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12-6-2018 The elr ationship of endoparasite diversity and feeding ecology in the seabird complex of South Florida Michael Nakama Nova Southeastern University, [email protected]

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NSUWorks Citation Michael Nakama. 2018. The relationship of endoparasite diversity and feeding ecology in the seabird complex of South Florida. Master's thesis. Nova Southeastern University. Retrieved from NSUWorks, . (500) https://nsuworks.nova.edu/occ_stuetd/500.

This Thesis is brought to you by the HCNSO Student Work at NSUWorks. It has been accepted for inclusion in HCNSO Student Theses and Dissertations by an authorized administrator of NSUWorks. For more information, please contact [email protected]. Thesis of Michael Nakama

Submitted in Partial Fulfillment of the Requirements for the Degree of

Master of Science M.S. Marine Environmental Sciences

Nova Southeastern University Halmos College of Natural Sciences and Oceanography

December 2018

Approved: Thesis Committee

Major Professor: David W. Kerstetter, Ph.D.

Committee Member: Christopher A. Blanar, Ph.D.

Committee Member: Sean Locke, Ph.D.

Committee Member: Bernhard Riegl, Ph.D.

This thesis is available at NSUWorks: https://nsuworks.nova.edu/occ_stuetd/500 Nova Southeastern University Oceanographic Center Halmos College of Oceanography and Natural Sciences

The relationship of endoparasite diversity and feeding ecology in the seabird complex of South Florida

By Michael Yoshio Nakama

Submitted to the faculty of the Nova Southeastern University Oceanographic Center Halmos College of Oceanography and Natural Sciences in partial fulfillment of the requirements for the degree of Master of Science with a specialty in:

Marine Environmental Sciences

December 2018

Acknowledgements I extend my sincerest appreciation to my committee members, Drs. David W. Kerstetter, Christopher Blanar, Sean Locke, and Bernhard Riegl for their continued support and mentorship throughout my thesis research. I thank my fellow lab mates and volunteers for their assistance with dissections, laboratory processing of samples, and seabird collections. A special thanks goes to my lab mates Brittany White, Caitlyn Nay, and Sarah Gumbleton for providing invaluable advice and resources for the progression of my research, and their continued support of pursuing higher educaiton. Finally, I would like to express a wholehearted thank you to my family, especially my mother and sister, and friends for the encouragement and support in completing my Master of Science degree. This project was made possible through the Title V Promoting Postbaccalaureate Opportunities for Hispanic Americans Program (PPOHA) – January 18, 2014 to October 31, 2015. The funding from Title V-PPOHA provided the opportunity to work as a research assistant conducting studies for a thesis Master of Science degree. Funding for the collection of specimens from the four wildlife rescue agencies (and other opportunistic collections), including required state and federal permits (FWC permit LSSC-12-00075 and USFWS permit MB8290-A-0), was provided by a FY2014 PFRDG award to D.W. Kerstetter and A. C. Hirons. Funding for the collection, identification, and preservation of specimens from host species, such as the Amscope dissection microscope and chemicals, was provided in part by a FY2015 PFRDG to C.A. Blanar. Last, I would like to thank Halmos College of Natural Sciences and Oceanography for providing a Teaching Assistant scholarship from Fall 2016 to Winter 2018.

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Abstract Endoparasite community structure has been poorly studied in migratory birds, particularly among the seabirds of south Florida. We examined parasite communities in seven south Florida seabird species: brown pelican Pelecanus occidentalis (n=33), northern gannet Morus bassanus (n=31), double-crested cormorant Phalacrocorax auritus (n=33), osprey Pandion haliaetus (n=27), royal tern Thalasseus maximus (n=30), herring gull Larus argentatus (n=12), and laughing gull Leucophaeus atricilla (n=40). We identified 33 parasitic helminth species: 6 nematodes, 2 cestodes, 3 acanthocephalans, and 22 digeneans. Subsequent pairwise tests and similarity profile analysis identified four distinct clusters with similar parasite community structures: (1) pelican and gannet; (2) cormorant; (3) osprey; and (4) tern and both gull species. The mean infracommunity observed species richness differed among the several seabird host species with the highest observed values in pelicans (5.7±0.4) and gannets (5.1±0.4), while the lowest values were seen in herring (0.8±0.7) and laughing (0.4±0.4) gulls. RELATE analyses indicated that the factors of host phylogeny (Rho=0.564, p=0.017), host feeding range (Rho=0.553, p=0.005), and host feeding technique (Rho=0.553, p=0.039) were significant and had similar magnitudes of effect on the structure of observed parasite communities within the several seabird species of this study. Host prey preference was not significant from the RELATE analyses (Rho=0.124, p=0.278), suggesting that preferred prey items of the several seabird hosts had a negligible impact in the structuring of parasite communities. From our results, host phylogeny and host feeding ecology are important driving factors of parasite community composition and structure of these south Florida seabirds, while host prey preference had little influence on parasite communities.

Keywords: Feeding ecology, seabirds, parasites, host species, species richness, Pelecaniformes, Suliformes, Accipitriformes, Charadriiformes

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Table of Contents Acknowledgements ...... ii Abstract ...... iii List of Figures ...... v List of Tables ...... vi Introduction ...... 1 Feeding Ecology ...... 1 Host-Parasite Trophic Interaction ...... 4 Life history and Host-Parasite Interaction of Studied Species ...... 9 Purpose and Objectives ...... 15 Materials and Methods ...... 15 Sample Collection ...... 15 Laboratory Processing...... 16 Helminth Identification ...... 17 Data Analysis ...... 18 Results ...... 19 Discussion...... 28 Host Species ...... 28 Feeding Ecology ...... 31 Future Research ...... 33 Conclusion ...... 34 References ...... 36 Appendix 1 ...... 48 Appendix 2 ...... 63 Appendix 3 ...... 80

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List of Figures

Figure 1. Foraging techniques of seabirds ...... 2

Figure 2. Feeding range and depth of seabird species ...... 7

Figure 3. Shade plot of parasite abundance in seabird species ...... 24

Figure 4. Non-metric multi-dimensional scale of parasite communities based on seabird hosts ...... 25

Figure 5. Non-metric multi-dimensional scale of parasite community similarity for infracommunities in individual birds ...... 26

Figure 6. 2STAGE non-metric multidimensional scale of similarity matrices compared to fourth root parasite centroids ...... 27

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List of Tables

Table 1. List of host species and feeding ecology ...... 8

Table 2. Community analysis of common marine-associated birds in south Florida ...... 22

Table 3. RELATE analyses of seabird hosts ...... 23

Table 4. Prey items of Pelecaniformes ...... 48

Table 5. Prey items of Suliformes...... 49

Table 6. Prey items of Accipitriformes ...... 53

Table 7. Prey items of Charadriiformes ...... 56

Table 8. Previously recorded parasite species of Pelecaniformes ...... 63

Table 9. Previously recorded parasite species of Suliformes ...... 66

Table 10. Previously recorded parasite species of Accipitriformes ...... 69

Table 11. Previously recorded parasite species of Charadriiformes ...... 71

Table 12. Parasite species diversity of targeted seabird species ...... 75

Table 13. Resemblance matrix values for host phylogeny ...... 76

Table 14. Resemblance matrix values for host feeding range ...... 77

Table 15. Resemblance matrix values for host feeding technique...... 78

Table 16. Resemblance matrix values for host prey preference ...... 79

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Introduction

Marine avifauna, colloquially termed “seabirds,” play a vital role in the functioning of marine ecosystems. As opportunistic and highly vagile predators, seabirds have a substantial impact within these environments, most notably on the available prey items of both vertebrate and invertebrate species found in oceans, seas, shorelines, and intertidal areas (Furness and Monaghan, 1987). These foraging areas are selected based on the abundance of suitable prey items where eutrophic waters support such high prey densities, although foraging can also occur in oligotrophic waters in areas such as the Florida Keys and Greater Caribbean. Due to highly abundant prey items in these environments, competition between seabird species often leads to different feeding strategies (Figure 1), such as plunge diving, for optimizing the chance of success when foraging. Consequently, feeding strategies result in the foraging of a diverse array of available prey species in various, marine ecosystems by seabirds.

Feeding ecology

Foraging range and prey preferences are generally tailored by the abiotic and biotic conditions present within the ecosystem (e.g., prey availability and abundance, competition between foragers within the same trophic level, depth of water column, and temporal and spatial variation), which often result in direct competition between foragers within the same environment for available resources. These interactions result in specialization among foragers, who effectively form trophic guilds to minimize competition (Figure 2). Seabirds are generally categorized into three distinct groups of feeders: inshore, coastal, and offshore (pelagic) (Clapp et al., 1982; Clapp et al., 1983; Shealer, 2001). These categories are somewhat overly simplistic, as seabirds are opportunistic feeders and will frequently cross boundaries among these three habitat types in search of adequate food sources (Shealer, 2001). As mentioned by Sukhdeo and Hernandez (2005), food availability has a pivotal role in ecology: (1) as a factor that is the biggest part of an organism’s life and (2) the connecting link between members within the community (see Elton, 1927 for detailed feeding strategies).

