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A widespread stranding event of Atlantic seabirds occurred along the western coast of the U.S. Atlantic in 2017. One of the most commonly impacted species was the Northern Gannet, Morus bassanus. Here, a small sample (15%) of stranded birds was used to train wildlife rehabilitation professionals through the process of quantitative necropsy, as the cause of the poor condition of birds was investigated. All birds had intestinal lesions (100% prevalence) that appear to have resulted as the tissues of the gut had been weakened from an accumulation of bile salts. While investigating the possibility that gannet strandings were related to infections of helminthic parasites, evidence of consumption of microplastic pollution, bile salt accumulations (associated with malnutrition), and an enterolith were observed. Infections of the 6 species of helminthic parasites observed here are not suspected to have been the underlying cause of the gut dysbiosis, because while they were present (mean prevalence = 40% ±14% SE), they were not abundant (mean intensity = 9 ±5 worms per host). However, the role of parasitic worms in the exacerbation of damage and facilitating secondary infection cannot be eliminated. Plastic pollution was found either on the external surfaces (100% prevalence) and/or in the gut (75% prevalence) of every gannet, and along with biological causes like starvation and protozoan parasites (malarial agents), could also have contributed to disorders of malabsorption in the small intestine. These findings, while cursory, provide insight into multiple factors that are likely to have contributed to the poor condition of the stranded birds.
Seabirds are considered sentinels of ecosystem change in oceanic systems, and while unexplained morbidity and mortality of an individual may not be indicative of widespread problems in the ocean, stranding events where many seabirds are found dead or dying is cause for alarm. In 2017, a stranding event occurred off the New England coast of the United States, and between the months of May and November, 52 Northern Gannets (Morus bassanus) were found alive but in a weakened state on the coast of Cape Cod, Massachusetts, USA. We processed a subsample of those birds to investigate potential underlying causes of beached birds, knowing that previous assessments of gannet stranding patterns indicate non-food-web-linked phenomena (oiling or entanglement in fishing gear) as major causative agents.
Northern Gannets (Suliformes: Sulidae) are plunge-diving seabirds that feed on commercial fish species along the continental shelves of the Atlantic Ocean, inhabiting territories of multiple countries. Some of their food items can transmit parasitic infections, that are well-described, but poorly quantified. This is not only a risk for adult seabirds: while provisioning chicks, adults can pass parasites and pathogens to their young. Trophically transmitted parasites are reported to infect the digestive tract, respiratory, and renal systems. While morbidity is not frequently associated with parasitic infections in high trophic level avian species and infection rates are documented in sulid seabirds exceeding 3,000 worms per host, in some cases, helminthic parasites (trematodes, cestodes, acanthocephalans, and nematodes) infecting the digestive tract produce pathogenic symptoms. Infections in the trachea and lungs (nematodes) can be problematic in animals where breath control limits foraging success (i.e., plunge-diving and pursuit-diving birds and mammals). Protozoan and trematode infections of the kidneys can reduce renal function, ultimately leading to renal hypertrophy, tubule dilation and ulceration, kidney failure, and death. Thus, quantitatively cataloging parasitic infections of seabirds not only provides insights into the infectious agents their food sources contain, but we can also use these records to better understand how frequently parasitic infections contribute to stranding events of international significance.
In addition to parasites, seabirds can ingest plastic marine debris while foraging. Plastic pollution has emerged as ubiquitous in every ecosystem where it has been searched for. Large plastic debris (macroplastic) is dangerous to wildlife for its physical effects in blocking digestive tracts and mechanical damage to internal tissues. Most commonly reported are small pieces called microplastics: fibers and pellets in the micron to millimeter scale. Plastics that enter the digestive tract of wildlife have the potential to leech chemicals that can impact the animal's health through endocrine and reproductive disruption. Biofilms that form on the surfaces of plastics also attract additional contaminants in the water, like heavy metals and persistent organic compounds, further increasing the potential of consumed plastics to negatively impact wildlife populations. As contaminants that enter the digestive system are directly exposed to the microbiome, consumed plastics can also impact digestive efficiency. One impact of gut dysbiosis includes a change in the ability of the intestine to properly absorb nutrients and to resorb metabolic substances. Lessons learned from stranded wildlife that have consumed plastics can be important in predicting and preventing human diseases associated with these contaminants.
