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.