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Figure 1. Various foraging techniques used by seabirds when hunting for prey items. Foraging techniques include which seabird species use them in marine habitats. The three common foraging techniques include surface skimming, plunge diving, and pursuit diving, which are used by a variety of avian species. As illustrated, larid species (gulls and terns) primarily use surface skimming techniques for prey items located near the surface of waters, while northern gannets use plunge diving for prey items located at surface waters to depths reaching 22 m. Double-crested cormorants primarily use pursuit diving to capture prey items and can dive as far as 25 m underwater. Brown pelicans and ospreys use a variety of techniques such as plunge diving and surface skimming that extend as far as 1 m underwater (from Nelson, 1979).

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Foraging techniques are specialized strategies utilized by organisms when searching for food to optimize the chance of success. For seabirds, developing various foraging techniques is essential for efficiently gathering food sources while minimizing the effect of interspecific competition with other seabird species (Marini et al., 2017). Simple strategies such as surface dipping for bait fish to more complex and specialized techniques, such as plunge diving, are used to capture prey items of various habitats. For example, brown pelicans use plunge-diving as their primary method of feeding; however, they are also inclined to scoop-feeding as well as kleptoparasitism (Clapp et al., 1982). Double-crested cormorants feed primarily by diving from the surface and chasing prey underwater with the use of their feet for propulsion but have been known to search along the bottom for prey for 30-70 seconds. Northern gannets use plunge diving tactics to secure prey items up to an average of 19.7 m depths (Brierley and Fernandes, 2001), as well as pursuit dive and surface seize behaviors (Clapp et al., 1982). Both herring and laughing gulls share similar foraging strategies when searching for suitable food sources, which include surface seizing, dipping, kleptoparasitism, and scavenging (Clapp et al., 1983). Royal terns use dipping, plunge diving, and kleptoparasitism when foraging for food, primarily shrimp and shallow-water schooling fishes. In general, foraging ranges of seabirds are variable based on the time of year (i.e., breeding versus non-breeding season) and availability of prey items. Per Clapp et al. (1982, 1983) and Shealer (2001), pelicans, gulls, terns, and cormorants are classified as coastal feeders, as they typically forage within sight of land and sometimes in estuarine areas; however, cormorants and terns have also been categorized as inshore feeders from observations made during foraging and breeding season (McGinnis and Emslie, 2001; Withers, Brooks, and Brush, 2004; Eisenhower and Parrish, 2009). Northern gannets have been observed to travel long distances, usually to the shelf-slope break (submerged offshore edge of a continental shelf) and beyond (up to 540 km offshore), but they forage closer inshore to the nesting site during breeding season (Hamer et al., 2000; Shealer, 2001; Pettex et al., 2012). Finally, ospreys usually forage around their established nesting site, typically the surface waters of lakes, streams, and rivers as well as estuarine habitats (Bent, 1937; Evans, 1982). This variety of foraging habitats leads seabirds to consume both freshwater and marine fish, along with other local vertebrate and invertebrate prey.

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The predator-prey trophic interactions of these foraging areas also allow seabirds to serve another important ecological role: as hosts for the parasites inhabiting the local prey items.

Host-parasite trophic interaction

Parasitism can be defined as the biological interaction (i.e., a symbiosis) where one species (the parasite) lives in close association with the other (the host) deriving some benefit (e.g., transportation and food) while causing some degree of harm to the host (Rohde, 2013). Some parasite species can reduce the fitness of their hosts by decreasing the chance of survival and reproduction. The regulation of host populations can in turn modulate energy flow within food webs and ecosystems (Lafferty and Morris, 1996; Loreau, Roy, and Tilman, 2005; Lafferty et al., 2008). Parasites have evolved life-history strategies that maximize transmission to their hosts, by fine-tuning the timing of their dispersal, increasing or decreasing the degree of host specialization, adopting alternate modes of transmission, and altering their life-cycle complexity and population structure (Levin and Parker, 2013). For parasites with multi- host life cycles, long-term ecological stability must exist among hosts and between hosts and their environment before establishment and specialization can occur (Marcogliese and Cone, 1997; Marcogliese, 2004; Sukhdeo and Hernandez, 2005). Several studies (e.g., Sukhdeo and Hernandez, 2005; Kuris et al., 2008) have examined the relationship between parasitism and food web dynamics, demonstrating that parasites contribute significantly to the biomass pyramid as consumers. However, studies of food web dynamics often ignore parasitism even though it is a common strategy used by 50-70% of species worldwide (Price, 1980). The addition of parasites into food webs can provide insight into the complexity of predator-prey interactions that occur within every ecosystem (predators and the prey consumed), which can provide a better understanding of trophic links between organisms within ecosystems as total parasite diversity is driven by factors favoring transmission, rather than being randomly distributed in food webs (Marcogliese and Cone, 1997; Lafferty et al., 2008; Sukhdeo, 2010; Locke et al., 2014).

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The study of host-parasite relationships can provide insights on the condition of ecosystems and trophic relationships among species (Marcogliese and Cone, 1997; Marcogliese, 2004; Hudson et al., 2006). Parasite assemblages can also provide information on prey identity, availability, and distribution of habitats frequented by host species when foraging for food (e.g., Muzaffar, 2009). Interactions between parasites and hosts have been linked to these hosts experiencing strenuous energetic demands, change of behavioral patterns, reduction of fecundity and growth development, alteration to host morphology and appearance, and eventual mortality with prolonged exposure (Marcogliese, 2004; Lafferty et al., 2008). In contrast, the study of parasites provide benefits not only to an assessment of the stability of an ecosystem, but to the understanding of dynamic trophic interactions. Parasite assemblages can reflect the diet of hosts over periods of time from weeks to months, which can detail prey composition, ontogenetic shifts in diet, feeding on one or more trophic levels, shifting of niches due to local competition, feeding specialization of hosts, seasonal changes in diet, and temporary links in food webs (i.e., periodic migrants) (Marcogliese, 2004). However, the factors that drive parasite species diversity remain the subject of intense scrutiny (see Poulin 1997), and are hypothesized to include multiple biotic and abiotic host-driven factors such as the host species’ geographic range, body mass, age, diet, metabolic rate, population density, temperature, and geographic latitudes (Bustnes and Galaktionov, 1999a; Bustnes and Galaktionov, 1999b; Hughes and Page, 2007). Per Locke et al. (2013), parasite communities coupled with host phylogeny had a greater impact on community composition than did the trophic level, diet, habitat usage, or spatial proximity and size of hosts, which highlights the key role that feeding ecology likely plays in influencing parasite communities; however, Kamiya et al. (2014) suggests that for certain taxa of hosts, host species’ traits account for the interspecific variation observed in parasite species richness, though inconsistency among studies using these factors along with low predictive power (i.e., R2) have been observed. Both Kleinertz et al. (2012) and Liccioli et al. (2015) observed greater diversity in parasite communities in localities with higher prey availability and population fluctuations of prey items, since high encounter rates with high abundance allowed increased chances of parasitic infections. These interactions are well documented in studies of both freshwater and

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marine habitats in both vertebrate and invertebrate hosts (Marcogliese, 2004), but relatively little work has been conducted in avian hosts due to federal regulations barring the capture of migratory seabirds under the Migratory Bird Treaty Act of 1918 (Santoro et al., 2012). The hypothesis of this study was that endoparasite faunal diversity differs among the targeted seabird species as a function of their membership in inshore, coastal, and offshore marine avifaunal guilds as well (see Figure 2), and that feeding ecology is significantly correlated with the structure of their endoparasite communities due to those differences in avifaunal guilds (see Table 1 for feeding ecology descriptions of the seven targeted host seabird species) (Locke et al., 2014).

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Figure 2. Conceptual diagram of vertical and horizontal habitat utilization for feeding purposes used by common marine- associated birds in south Florida, including regions of overlap and lagoon waters inshore of barrier islands.

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Table 1. List of host species and feeding ecology: foraging area, distance, and diet. Foraging area indicates general locality of feeding sites near shoreline. Foraging distance is the range seabirds will travel from shore or inland to feed except for seagulls due to an opportunistic diet. Last, diet notes preference of food for the seven targeted seabird species.

Foraging Foraging Avian Hosts Diet Feeding techniques area distance (km) Pelecanus Surface seizing, plunge diving, occidentalis Coastal 32-80 Teleosts kleptoparasitism

Morus Offshor Teleosts, Loligo spp., offal from bassanus 322-483 Pursuit diving, plunge diving e fishing vessels

Phalacrocorax Teleosts, amphibians, auritus Inshore 20 crustaceans, aquatic insects, Pursuit diving vegetation Pandion Teleosts, reptiles, amphibians, haliaetus Inshore 1-5 Surface seizing avifauna

Thalasseus maximus Coastal 50 Teleosts, crustaceans, Loligo spp. Dipping, plunge diving, kleptoparasitism

Leucophaeus Teleosts, crustaceans, insects, Surface seizing, dipping, kelptoparasitism, Coastal 19-120 atricilla avifauna, human garbage scavenging Teleosts, amphibians, reptiles, Larus arthropods, molluscs, Surface seizing, dipping, kelptoparasitism, Coastal 40-90 argentatus echinoderms, avifauna, mammals, scavenging fruit, vegetation, human garbage References: Bent (1937), Clapp et al. (1982), Clapp et al. (1983), Shealer (2001)

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The host species in this study were brown pelican Pelecanus occidentalis, northern gannet Morus bassanus, double-crested cormorant Phalacrocorax auritus, osprey Pandion haliaetus, royal tern Thalasseus maximus, laughing gull Leucophaeus atricilla, and herring gull Larus argentatus. These species were selected primarily for their differences in feeding ecology – a synthesis of preferred foraging habitat and range, dietary niche breadth, and preferred prey is depicted in Figure 3 and Table 1. These seven species occupy middle-to-upper trophic levels within the ecosystem as either inshore or offshore piscivores (brown pelicans, double-crested cormorants, northern gannets, ospreys, and royal terns) or opportunistic, generalist feeders (laughing and herring gulls) (Bent, 1937; Pearson, 1968; Brouwer, Hiddinga, and King, 1994; Montevecchi and Myers, 1997; Withers and Brooks, 2004; Hamer et al., 2007; Isaksson et al., 2016). These species were also chosen because of carcass availability at four collaborating wildlife rehabilitation centers, namely the South Florida Wildlife Center (Fort Lauderdale), the Pelican Harbor Seabird Station (North Miami), the Florida Keys Wild Bird Rehabilitation Center (Tavernier), and the Key West Wildlife Center (Key West).