The objective of our study was to better understand what role parasitic organisms might play in strandings of wildlife and whether higher prevalences of parasites or consumed microplastics correspond with injuries and the diminished health of gannets in 2017 could have contributed to their strandings. A secondary objective was to train wildlife rehabilitation professionals and undergraduate students on the techniques of quantitative necropsy, where all major organ systems are systematically assessed for tissue disorders (using light microscopy) and searched for parasitic organisms.
6 endoparasites were found infecting the gannets processed for gastrointestinal parasites: Stephanoprora sp. (Trematoda: Echinostomatidae), Cryptocoytle sp. (Trematoda: Heterophyidae), Diplostomum sp. (Trematoda: Diplostomatidae), Tetracladium sp. (Trematoda: Heterophyidae), and Contracaecum sp. (Nematoda: Anisakidae). In addition, we recovered at least one genus of tetrabothriid cestode that we suspect are Tetrabothrius sp.; however, the scolexes and strobila were too degraded for identification to genus. Endoparasites were ubiquitous with intensities ranging from a singleton infection to 102 parasites in a single host (Suppl. Table 2). Compared to assessments of related host species, where thousands of renal trematode infections were observed, the endoparasite infection intensities observed here are lower than might be expected with a mean intensity of 11.2; however, quantitative reports of Northern gannet infection intensities are generally lacking, so it is possible these infection rates are consistent with typical infection loads. None of the non-digestive organs (kidneys, lungs, trachea, spleen) were infected by helminthic parasites; however, the spleen of one bird showed signs of an apicomplexan infection (Fig. 1A). While parasites were recovered from each gannet assessed (100% overall prevalence), we do not propose that they were the underlying cause of widespread morbidity considering their low intensities and limited evidence that the taxa recovered here are in any way pathogenic in gannets.
Pectinopygus bassani, Eidmanniella pustulosa, Morinyssus simplex, and ticks were recovered from the washed skin and feathers (Fig. 1B & Suppl. Table 2). Observation of the skin and feathers revealed heavy feather molting of nearly all birds, with numerous growing body feathers with very little subcutaneous fat occurring over the breasts. Although there were feather anomolies, we observed no evidence of skin irritation for any of the stranded gannets. Thus, despite relatively abundant ectoparasite intensities (mean infection = 205 ±146 SE), we do not suggest ticks or feather lice contributed to their hosts’ diseased states.
All birds assessed in this survey were under-conditioned, with little to no subcutaneous fat, and atrophy of the pectoral muscles, suggesting each individual was in some state of starvation and malnutrition. The stomachs of all birds were empty despite having digestate within the intestine. The intestinal contents of one bird were predominantly digested fish, squid (beaks) for another, and the remaining birds had no identifiable food items with the exception of algal holdfasts. Algae was found in all birds that we processed. Some birds had successfully fed while being rehabilitated, and there was plentiful digestate in the intestines of each bird. With the exception of the aforementioned undigested algal, bone, and beaks of prey, the components of the digestate were indiscernible.
