps) and anthropogenic sources (e.g. petroleum spills, coal and wood burning, combustion of fossil fuels), with an estimated 1.3 million metric tons of PAHs released annually (National Research Council 2003). In general, PAHs are unlikely to have negative impacts upon marine mammals, as they are capable of metabolizing hydrophobic compounds. While PAH
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chemicals can interfere with individual fitness and survival on multiple levels, PAH concentrations are often found in free-swimming marine mammal species. Disentangling background levels from those resulting from a specific exposure is complex. Low but detectable levels of PAH were detected in the muscle, liver, kidney and blubber of sperm whales that stranded in the North Sea, the occurrence of which was not attributed to their apparent stranding event (Holsbeek et al. 1999). In the Mediterranean Sea, blubber biopsies from free-swimming fin whales and striped dolphins produced detectable PAH concentrations, some of which were attributed to crude oil spilled from tankers two years prior to sample collection (Marsili et al. 2001). PAH concentrations were also detected in blubber biopsy samples from bottlenose dolphins from the USA (Fair et al. 2010) and the Canary Islands (García-Alvarez et al. 2014). In Argentina, PAHs were identified in the blubber, fur, blood, liver and faeces of Southern sea lions, and high concentrations of carcinogenic PAH were found in animals from areas heavily polluted by petroleum (Marsili et al. 1997). Biopsy samples from three estuaries in the Great Barrier Reef, revealed evidence of PAH and organochlorine compounds accumulation in Indo-Pacific humpback and Australian snubfin dolphins (Cagnazzi et al. 2013). In that study the most abundant PAHs were those with lower molecular weight, the most water-soluble and therefore the most bioavailable (Cagnazzi et al. 2013).
In most of these results, the PAH content corresponded to a low toxicity profile, since most of the carcinogenic PAHs belong to the high molecular weight compounds (García-Alvarez et al. 2014). However, comparisons of these results are not possible as each study used different analytical methods, and reliable thresholds values for PAHs have not been proposed (Cagnazzi et al. 2013). Impacts from oil compounds are complex and contingent on the composition, prevailing environment conditions and sensitivities of the receptor species. Individual animals respond differently to pollutant stressors based on their biological and life history parameters (e.g. such as age, sex, diet, habitat, metabolism, parturition and lactation). Furthermore, unlike most organohalogenated compounds, PAHs are efficiently metabolized, and any evidence present in a given moment will reflect only recent exposure at the time of sampling (García-Alvarez et al. 2014). Without evaluating the reproductive success, health status and toxicological studies, the long-term impacts of exposure to PAH compounds in the marine environment can only be guessed for wild marine mammal populations.
The capacity for marine mammal recovery following an oil spill event will depend on the cumulative impacts on surviving individuals whose health was compromised by the initial exposure to toxic hydrocarbons. Subsequent toxic exposure of an unplanned discharge may further compromise health of animals that are weak and deficient due to depleted food resources, bacterial infection or environmental stressors. After the first bottlenose dolphin calving season following the Deepwater Horizon oil spill, an unusual number of near-term and neonatal calf mortalities occurred in the northern Gulf of Mexico, and observational evidence identified possible associations between the timing of the oil spill event and unusual environmental disturbances from extreme cold weather (Carmichael et al. 2012).
5. Conclusions
Marine mammals are subject to various levels of environmental stressors, and exposure to toxic petroleum compounds may increase susceptibility to other life-threatening illnesses and mortality. Habitats of high biological significance and vulnerability should be considered for additional protection against potential spills. Finally, more research is required following spill events, especially to understand long-term impacts from dispersant and oil mixes.
APPEA: Marine Mammals 13 6. References
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