Life history and host-parasite interaction of studied species (See Appendix 1 for comprehensive list of dietary prey items and Appendix 2 for comprehensive list of previously recorded parasite species of the seven seabird hosts)

Pelicaniformes Pelecanus occidentalis (Linnaeus, 1766) The brown pelican Pelecanus occidentalis is a large, seabird common in eastern North America. Brown pelicans occur along the western Atlantic and Gulf of Mexico coasts from the Carolinas to Florida, the greater Caribbean region, and South America, but have also been observed breeding along the west coast of California (Clapp et al., 1982; Lowe et al., 1990). Brown pelicans are year-round residents of Florida, but there also seasonal migrants (northern populations) that travel south during the winter (Clapp et al., 1982; Forrester and Spalding, 2003). Brown pelicans use plunge-diving tactics for capturing prey items, diving as deep as 1 m, although their spatial range is somewhat limited, as they rarely venture further than 32 km out to sea (Clapp et al., 1982).

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Common prey items are surface-swimming baitfish such as juvenile and adult mullets (Mullidae), herrings and menhadens (Clupeidae), and anchovies (Anchoa spp.). The parasite communities of brown pelicans include a wide variety of marine- based endohelminths: acanthocephalans, digeneans, cestodes, and nematodes. Courtney and Forrester (1974) found 31 helminth species in 113 brown pelicans, including 2 acanthocephalans, 11 nematodes, 14 trematodes, and 3 cestodes. Dronen et al. (2003) found 21 helminth species in ten brown pelicans sampled at Galveston Bay, Texas, with high intensity of Ascocotyle longa (828-12,624), Mesostephanus microbursa (418-9315), and Contracaecum spp. (1-750). Other species previously documented in brown pelicans include Corynosoma sp., Bolbophorus, and Galactosomum spp.

Suliformes Morus bassanus (Linnaeus, 1758) The northern gannet Morus bassanus is a large seabird common to the North Atlantic, spending most of winter at sea and ranging as far south as the greater Caribbean. They are abundant off the Florida Atlantic coast and present in nearshore areas from October to April with populations peaking from November through February (Clapp et al., 1982). Based on observations from Nelson (1978a, 1978b), migration typically ends at the Florida Atlantic coast; however, band tracking has found some populations migrating to the Gulf of Mexico. Northern gannets respond to changes in prey availability and distribution from changing oceanic conditions by increasing foraging efforts or switching to alternative prey items (Pettex et al., 2012). They can exploit a large array of prey such as schooling fish (e.g., menhaden Brevoortia spp. or sciaenid drums) or fishery discards (Votier et al., 2010; Pettex et al., 2012; Fifield et al., 2014). They use plunge- diving to attain depths up to 22 m, and forage as far as 540 km (230 km mean distance) from shore (Hamer et al., 2000). However, foraging is constrained to areas near the nest site during the breeding period, within which the pair’s single chick is fed at relatively short intervals (Pettex et al., 2012). As pelagic piscivores, northern gannets acquire endohelminth communities directly from the available prey items of their foraging range. Parasite communities consist of acanthocephalans, cestodes, digeneans, and nematodes – similar to other

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seabird species. Previously recorded helminths of northern gannets include species such as Galactosomum cochleariformum, Mesostephanus sp., Asococotyle sp., and Contracaecum sp. (Forrester and Spalding, 2003). Wardle et al. (1999) documented species of Bursacetabulus and Bursatintinnabus from northern gannets collected from Galveston Bay, Texas off the Gulf of Mexico.

Phalacrocorax auritus (Lesson, 1831) Double-crested cormorants Phalacrocorax auritus, which includes multiple putative subspecies, are common colonial waterbirds distributed throughout an extensive North American range encompassing Saskatchewan, Canada through the Gulf of Mexico and U.S. Atlantic coast (Wagner et al., 2012). Wintering of this species usually occur for northern populations where migratory routes trail along the Atlantic coast and Gulf of Mexico, although southern, tropical locations may also have resident populations (Clapp et al., 1982). As opportunistic foragers in both freshwater and saltwater environments, double-crested cormorants exhibit spatial and temporal variation in diet that is dependent on the location, season, and availability of prey items (Coleman and Richmond, 2007). Foraging occurs within littoral habitats upon a wide variety of prey items such as benthic or small schooling fishes, crustaceans, and even sub-surface plants (i.e., foraging at diving depths less than 25 m and foraging range of ca. 5-20 km); however, they will feed on the most abundant, largest, or easiest to catch prey (Eisenhower and Parrish, 2009; Withers and Brooks, 2004). As freshwater and saltwater foragers, double-crested cormorants exhibit a wide array of helminth species found in freshwater lakes, ponds, and streams as well as species of coastal habitats such as estuaries and marshes. Like brown pelicans, double-crested cormorants host a wide variety of acanthocephalans, digeneans, cestodes, and nematodes. Threlfall (1982) found 19 helminth species from 76 cormorants collected from both the Gulf and Atlantic coasts of Florida: 8 digenea, 1 cestode, 7 nematodes, and 3 acanthocephalans. Of these species, Hysteromorpha corti (redescribed from the previously accepted name, H. triloba; see Locke et al., 2018), Drepanocephalus spathans, and Contracaecum spp. were the most abundant. Double-crested cormorants from the west coast also harbored more parasite species and greater intensity of infection

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compared to the east coast (Threlfall, 1982). Previously recorded species from double- crested cormorants include Ascocotyle longa, Mesostephanus appendiculatoides, and Andracantha spp.

Accipitriformes Pandion haliaetus (Linnaeus, 1758) Osprey Pandion haliaetus are distributed worldwide and feed almost exclusively on live fishes, although they have been known to opportunistically feed on mammals, birds, reptiles, and amphibians (Evans, 1982; King, 1988; Shoji et al., 2011). During the winter seasons, ospreys migrate to the southeastern United States and as far south as Chile and Argentina; however, there are a few colonies that reside year-round in south Florida, primarily in the Everglades National Park and surrounding areas (Evans, 1982; Lounsbury-Billie et al., 2008). Ospreys consume a diverse array of fishes (e.g., ictalurid catfishes, clupeid shads, and menhadens) from a variety of habitats, such as coastlines, estuaries, marshes, lagoons, rivers, lakes, and reservoirs (Glass and Watts, 2009). Reports of alternative prey species include carrion, voles, muskrats, and tiger salamanders (Evans, 1982; King, 1988). The foraging range extends approximately 5 km from the nest with a diving depth less than a meter (Bent, 1937; Evans, 1982). The osprey dietary plasticity is a primary factor for its worldwide distribution, with the exception of Antarctica. Although ospreys are usually not categorized as seabirds, they forage in both freshwater and marine habitats, which expose them to similar endohelminths previously recorded from seabirds and terrestrial birds. Reports of endohelminths of ospreys are rare in southeastern Florida, but statewide, 14 trematodes, 2 cestodes, 6 nematodes, and 3 acanthocephalans were found on both the Gulf and Atlantic coasts of the state of Florida (Forrester and Spalding, 2003). Of these identified species, five helminths are considered specialists in ospreys due to likely reproductive and ecological isolation from other Accipitriformes: Scaphanocephalus expansus, Neogogatea pandionis, Paradilepis rugovaginosus, Contracaecum pandioni, and Sexanoscara skrjabini (Kinsella et al., 1996; Forrester and Spalding, 2003). Other parasite generalists include Mesostephanus appendiculatoides, Ribeiroia ondatrae, Ascocotyle longa, Clinostomum sp., Capillaria

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ibisae, Andracantha mergi, and Polymorphis brevis (Kinsella et al., 1996; Forrester and Spalding, 2003).