Host Organ Assessment
Lesions and tears were noted in the stomach, esophagus, or small intestine of every bird; however, the parasites observed here are not typically associated with intestinal damage to the extent observed. The gut of each bird assessed contained substantial bile pigment and bile salts, leading to staining of digestate throughout the small intestine. Because excessive bile release can be a by-product of starvation, we suggest that the inability to successfully feed was a strong contributor to the stranding event. Birds in rehabilitation had been fed ad libitum for 24–48 h prior to their expiration, thus, starvation-associated accumulation of bile salts could have been treated during their brief rehabilitation period. However, if the degree of bile production was severe, the condition could have persisted in the intestine even after sufficient food was taken. We also suggest that malabsorption of bile salts by damaged ileal epithelial tissues (that could lead to enterocolitis and acute necrosis) also contributed to the condition of the stranded seabirds. Consequently, weakened tissues of the gut lumen from bile accumulations could have been more easily damaged by helminthic parasites adhering to the gut wall. Thus, we suggest the combination of starvation, malabsorption issues with bile accumulation, and parasites likely exacerbated the ubiquitous (100% prevalence) extent of the lesions observed. Finally, we suspect catastrophic damage to these tissues resulted from physical blockages of the gastrointestinal tract.
Two birds of particular interest provide additional insight into the diseased conditions of the gannets, although we were not able to confirm that their maladies were not also present in other birds. One bird likely suffered from avian malaria (Apicomplexa), as it presented with an enlarged and distended spleen that was full of damaged red blood cells (Fig. 1A). In contrast, the spleens of all other gannets assessed here were small and exhibited no signs of inflammation or disease. While malaria infections are not typically fatal in birds, as secondary infectious agents, apicomplexans that attack red blood cells can lead to accumulations of ruptured blood in the liver and spleen, subsequent liver failure, and bile production problems – as the liver mediates bile synthesis and recycling. The second bird of interest had a blocked cloaca with a pasty and internally hardened enterolith or ‘cloacalith.’ This effectively prevented the elimination of digested products (and parasite eggs) through typical peristaltic activity. With the exception of this individual, all birds processed here experienced diarrheal ‘blow out’ events, and while the cloacaliths were not actively sought out following the discharge, it is possible that enteroliths were more common than we report. All birds experienced these events and all had substantial tearing of the intestinal epithelium and we suspect the clearing of intestinal blockages could have caused the damage (or worsened it) that we observed in the digestive systems of stranded gannets.
Enteroliths form from bile salt accumulations in the gastrointestinal tract and can lead to blockages of diverticula and intestinal sections, fistula, and secondary infections. All birds assessed here exhibited bile pigment staining in the stomach, duodenum, and jejunum (80% of subjects) and/or excessive bile salt accumulation (80% of subjects). One cause of bile salt accumulation is the overproduction and underuse of digestive components during times of starvation. Another factor that can lead to accumulation is the damage of epithelial tissues that reabsorb bile salts within the ileum. Malabsorption can result from protozoan parasite infections and through disruptions to the bacterial composition (the microbiome) of the gut. Only one bird examined here exhibited cloacaliths; however, all gannets had excessive bile coloration in their digestate, and the gastrointestinal tract of all birds assessed with quantitative necropsy (100% of subjects) experienced intestinal damage. Thus, it is possible that they had already cleared their enteroliths and we were simply observing the aftermath of those clearances.
Interestingly, many but not all (75% of subjects), birds had consumed plastic pollution, and all that were externally washed (100% of subjects) had long linear fibers of plastic on their feathers that had presumably been floating in the ocean (Fig. 1B). Consumed microplastic particle intensity ranged from 2–4 plastics per bird (mean=2.7), and external plastic intensity ranged from 35–116 particles per bird (mean=62). There is limited evidence because it has yet to be studied in-depth, that environmental plastic contaminants interfere with metabolic and physiological systems in wildlife. Environmental contaminants can alter the microbiome of wildlife, effectively changing the ability of the gut to properly absorb nutrients and other metabolic substances like bile salts. Thus, it is important for studies to be developed in order to investigate the possibility and degree to which plastic pollution – and the other chemical contaminants that adsorb to their surfaces, contributes to physiological problems in wildlife.