Charadriiformes Thalasseus maximus (Boddaert, 1783) Royal terns Thalasseus maximus are distinct, colonial-nesting seabirds that breed and nest on natural barrier islands and man-made dredge spoil islands along the mid- Atlantic seaboard (Aygen and Emslie, 2006). Royal terns are found throughout the year along the Atlantic coast of Florida but have also been observed in the Dry Tortugas and the Florida Gulf coast. During the winter migratory season, royal tern populations in Florida increase in size by large breeding colonies from the north (Clapp et al., 1983). This species tends to feed inshore in shallow waters, although individuals have been observed to forage as far as 50 km offshore at depths of less than a meter (McGinnis and Emslie, 2001). Foraging consists of plunge diving techniques for shrimp and shallow- water schooling fishes, including anchovies, herrings, and small drums (Sciaenidae) (Aygen and Emslie, 2006; Wambach and Emslie, 2003; Wood, 2008). The diet of royal terns shows widely opportunistic foraging, which presumably aids in survival during annual fluctuations of individual prey availability (Aygen and Emslie, 2006). As opportunistic foragers, royal terns feed on a variety of prey items from crustaceans to surface-swimming baitfish and squid (Family Loliginidae). With a wide range of suitable prey items, royal terns are host to a diverse array of endohelminth species, similar to other studied species: acanthocephalans, cestodes, digeneans, and nematodes. Previously recorded species from royal terns include Stephanoprora denticulata, Cardiocephaloides spp., Pachytrema sp., and Contracaecum sp. (Hutton, 1964; Ubelaker, 1965; Dronen et al., 2007).

Leucophaeus atricilla (Linnaeus, 1758) The laughing gull Leucophaeus atricilla is a widely distributed species within North America and with increasing populations in the northeastern United States over recent decades (Clapp et al., 1983; Bernhardt et al., 2010). This gull is found in Florida throughout the year, with individuals observed to travel throughout and beyond the

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greater Caribbean region during the winter migration as far south as Panama and the mouth of the Amazon River in Brazil. Spring migration usually occurs during March with fall migration occurring late August to November (Clapp et al., 1983). Laughing gulls are dietary generalists for both terrestrial and aquatic habitats (including freshwater and saltwater systems). Foraging similarly occurs in a wide array of environments, from various marine ecosystems to urban areas (foraging ranges are up to 60 km inland during nonbreeding seasons and up to 40 km inland during breeding season). As upper trophic level consumers, the laughing gull diet generally includes a mixture of terrestrial, marine and freshwater prey typically enriched in δ15N and δ13C (e.g., large crustaceans, molluscs, forage fishes, and even small rodents). However, they are also well-known to take advantage of food availability of anthropogenic environments (e.g., coastal restaurants and landfills) (Knoff et al., 2002; Burger and Gochfeld, 2004). The plasticity of the laughing gull diet allows transmission of endohelminths to occur from prey items other than the typical marine organisms targeted by seabirds, such as arthropods (freshwater and terrestrial crustaceans and insects) and even smaller avifauna. Previously recorded helminthic species of laughing gulls have been documented in the Gulf coast of Florida such as Galactosomum spp., Cardiocephaloides megaloconus, Renicola glandoloba, and Stictodora lariformicola (Forrester and Spalding, 2003).

Larus argentatus smithsonianus (Coues, 1862) The American herring gull Larus argentatus smithsonianus (sometimes named the Smithsonian gull or Larus smithsonianus; hereafter simply “herring gull”) is a common predator distributed throughout most of North America and greater Caribbean. Herring gulls are common residents of the Florida Atlantic coast and the Florida Keys during winter season with arrivals in mid-October and departures in mid-May (Schreiber and Schreiber, 1977; Clapp et al., 1983). Strategies for foraging of herring gulls are similar to those of laughing gulls. Herring gulls are also relatively long-lived, upper- trophic level species with natural lifespans of 20 to 40 years (Botkin and Miller, 1974). The species feeds primarily inshore, diving no deeper than 2 m and foraging within 20 to 100 km from the colony; however, they often forage in urbanized areas (Burgess et al.,

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2013; Burger and Gochfeld, 2004; Schreiber and Mock, 1988). Like laughing gulls, herring gulls shift their diet to take advantage of changes in prey availability, which consists primarily of marine fish, invertebrates, and bird chicks, as well as anthropogenic sources such as landfills (Burgess et al., 2013). Previously recorded species of endohelminths found in herring gulls have been extensively studied by Threlfall (1968) in Northern Caernarvonshire, Wales and Anglesey, Wales with a total sample size of 657 individuals (1965, 1967) and 410 individuals examined in Newfoundland, Canada (1968). Species found include digeneans Stephanoprora pseudoechinata and Ornithobilharzia lari along with cestodes (Tetrabothrius cylindraceus), nematodes (Contracaecum sp.), and acanthocephalans (Arhythmorhynchus longicollis). Recorded species in Florida include trematodes: Cryptocotyle lingua, Gymnophallus deliciosus, Stictodora lariformicola, and Stephanoprora denticulata (Forrester and Spalding, 2003).

Purpose and Objectives: The overall purpose of the project was to examine parasite community composition and structure in seven seabird host species based on host phylogeny and feeding ecology. The specific objectives of this study were: 1) to describe endoparasite community composition and overall observed species richness of all seven common south Florida seabirds and 2) determine how parasite communities of these seabirds change in composition and structure according to host phylogeny and their respective feeding ecology.

Materials and Methods:

Sample Collection Specimens were obtained between August 2013 and December 2017 from four wildlife rehabilitation agencies in southeast Florida: the South Florida Wildlife Center (Fort Lauderdale), the Pelican Harbor Seabird Station (North Miami), the Florida Keys Wild Bird Rehabilitation Center (Tavernier), and the Key West Wildlife Center (Key West). Specimens were transported to the laboratory in coolers filled with ice to preserve

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organs and endoparasites from degradation. In the laboratory, each specimen was identified to species and given a unique American Ornithologists Union (AOU)- compliant alphanumeric identifier code and labeled with a Tyvek or aluminum tag attached to the leg prior to storage at ≤0°C.

Laboratory Processing Prior to dissection of collected seabirds, host specimens were placed in a refrigerator for thawing, with actual thawing time dependent on species and body size (ca. 24-72 hours depending on the bird species). After the specimens were thawed, biometric measurements were taken and recorded on the assigned datasheet for the individual: total weight, bill from base, bill from feathers, bill from nostril, bill depth, tarsus length, tail length, wing chord, and wing span. The weights of whole host specimens were measured with a hanging scale (model PHS100; PESOLA Präzisionswaagen AG, Switzerland) to 0.1 kilograms (kg). All measures of weights were converted to grams (g), while all measures of lengths (e.g., bill, wing, and tarsus) were converted to millimeters (mm). The body cavity was opened by first making an incision below the sternum and cutting towards the furcula to peel back the skin covering the abdominal region (McLaughlin, 2001). After exposing the sternum, it was cut vertically, and the clavicles separated by shears to allow entry into the body cavity. The internal organs from the cranial, thoracic, and abdominal cavities (brain, eyes, trachea, esophagus, heart, lungs, liver, kidneys, stomach, and intestines) were removed from each specimen for parasite examination and extraction. The brain was placed and pressed between two glass plates for examination under a stereomicroscope, while the eyes were dissected to determine if parasites were present in the humor, retina, and lens. The heart, lungs, liver, and kidneys were divided into smaller pieces (1/4th sections), and then pressed between glass plates for thorough examination of parasites. The discontinuation of examining the brain, eyes, heart, and lungs were due to the absence of infection in all samples processed (n=102). For the stomach, esophagus, and intestines, each organ was separated and cut open to remove any parasites using a stir-rinse-repeat cycle in glass specimen dishes filled approximately 80% with tap water – the supernatant was decanted repeatedly until water

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clarity was sufficient to allow the collection of parasites from the precipitate (McLaughlin, 2001). Organs were then compressed between glass plates for examination of any parasites not removed through the initial process. Infection intensities for each taxon (using provisional identifications in most cases) were recorded on the host specimen datasheet, noting the tissue location, then collected (McLaughlin, 2001). Subsets of all parasite taxa (e.g., digeneans, cestodes, acanthocephalans, and nematodes) were fixed in 70% ethanol or 95% ethanol prior to staining and mounting, respectively (Pritchard and Kruse, 1982). Trematodes fixed in 70% ethanol and in good condition (little to no deterioration of sample) were stained with acetocarmine using a 1:3 acetocarmine to 70% ethanol solution (Pritchard and Kruse, 1982). They were then serially dehydrated through solutions of 70%, 95%, and pure ethanol. They were cleared in clove oil for approximately three minutes and mounted on glass slides in Permount. Acanthocephalan specimens underwent the same fixing, staining, and mounting process of trematodes; however, the tegument was pierced with entomological needles before staining to allow the acetocarmine, ethanol, and clove oil solutions to effectively disperse into and throughout the sample specimens. Nematode specimens were immersed in warm 70% ethanol to fix them in extended positions and transferred into a 7:3 ethanol and glycerol solution for a minimum of fourteen days to clear. After clearing, each specimen was examined and identified to the lowest taxon through temporary mounts in glycerol or semi-permanent mounts in glycerin jelly (Pritchard and Kruse, 1982).

Helminth Identification

Identification of parasites was based on keys (Price, 1929; Cable et al., 1960; Farley, 1971; Pearson, 1973; McDonald, 1981; McDonald, 1988; Gibson, Jones, and Bray, 2002; Kostadinova, Vaucher, and Gibson, 2002; Jones, Bray, and Gibson, 2005; Dronen et al., 2007; Bray, Gibson, and Jones, 2008) and primary literature. The World Register of Marine Species (WoRMS) was used to ensure that only the current accepted names were used.

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Data Analysis

In this study, prevalence is the percentage of a given host taxon infected with a given parasite taxon, and mean intensity is the mean number of parasites of a given taxon found in an infected host. Mean abundance is the mean number of parasites of a given taxon found across all hosts, infected or uninfected, while overall species richness refers to the number of parasite species found within each individual bird (Bush et al., 1997). PRIMER 7.0.13 (v. 7.0.13; Plymouth Routines In Multivariate Ecological Research) was used for all diversity and community-level analyses in generating alpha and beta diversity indices with inclusion of (1) overall community richness for each host species (component community), (2) mean species richness for individual seabirds (infracommunity), (3) community evenness, as well as (4) the Shannon and Hill indices (Clarke et al., 2014; Clarke and Gorley, 2015). The component community refers to all infrapopulations of parasites typically associated with a subset of the studied host species, while infracommunity refers to a community of parasite infrapopulations within a single host specimen (Bush et al., 1997). PRIMER 7.0.13 was used to test whether parasite community structure (i.e., the presence or absence of taxa as well as their relative abundances) varied as a function of host trophic guild (i.e., feeding ecology dictating the parasite assemblages of seabirds). A triangular matrix of Bray-Curtis endoparasite infracommunity similarities was established and formed the basis for the remaining procedures: (1) cluster analysis, (2) unconstrained ordinations (two- and three- dimensional nonmetric multidimensional scaling, nMDS, which allowed visual examination of how parasite infracommunity structure related to host phylogeny, feeding ecology, and host prey preferences, and (3) RELATE and 2STAGE analyses. A dummy variable was included in each analysis to include uninfected hosts for the purpose of examining parasite communities within each host species as a population, rather than a single individual replicated numerous times as a representation of a population. The relative effects of host species and feeding range on observed infracommunity species richness were assessed using least squares regression in JMP 12.1.0 (v. 12.1.0; SAS Institute).

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To test for correlation between host phylogeny and feeding ecology, a RELATE analysis in PRIMER was used to create resemblance matrices based on the taxonomic level for each seabird host species and their feeding ecology. The factors used for feeding ecology were (1) foraging distance from shore (i.e., the feeding range for each host seabird species), (2) foraging techniques, and (3) prey preferences for each seabird taxa. A fourth resemblance matrix was created for parasites summed at the genus level to provide more robust results regarding issues that may have arose from misidentification of parasites (i.e., incorrect species identification due to lack of sufficient morphological identifiers), while a fifth resemblance matrix consisted of fourth root parasite centroids from the original data set. The inclusion of a dummy variable was used to capture uninfected host seabird species in the similarity analyses to represent each taxa as a population. A 2STAGE analysis was used to ordinate the similarity matrices generated by RELATE to graphically illustrate how they clustered among each other.

Results:

Parasites were found in 146 of the 206 birds examined. The majority of parasites found in all host species were located within the intestinal tract, with the remaining being located within the stomach, esophagus, and trachea. Few parasites were found in the liver and kidneys. Parasite taxa found included members of the Trematoda, Cestoda, Acanthocephala, and Nematoda (see Appendix 3 for a detailed description of the basis for all species-level identifications). Two cestode taxa could not be identified beyond genus level due to lack of both scolices and proglottids being present in the samples collected along with the absence of rostellar hooks on those scolices; genus-level identification for both cestode taxa was based on the comparative morphology of proglottids from a taxonomic key (Khalil et al., 1994). Prevalence of infection for each host species – number of host specimens infected divided by the total number of host specimens examined – varied among the seven seabird hosts, while observed species richness (OSR) varied among the several seabird species (see Table 2 for calculated values). Northern gannets (S=17) and brown pelicans (S=16) displayed the highest numbers of parasite species richness. Brown pelicans had

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the second highest OSR, while double-crested cormorants had the third highest (S=15). The OSR of both ospreys (S=11) and royal terns (S=11) were subsequent to double- crested cormorants. Laughing gulls (S=6) and herring gulls (S=4) had the lowest OSR among the seven seabird species. Mean infracommunity species richness for the several seabird species varied as well. Parasite communities displayed strong clustering among seabird species with occasional overlap occurring between seabird hosts (seen in Figure 3 with the shade plot). Cluster analysis combined with a similarity profile analysis was used to distinguish co-occurring groups of parasites among the seven seabirds examined. A shade plot (Figure 3) was generated to illustrate the distribution of co-occurring parasite communities for the seven species of seabirds. Seabird species were clustered based on similarity of parasite communities. The royal tern, laughing gull, and herring gull had closely related parasite communities not found in any of the other seabird host species, while brown pelicans, northern gannets, and double-crested cormorants had similar parasite communities, such as Ascocotyle, Mesostephanus, and Galactosomum. Ospreys did not have similar parasite communities compared to the other seabird species, since parasite taxa found were exclusive to them alone. Non-metric multidimensional scaling (nMDS) of the parasite community analyzed at the species level determined the relationship between community structures of parasites to the several seabird host species examined (Figures 4 and 5). Based on the community structure of parasites, there are four distinct groupings for seabird species (Figure 4). Brown pelicans and northern gannets showed similarity among parasite species found, while herring and laughing gulls and royal terns were grouped together. Ospreys and double-crested cormorants were separately grouped, forming the last two distinct groups. Proximity of the data points indicates similarity among the infracommunities: data points that are closer represent individual seabirds with more similar community structure of endoparasites. Pearson Correlation vectors of parasite species are displayed in Figure 5 for each individual seabird specimen examined. The RELATE analysis detected significant correlations between fourth root parasite similarity centroids to host phylogeny (Rho= 0.564, p=0.017) and feeding ecology (feeding technique: Rho= 0.564, p= 0.017; feeding range: Rho= 0.553, p=0.005),

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whereas prey preference (Rho= 0.124, p=0.278) was not significant. The magnitude of effect for both phylogeny and feeding ecology were similar, suggesting each factor had a role in structuring the observed parasite communities (see Table 3 for RELATE values). In regards to prey preference, the effect observed was small compared to the other three factors, suggesting it had little influence on the structure of parasite communities. Comparing genus-level to species-level identification matrices, the correlation had high similarity (Rho=0.961, p=0.001), indicating a lack of discrepancy when analyzing parasite data at either taxonomic level. 2STAGE analysis was used to ordinate RELATE data through presence or absence measures of similarity matrices, which generated a visual representation of each factor and its correlation to fourth root parasite centroids. Factors that clustered closely together indicated high similarity (i.e., presence or absence measures were nearly similar), and the distance from the parasite centroids indicated the magnitude of effect each factor had on the structure of parasite communities (i.e., clusters closer to parasite centroids had a stronger effect and vice versa). Of the four factors, host phylogeny, feeding technique, and feeding range clustered near parasite centroids, while host prey preference formed a separate cluster indicating little effect it had on the structuring of parasite communities (refer to Figure 6 for visual representation).

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Table 2. Community analysis of common marine-associated birds in south Florida, including regions of overlap and lagoon waters inshore of barrier islands. Prevalence is the percent infection rate of each host species examined, Community Species Richness (S) is total number of parasite taxa observed, and Observed Species Richness (OSR) is the number of parasite species seen per individual bird specimen. Evenness is Pielou’s evenness (values approaching zero indicate uneven samples dominated by one or two key taxa, values approaching one indicate even samples where all parasite taxa are equally present).

Specimens Prevalence Community species Infracommunity Avian Hosts examined (n) (%) richness (S) OSR Evenness Pelecanus occidentalis 33 75.8 16 5.7 ± 0.4 0.7 ± 0.0 Morus bassanus 31 93.5 17 5.1 ± 0.4 0.8 ± 0.0 Phalacrocorax auritus 33 81.8 15 5.0 ± 0.4 0.9 ± 0.0 Pandion haliaetus 27 88.9 11 2.0 ± 0.4 0.9 ± 0.0 Thalasseus maximus 30 70.0 11 1.5 ± 0.4 0.8 ± 0.0 Leucophaeus atricilla 40 30.0 6 0.4 ± 0.4 1.0 ± 0.1 Larus argentatus 12 66.7 4 0.8 ± 0.7 0.7 ± 0.1

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Table 3. RELATE values for host phylogeny, host feeding technique and range, and host prey preference compared to fourth root parasite centroids. The significance of each factor is determined by the p-value (p<0.05=significant), while rho values indicate the magnitude of effect each factor had on the observed parasite communities in the seven seabird species. Phylogeny, feeding technique, and feeding range were significant and had similar effects when compared to parasite centroids, while prey preference had no significance. Parasites summed at genus level compared to species level were also analyzed through RELATE and indicated no discrepancies when using either taxonomic level with parasite data.

Rho p Host Phylogeny 0.564 0.017

Host Feeding Range 0.553 0.005

Host Feeding Technique 0.553 0.039

Host Prey Preference 0.124 0.278 Parasites Summed at Genus Level Compared 0.961 0.001 to Species Level

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Figure 3. Fourth root transformed shade plot of parasite abundance within the several targeted seabird species. Parasites were analyzed at the species level across seven seabird species. Seabird host species are clustered by the similarity of their parasite communities, while parasites are clustered into co-occurring groups based on the likelihood of parasites being found together in each host species. Darker shades indicate greater abundance of parasite species, while lighter shades indicate lower

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abundance.