Here, we assessed a subsample of deceased stranded seabirds for parasites, organ condition through quantitative necropsy, and plastic pollution. The ultimate cause of mortality included intestinal blockage (possibly by enteroliths); however, the underlying cause of accumulated metabolic substances is speculative. We suggest a likely reason for the strandings could have been a combination of starvation and disruption of bile salt reabsorption. Although ingested plastic was not ubiquitous, the feathers and skin of all stranded birds assessed here were covered in plastic pollution and that plastic on the body could have been consumed (perhaps while preening) and lost as intestinal blockages were cleared. Intestinal injuries and blockages associated with marine debris are documented in instances of seabird starvation and it is possible that was also the case here. While parasites were ubiquitous, we found infections of species that were expected based on previous reports of gannets and endoparasites were not abundant. Thus, it is unlikely that parasitic infections triggered the initial injury, although they could have contributed to the fragility of intestinal tissues that were already compromised by bile salt accumulations. Linking parasite ecologists and wildlife rehabilitation experts to study the independent and combined effects they have on wildlife is a worthwhile pursuit.
This study was limited by the number of specimens that could be examined – many birds had been given anti-helminthic treatments, died before making it to the rehabilitation centers, or were successfully rehabilitated and thus, ethically, could not have been included in our assessments.
The swelling and contents of the spleen have not been confirmed as a malarial agent through molecular or histological assessments as our budget precluded us from doing so. Further, a sample of the spleen could not be preserved and downstream confirmation was not possible. We obtained the spleen from the fascia around the proventriculus and gizzard at the interface of the liver and are confident it is not an occlusion or bolus associated with dietary products.
Because some birds were processed during training sessions for ectoparasite washes, quantitative necropsies that include the weighing of organs was not possible for all specimen. Despite an unequal sampling of all systems within all birds (some did not get processed for ectoparasites/external plastics, weights, or parasitology), each assessment was quality assured by professional veterinary and parasitologist faculty and staff and the data presented here are sound.
We stand by our conclusion that metabolic product accumulation in the form of enteroliths contributed to gannet deaths, yet the reason for the accumulation of bile salts could be debated – where some might argue that starvation alone can cause this issue. We suggest that some additional factor(s) must have lead to the weakened state of the birds, like starvation/lack of food for foraging (as these are pelagic birds emigration to productive feeding grounds is likely), starvation because of malabsorption of nutrients (possible if this is an issue in general), ingestion of contaminants (eg., symptoms of heavy metals consumption include wing droop and an overall weakened state), parasitic or viral infections (causing neurological symptoms that interfere with foraging or nutritional deficits). Previous assessments of stranded gannets have indicated that this species is often a victim of oiling and entanglement in fishing gear; however, there was no evidence of those types of events in any of the birds assessed here.
As our marine environments change in their physical, chemical, and biological compositions, it is likely that more and more seabird stranding events will occur. We are actively working to establish additional partnerships to further document the conditions of stranded birds and to evaluate those that cannot be successfully rehabilitated for parasitic infections and microplastic consumption. Our understanding of parasites in the health and condition of long-lived, highly mobile, and difficult to salvage and treat species is limited to descriptive species accounts, and as such, more qualitative assessments are needed so that we can better appreciate how hosts are interacting within ecological systems. Further, more consistent methodologies using quantitative techniques should be employed so that datasets of these species with low sample sizes can be combined for more powerful analyses and holistic perspectives on population status. Samples generated from rehabilitated and 'accidental' fatalities of wildlife (bycatch, window strikes, oil rig collisions, etc.) could provide unique and useful data without the need for lethal sampling; however their ecology (though parasite assessments) should proceed with some caution: Without knowing how many parasites a healthy gannet might have, we cannot even begin to confidently answer ecological questions. Further, it is critical to disentangle the independent and combined effects of parasites and plastics and understand their interactions with one another. As these potentially problematic components of contemporary food webs (parasites and plastics) are not well documented (especially from a quantitative perspective) or understood in wildlife, we strive to fill in these gaps in knowledge.