Transform: Square root Resemblance: S17 Bray-Curtis similarity (+d) 2D Stress: 0 Distance 45

NOGA

BRPE

LAGU RLTE

HEGU

OSPY DCCO

Figure 4. Square root transformed non-metric multi-dimensional scaling of parasite communities based on host seabird species. Distance (resemblance level = 45) between hosts indicates similarity in parasite community composition (i.e., parasite communities are similar the closer host species are to one another, while parasite communities were less similar with greater distance from each other). As illustrated, there are four distinct groupings: 1) laughing gull (LAGU), herring gull (HEGU), and royal tern (RLTE); 2) northern gannet (NOGA) and brown pelican (BRPE); 3) osprey (OSPY); and 4) double-crested cormorant (DCCO). A dummy variable of 1 was added to account for uninfected individual seabirds.

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Figure 5. Square root transformed non-metric multi-dimensional scaling of parasite community similarity for infracommunities in individual seabirds. Clustering of host species illustrate close similarity of parasite taxa found within individual seabirds. Each symbol represents the seven host seabird species, while each vector represents the most abundant parasite taxa found among them. As illustrated, Cardiocephaloides spp. were found only in the larids, while parasite taxa consisting of Contracaecum, Ascocotyle, Galactosomum, and Mesostephanus were found among host species belonging to

26 brown pelicans, northern gannets, double-crested cormorants, and ospreys. A dummy variable was added to illustrate similarity

among individual uninfected seabirds.

Figure 6. 2STAGE non-metric multi-dimensional scaling (square rooted) of similarity matrices for host phylogeny, host feeding range and technique, host prey preference, and fourth root parasite centroids. Clustering of host phylogeny, feeding range and technique, and parasite centroids suggest the first three factors having more influence on the structure of parasite communities compared to prey preference (forming its own separate cluster). Each factor was based on categorical values

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(e.g., presence or absence, distance foraged, and feeding technique used by each seabird species).

Discussion:

This study identified a total of 33 parasite taxa from 146 infected individual birds. Of these, 21 are new host records, while seven are range extensions in Florida. The parasite community structure was examined on two different factors: host phylogeny and host feeding ecology. RELATE analyses suggested that host phylogeny, host feeding range, and host feeding technique were significant and had similar effects on the structuring of observed parasite communities in the seven seabird species studied (see Table 3 for RELATE values). Host prey preference was not significant (Rho= 0.124, p= 0.278) when compared to fourth root parasite centroids, which could be attributed to the broad generalization of prey items used in the analyses (i.e., lack of data with regards to preferred size of prey items, preferred prey taxa, and quantity consumed of prey items). Analyses of the host age, date of death, and cause of death were not included in this study, as rehabilitation facilities prior to 2016 did not include patient identification numbers, so pre-mortality details were unavailable for most (n=50; 24% of the total) host specimens.

Host Species

Based on parasite community structure of the several targeted seabird species, variation was observed in parasite community composition and richness among each seabird host species (see Appendix 2 for comprehensive list of recorded parasites for each seabird host species). Northern gannets had the highest observed species richness at 17 parasite species (14 digeneans, 1 cestode, 1 nematode, and 1 acanthocephalan), while brown pelicans had the second highest species richness at 16 (9 digeneans, 1 cestode, 4 nematode, and 2 acanthocephalans). Since brown pelicans and northern gannets forage in coastal and offshore areas with great dietary plasticity, their feeding ranges and broad diet would account for greater exposure and occurrence of multiple parasite species from a variety of coastal and offshore intermediate hosts (Dronen et al., 2003; Muzaffar, 2009; Pettex et al., 2012). From previous studies in south Florida of both the Gulf and Atlantic coasts, the parasite species found in this study matched previously recorded species from

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these two seabird hosts (Forrester and Spalding, 2003). Common generalists overlapping both host species included Ascocotyle, Mesostephanus, Galactosomum, and Contracaecum. Since these species along with Andracantha and Tetrabothrius were found in other fish-eating birds of both freshwater and marine water environments, it provides insight on the broad range of food items brown pelicans and northern gannets include in their diet when foraging (Clapp et al., 1982; Shealer, 2001; Votier et al., 2010). As opportunistic feeders of both freshwater and brackish to marine waters, double-crested cormorants are hosts to a variety of parasite taxa, similar to piscivorous seabird species foraging in coastal areas (Threlfall, 1982; Withers and Brooks, 2004; Coleman and Richmond, 2007; Eisenhower and Parrish, 2009). Double-crested cormorants often exploit the most readily available food sources, primarily fishes; however, crustaceans, amphibians, aquatic insects, and plants are all known to make up a small percentage of their diet (Withers and Brooks, 2004). This display of foraging behavior varies on a spatial and temporal scale depending on the location, season, and prey availability, often times feeding at night on wintering grounds (Coleman and Richmond, 2007). The species richness and community composition of parasites in double-crested cormorants consisted of 15 species: 9 digeneans, 1 cestode, 3 nematodes, and 2 acanthocephalans. Parasites recorded were noted as generalists (with the exception of Drepanocephalus spathans and Hysteromorpha corti), even cosmopolitans (parasite species distributed worldwide) with no obligate definitive hosts, such as Ascocotyle, Mesostephanus, Contracaecum, and Ascodilepis. Given the generalist characteristic of these parasites in intermediate and definitive host species, as well as the opportunistic foraging of most piscivorous birds, these parasite taxa are commonly found within double-crested cormorants. Similar to the foraging ecology of double-crested cormorants, ospreys showed variability between freshwater and marine water community species richness of parasites. Parasite species diversity for ospreys was at 11 observed species (8 digeneans, 1 cestode, 1 nematode, and 1 acanthocephalan). Of these species with the exception of Nematostrigea serpens and Scaphanocephalus expansus, the nine remaining species are considered to be generalists to a variety of piscivorous birds (Kinsella et al., 1996).

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Ascocotyle, Mesostephanus, Contracaecum, and Ribeiroia are a few genera typically found in members belonging to other orders of fish-eating birds (Anseriformes, Pelecaniformes, and Ciconiiformes) and have life cycles that are primarily associated with estuarine and marine ecosystems (Kinsella et al., 1996; Drago and Lunaschi, 2011). Although royal terns are grouped within the broad order Charadriiformes, they exhibited greater species richness compared to the laughing and herring gull: 11 total parasite species (9 digeneans, 1 cestode, and 1 nematode). Unlike gulls, royal terns feed almost exclusively on fishes, which is mostly observed through the two species Cardiocephaloides and Tetrabothrius. The overlap of Cardiocephaloides with the laughing and herring gull (Figure 4), provides insight into the targeted fish species (e.g., mullets, silversides, and killifish) that is likely foraged by all three seabirds. The present study also found the rare-event Pachytrema sanguineum in the intestines of a royal tern (n < 1), which was also observed in a previous study by MacInnis (1966). In a parasite assessment of approximately 200 royal tern individuals, only a single specimen of P. sanguineum was found within a gall bladder (MacInnis, 1966). For herring and laughing gulls, both had the lowest observed species richness when compared to the other five seabird host species. Herring gulls had a total of 4 parasite species found (3 digeneans and 1 nematode), whereas laughing gulls had a total of 6 parasite species (4 digeneans, 1 cestode, and 1 nematode). Cardiocephaloides spp. overlapped both the herring and laughing gull, which is a frequently observed helminth found in the order Charadriiformes (Born-Torrijos et al., 2016). As with the other five seabird hosts, gulls are proficient opportunistic feeders, but they are also efficient scavengers of landfills. Given this foraging behavior, the low infection rates could be attributed to the highly urbanized areas of south Florida along with the seasons, which provide readily accessible and easily acquired food items (Clapp et al., 1983). Per Plaza and Lambertucci (2017), food subsidies from landfills showed improvement to reproductive parameters of both herring and laughing gulls: larger clutch size and egg volume and enhanced growth and survival of chicks, respectively. The increased use and positive relationship between both gull species and refuse sites could be a contributing factor to the low species richness observed from the experiment, as previous studies have

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noted infections with foraging in these areas to be of bacterial and viral origin (Plaza and Lambertucci, 2017). Ascocotyle, Mesostephanus, Galactosomum, Scaphanocephalus, and Contraceacum were the five most frequent genera of parasites found in the seabird samples. In particular, Ascocotyle, Mesostephanus, and Contracaecum were the most abundant genera that overlapped four of the seven targeted seabird species: brown pelican, northern gannet, double-crested cormorant, and osprey. Galactosomum species showed strong overlap with brown pelican, northern gannet, and double-crested cormorant, as well as a small number being present in osprey and royal terns. Since these parasite taxa are generalists, they are commonly found in piscivorous birds through the ingestion of various fish species that serve as intermediate hosts from marine and freshwater habitats (Marcogliese, 2002; Marcogliese, 2004; Muzaffar, 2009). Scaphanocephalus had the highest presence in osprey with no overlap in any other species, which can be attributed to host specialization of ospreys (Foronda et al., 2009). Parasite species that were found in low abundance (n<2) were Pachytrema sanguineum and Nematostrigea serpens, which are considered rare event species based on previous studies noting one specimen found for both species in their respective hosts (MacInnis, 1966; Lebedeva and Yakovleva, 2016). Ribeiroia ondatrae was found in moderate abundance within ospreys, which may indicate feeding between the secondary intermediate hosts of fish and amphibian species.

Feeding Ecology

Feeding ecology was significant with the overall community composition and richness of parasites observed (Table 3) with a similar magnitude of effect on the diversity as host phylogeny (Figure 3). The presence of parasite species provided insight into the foraging locations of the targeted seabird hosts and the potential prey items consumed in those areas. Ascocotyle, Mesostephanus, and Contracaecum are mostly found in brackish and coastal waters, which were the most abundant genera when observed in brown pelicans, northern gannets, double-crested cormorants, and ospreys (Figure 5). The overlap of parasite taxa suggests that these seabird species are

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opportunistically feeding on similar prey items available in south Florida waters, both in freshwater and marine environments (Withers and Brooks, 2004; Pettex et al., 2012; Lamb, 2016). Given the four clusters with feeding ranges (Figure 4), brown pelicans and northern gannets actively foraged within nearly similar environments, which are also observed for the group consisting of laughing and herring gulls and royal terns. Contrary to those two groups, double-crested cormorants and ospreys clustered into individual groupings, which would suggest not only a variability of foraging location, but a dissimilarity of prey items in both freshwater and saltwater environments (Figure 4). As Threlfall (1982) reported, brown pelicans and double-crested cormorants in Florida share similar parasite profiles of at least eight helminth species due to similar food habits. Comparing host phylogeny, host feeding range and techniques, and host prey preferences to fourth root parasite centroids, 2STAGE RELATE suggested that host phylogeny, feeding range, and feeding technique were significant and had a greater influence on the structure of parasite communities found within the several seabird species (Figure 6). As for prey preference, it was not significant within the RELATE analysis suggesting the range of prey items consumed was less important compared to host phylogeny and overall feeding ecology (e.g., range, depth, and techniques). Per Poulin (1995), prey content in host diet had a weak effect on gastrointestinal parasite communities in fish. However, he mentions that although carnivorous behavior did not reflect in greater parasite species richness, host diet should not be considered unimportant in parasite community studies. He suggests that an ideal measure of diet (virtually impossible to obtain) would consist of an estimate of its diversity based on the variety of prey consumed and the relative importance of those prey in the host’s diet. Biotic alterations to feeding ecology of seabird species is another factor to take into consideration, as their feeding tactics may change due to competition with other top predators, group or colony hunting, or breeding versus non-breeding seasons. Overall, feeding ecology, trophic dynamics, and the integration of parasites into food webs is a continuous topic of intense study (Marcogliese and Cone, 1997; Marcogliese, 2004; Lafferty et al., 2008). By incorporating the life history, behavior, and prey preferences of seabird hosts, it is possible to link parasite life cycle transmissions through the food web to better understand the community composition and richness of parasites on an annual

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timeframe. Although the study did not fully assess these factors, it is one of key interest to consider for future research.

Future Research

Recent studies have investigated how parasite communities help to shape the condition within ecosystems from terrestrial to marine-based environments. Recent studies have shown high variability of parasite community composition from numerous targeted host species ranging from intermediate and definitive hosts, yet how parasites are acquired from trophic interactions is still being studied. The present study looked at how feeding ecology could shape the diversity of parasites seen within host species, while determining if host phylogeny was the strongest factor that dictates the community composition of parasites. Future studies should include an assessment for migratory behavior of host species (brown pelicans, northern gannets, double-crested cormorants, and gulls and terns), since they are known to be either migratory or residential inhabitants. Although dates were noted when collecting sample host specimens, it was not known whether the birds were residents of south Florida or migrant species, especially with double-crested cormorants as they are both residents and migrants in south Florida. As vagile species, seabirds act as vectors – transportation mechanisms – for redistributing parasite species into new environments, which could account for the diversity seen from previous studies and new location records. Coupling the factors of seasonal variation along with migratory patterns of both host species and prey items could provide greater insight into the distribution and diversity of parasites along the eastern coast of south Florida. One method, albeit not entirely effective, could be the wider application of global positioning system (GPS)-based electronic tracking: harness attachments for seabird species and direct or imbedded attachments for prey items. Assessing parasite communities of intermediate hosts, both first and secondary, in tandem could aid in determining the accuracy of parasite life cycle transmissions. If parasite species are targeting preferred prey items of these seabird hosts, then community composition observed should be similar between intermediate and definitive host species.

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Previous reports have noted that very little is known about the dynamics of transmission of parasites in host species, although spatial and temporal variation of infections has been well-documented in freshwater and marine fishes (Marcogliese, 1995). Per Parker et al. (2003), the evolution of life-cycle complexity is essential in understanding trophic dynamics, yet it is seldom considered when assessing energy transfers in food web patterns (Thompson et al., 2005). Transmission of parasites between host species involves a transmission window (the timeframe of transmission of parasites from one host to another that can take place), which varies depending on parasite species and seasonal periods (MacKenzie et al., 1995). Transmission windows can last throughout the entire lifespan of the host (i.e., infection occurring at almost any time) or may be limited to brief seasonal periods due to alterations in environmental conditions. Understanding how transmission cycles occur for parasites can provide greater insight into selective pressures that may favor increased life cycle complexity, which benefits parasite fitness and affects virulence towards various host species (Auld and Tinsley, 2015). Thus, information of transmission cycles for parasites is essential for both basic and applied biology from an ecological perspective. Parasite community composition should also be tested against anthropogenic impact along coastal areas. As ideal sentinels used for chemical pollution, parasites are able to bioconcentrate chemical pollutants in low concentrations within the environment. Determining if heavy pollutants reduce overall host fitness could account for the intensity of infection rates and overall abundance and diversity of parasite species. Lowered immune responses could potentially result in greater diversity among parasite communities; however, if parasites sequester these heavy metals and toxins, it may improve overall host fitness resulting in less diversity and community structure observed from previously recorded studies (Blanar et al., 2009; Robinson et al., 2010; Blanar, Marcogliese, and Couillard, 2011).

Conclusion

The purpose of this study was to determine the extent feeding ecology had on the community structure and composition of parasite assemblages within the seven seabird

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species of south Florida. Based on the analyses, the host phylogeny was the greatest driving factor for the community composition and structure of parasites with feeding ecology having an almost identical effect. It was found that seabirds foraging further offshore and in pelagic environments, including brown pelicans, harbored greater parasite abundance of a few dominate taxa, whereas species that foraged in coastal to inshore locations displayed low to moderate abundance with greater parasite diversity, except for both laughing and herring gulls. Although prey preference did not have as strong of an effect on the parasite community composition when compared to the factor of seabird host species, it did provide invaluable insight on the dietary preferences of the targeted seabird species. Ribeiroia ondatrae, for example, can use both fishes and larval amphibians as secondary intermediate hosts, which are both preyed on by ospreys. Ascocotyle longa are generalist parasites typically found in Mugil spp., which are found in coastal waters, lagoons, and estuaries. Since these parasite species overlapped in brown pelicans, northern gannets, double-crested cormorants, and ospreys, it provides information on the location of where these host species feed and the type of prey targeted. In future studies, active foraging with the inclusion of location and targeted prey items should be noted when collecting seabird specimens. Due to the regulations and ethical aspect of actively killing and collecting seabird specimen samples, it is an obstacle that should be taken into consideration for determining the effect these factors play in structuring the endoparasite community composition of the host species.

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References:

Aygen, D. and Emslie, S. D. (2006). Royal Tern (Sterna maxima) chick diet at Fisherman Island National Wildlife Refuge, Virginia. Waterbirds, 29(3), 395-400. Beja, P., Palma, L., Martins, S., and Freitas, R. (2011). Diet of breeding ospreys in the Cape Verde Archipelago, Northwestern Africa. Journal of Raptor Research, 45(3), 244-251. Bent, A. C. (1937). Life Histories of North American Birds of Prey Pt. 1: Order Falconiformes. Taunton, MA: Smithsonian Institution United States National Museum. Bernhardt, G. E., Kutschbach-Brohl, L., Washburn, B. E., Chipman, R. B., and Francoeur, L. C. (2010). Temporal variation in terrestrial invertebrate consumption by Laughing Gulls in New York. American Midland Naturalist, 163(2), 442-454. Blanar, C. A., Munkittrick, K. R., Houlahan, J., MacLatchy, D. L., and Marcogliese, D. J. (2009). Pollution and parasitism in aquatic animals: A meta-analysis of effect size. Aquatic Toxicology, 93(1), 18-28. Blanar, C. A., Marcogliese, D. J., and Couillard, C. M. (2011). Natural and anthropogenic factors shape metazoan parasite community structure in mummichog (Fundulus heteroclitus) from two estuaries in New Brunswick, Canada. Folia Parasitologica, 58(3), 240-248. Born-Torrijos, A., Poulin, R., Pérez-del-Olmo, Culurgioni, J., Raga, J. A., and Holzer, A. S. (2016). An optimised multi-host trematode life cycle: fishery discards enhance trophic parasite transmission to scavenging birds. International Journal for Parasitology, 46, 745-753. Botkin, D. B. and Miller, R. S. (1974). Rates and survival of birds. The American Naturalist, 108(960), 181-192. Bray, R. A., Gibson, D. I., and Jones, A. (Eds.). (2008). Keys to the Trematoda (Vol. 3). London, UK: CABI Publishing and The Natural History Museum. Breton, A. R., Fox, G. A., and Chardine, J. W. (2008). Survival of adult Herring Gulls (Larus argentatus) from a Lake Ontario colony over two decades of