Seabirds from the Cape Cod area of Massachusetts, USA were found alive floating in the water or washed on the shore and brought to the New England Wildlife Center (South Weymouth, Massachusetts, USA) or the Cape Wildlife Center (Barnstable, Massachusetts, USA) for treatment. In captivity, they were given electrolytes through feeding tubes, supplemental feedings of fish, and some received anti-helminthic and antibiotic medications. All the birds assessed here had fed within 12 h of death and thus, were not expected to show pathologies associated with starvation. Birds used in this survey succumbed after an average of 2.3 days of rehabilitation treatment (Table 1) and were all euthanized after experiencing explosive intestinal clearing (diarrheal ‘blow out’), where bile-rich fecal material burst from the cloaca, or was suspected to have occurred within their treatment holding area. Birds used in this survey stranded between the months of May and September 2017.
To ensure that we could evaluate the potential roles of parasites in the strandings of Northern Gannets, samples processed for this survey were limited to individuals where medical intervention would not have interfered with parasitic assessments. Because birds that were already deceased, euthanized or injured in the field had a potential for accelerated decomposition, only birds that were successfully transported whole and alive were considered for inclusion in this survey. Candidate birds 1) were alive when recovered by rehabilitation staff or animal control agents for the Commonwealth of Massachusetts, USA, 2) were euthanized within 48 h of collection (Suppl. Table 1), 3) did not receive anti-helminthic treatments before death, and 4) were frozen immediately following death. These restrictions limited our sample size to 8 of 52 (15%) of the birds that stranded on Cape Cod, Massachusetts, USA that year.
We used some of the birds to train rehabilitation staff at the Cape Wildlife Center and undergraduate students enrolled in a course on methods in wildlife parasitology. Consequently, each bird received a different combination of examinations (Suppl. Table 1): 5 birds (10% of stranded birds) received intestinal assessments - where assessed endoparasites and consumed plastic pollution within their gastrointestinal tract was documented, 4 birds (7% of stranded birds) received quantitative necropsy - where major organ systems were removed and systematically weighed, and 6 birds (11% of stranded birds) received external assessments - where the body was washed of its ectoparasites and external plastic contaminants. Organ samples that we processed consisted of gastrointestinal tracts (esophagus, proventriculus, ventriculus, duodenum, jejunum, ileum, caeca, colon, and cloaca), spleens, kidneys, tracheas, and lungs.
Prior to necropsy or intestinal removal, the cloaca, mouth, and nares were closed by tape and the outer surfaces of each seabird (skin and feathers) were washed with dish detergent. Any ectoparasites and other debris were collected in a 50-micron sieve and preserved in 70% ethanol for the later assessment using stereoscope microscopy at 8–40x magnification (AmScope SM-1BS).
During quantitative necropsy, all major organ systems mentioned above were removed, assessed for injury and degradation of tissue condition (using squash plate methods under 8–40x magnification), and weighed. Because the weight of birds is not indicative of body condition, whole-body weight was is not used for condition assessments. No differences in organ weight were detected with the exception of one bird with an enlarged spleen (Fig. 1A).
Gut contents from the lumen of the esophagus, stomach, small intestine, colon, and cloaca were removed by scraping the epithelial tissue with a glass slide and observing the tissue under a stereoscope (8–40x magnification) for embedded parasites. The trachea was cut longitudinally and the lumen observed for the presence of nematode parasites under a stereomicroscope. Kidney and lung tissues were subsampled and pressed between two panes of glass to inspect for the presence of metazoan parasites. Any helminthic parasites were identified using taxonomic keys by our parasitological faculty to the lowest taxonomic classification.
This study was supported financially through an NOAA Sea Grant Rapid Grant, sub-award A101366 under prime award FAIN NA14OAR4170074.
This research was made possible through the cooperation of the Cape Wildlife Center and the New England Wildlife Center. Medical care was provided by wildlife center staff, sample confirmation and processing of parasites and plastics occurred at the New England Wildlife Center and Frostburg State University.