36

environmental change. Waterbirds, 31(1), 15-23. Brierley, A. S. and Fernandes, P. G. (2001). Diving Depths of Northern Gannets: Acoustic Observations of Sula bassana from an Autonomous Underwater Vehicle. The Auk, 118(2), 529-534. Brouwer, K., Hiddinga, B., and King, C. E. (1994). Management and breeding of pelicans Pelecunus spp: in captivity. International Zoo Yearbook, 33(1), 24-39. Buckley, F. G. and Buckley, P. A. (1972). The breeding ecology of Royal Terns Sterna (Thalasseus) maxima maxima. Ibis, 114, 344-359. Burger, J. and Gochfeld, M. (2004). Marine birds as sentinels of environmental pollution. EcoHealth, 1(3), 263-274. Burgess, N. M., Bond, A. L., Hebert, C. E., Neugebauer, E., and Champoux, L. (2013). Mercury trends in Herring Gull (Larus argentatus) eggs from Atlantic Canada, 1972–2008: Temporal change or dietary shift? Environmental Pollution, 172, 216-222. Bush, A. O., Lafferty, K. D., Lotz, J. M., and Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of Parasitology, 83(4), 575-583. Bustnes, J. O. and Galaktionov, K. V. (1999a). Anthropogenic influences on the infestation of intertidal gastropods by seabird trematode larvae on the southern Barents Sea coast. Marine Biology, 133, 449-453. Bustnes, J. O. and Galaktionov, K. V. (1999b). Distribution patterns of marine bird digenean larvae in periwinkles along the southern coast of the Barents Sea. Diseases of Aquatic Organisms, 37, 221-230. Clapp, R. B., Banks, R. C., Morgan-Jacobs, D., Hoffman, W. A. (1982). Marine Birds of the Southeastern United States and Gulf of Mexico Pt. 1: Gaviiformes through Pelecaniformes. U.S. Fish and Wildlife Service, Washington, D.C. United States. Clapp, R. B., Morgan-Jacobs, B., and Banks, R. C. (1983). Marine Birds of the Southeastern United States and Gulf of Mexico Pt. 3: Charadriiformes. U.S. Fish and Wildlife Service, Washington, D.C. United States. Clarke, K. R. and Gorley, R. N. (2015). PRIMER v7: User Manual/Tutorial. PRIMER-E, Plymouth, 296pp.

37

Clarke, K. R., Gorley, R. N., Somerfield, P. J., and Warwick, R.M. (2014). Change in marine communities: an approach to statistical analysis and interpretation. 3rd Edition. PRIMER-E, Plymouth, 260pp. Coleman, J. T. H. and Richmond, M. E. (2007). Daily foraging patterns of adult double- crested cormorants during the breeding season. Waterbirds, 30(2), 189-198. Courtney, C. H. and Forrester, D. J. (1974). Helminth Parasites of the Brown Pelican in Florida and Louisiana. The Helminthological Society of Washington, 41(1), 89-93. D'Amelio, S., Barros, N. B., Ingrosso, S., Fauquier, D. A., Russo, R., and Paggi, L. (2007). Genetic characterization of members of the genus Contracaecum (Nematoda: Anisakidae) from fish-eating birds from west-central Florida, USA, with evidence of new species. Parasitology, 134(7), 1041-1051. D'Amelio, S., Cavallero, S., Dronen, N. O., Barros, N. B., and Paggi, L. (2012). Two new species of Contracaecum Railliet and Henry, 1912 (Nematoda: Anisakidae), C. fagerholmi n. sp. and C. rudolphii F from the brown pelican Pelecanus occidentalis in the northern Gulf of Mexico. Systematic Parasitology, 81(1), 1-16. Diaz, J. I. and Cremonte, F. (2010). Development from Metacercaria to adult of a new species of Maritrema (Digenea: Microphallidae) parasitic in the Kelp Gull, Larus dominicanus, from the Patagonian Coast, Argentina. Journal of Parasitology, 96(4), 740-745. Dietrich, M., Kempf, F., Gómez-Díaz, E., Kitaysky, A. S., Hipfner, J. M., Boulinier, T., and McCoy, K. D. (2012). Inter-oceanic variation in patterns of host-associated divergence in a seabird ectoparasite. Journal of Biogeography, 39(3), 545-555. Dorr, B. S., Burger, L. W., Barras, S. C., and Godwin, K. C. (2012). Double-crested cormorant distribution on catfish aquaculture in the Yazoo River Basin of Mississippi. Wildlife Society Bulletin, 36(1), 70-77. Drago, F. B. and Lunaschi, L. I. (2011). Digenean parasites of Ciconiiform birds from Argentina. Revista Mexicana de Biodiversidad, 82, 77-83. Dronen, N. O., Blend, C. K., and Anderson, C. K. (2003). Endohelminths from the Brown Pelican, Pelecanus occidentalis, and the American White Pelican, Pelecanus erythrorhynchus, from Galveston Bay, Texas, U.S.A., and checklist of pelican parasites. Comparative Parasitology, 70(2), 140-154.

38

Dronen, N. O., Blend, C. K., Gardner, S. L. and Jiménez, F. A. (2007). Stictodora cablei n. sp. (Digenea: Heterophyidae) from the royal tern, Sterna maxima (Laridae: Sterninae) from Puerto Rico and the Brazos County area of the Texas Gulf coast, U.S.A., with a list of other endohelminths recovered in Texas. Zootaxa, 1432, 35- 56. Dubois, G. (1968). Synopsis des Strigeidae et des Diplostomatidae (Trematoda). Neuchâtel, CH: Société neuchâteloise des sciences naturelles. Eisenhower, M. D. and Parrish, D. L. (2009). Double-crested Cormorant and fish interactions in a shallow basin of Lake Champlain. Waterbirds, 32(3), 388-399. Elton, C. S. (1927). Animal Ecology. London, UK: Sidgwick and Jackson. Evans, D. L. (1982). Status reports on twelve raptors. U.S. Fish and Wildlife Service, Washington, D.C. United States. Fifield, D. A., Montevecchi, W. A., Garthe, S., Robertson, G. J., Kubetzki, U., and Rail, J.-F. (2014). Migratory tactics and wintering areas of Northern Gannets (Morus bassanus) breeding in North America. Ornithological Monographs No. 79 (Vol. No. 79, pp. 1-63): American Ornithologists' Union. Font, W. F., Overstreet, R. M. and Heard, R. W. (1984). Taxonomy and biology of Phagicola nana (Digenea: Heterophyidae). Transactions of the American Microscopical Society, 103(4), 408-422. Forrester, D. J. and Spalding, M. G. (2003). Parasites and Diseases of Wild Birds in Florida. Gainesville, Florida: University Press of Florida. Furness, R. W. and Monaghan, P. (1987). Seabird ecology. Blackie, New York, New York, USA. Garthe, S., Montevecchi, W. A., and Davoren, G. K. (2007). Flight destinations and foraging behaviour of northern gannets (Sula bassana) preying on a small forage fish in a low-Artic ecosystem. Deep-Sea Research II, 54, 311-320. Gibson, D. I., Jones, A., Bray, R. A. (Eds.). (2002). Keys to the Trematoda (Vol. 1). London, UK: CABI Publishing and The Natural History Museum. Glass, K. A. and Watts, B. D. (2009). Osprey diet composition and quality in high- and low-salinity areas of lower Chesapeake Bay. Journal of Raptor Research, 43(1), 27-36.

39

Hamer, K. C., Humphreys, E. M., Garthe, S., Hennicke, J., Peters, G., Grémillet, D. et al. (2007). Annual variation in diets, feeding locations and foraging behaviour of gannets in the North Sea: Flexibility, consistency and constraint. Marine Ecology Progress Series, 338, 295-305. Hamer, K. C., Phillips, R. A., Wanless, S., Harris, M. P., and Wood, A. G. (2000). Foraging ranges, diets and feeding locations of gannets Morus bassanus in the North Sea: evidence from satellite telemetry. Marine Ecology Progress Series, 200, 257-264. Hatch, J. J. (1995). Changing populations of Double-crested Cormorants. The Double- crested Cormorant: biology, conservation and management (D. N. Nettleship and D. C. Duffy, Eds.). Colonial Waterbirds, 18(Special Publication 1), 8-24. Hingtgen, T. M., Mulholland, R., and Zale, A. V. (1985). Habitat suitability index models: Eastern Brown Pelican. U.S. Fish Wildlife Service Biological Report 82(10.90). 20 pp. Hudson, P. J., Dobson, A. P., Lafferty, K. D. (2006). Is a healthy ecosystem one that is rich in parasites? Trends in Ecology and Evolution, 21(7), 381-385. Hughes, J., and Page, R. D. M. (2007). Comparative tests of ectoparasite species richness in seabirds. BMC Evolutionary Biology, 7, 227. Hundt, P. J., Simons, A. M., and Pereira, D. L. (2013). Double-crested cormorants (Phalacrocorax auritus) of Leech Lake, Minnesota: temporal variation of diets and assessment of differential prey selection in adults. American Midland Naturalist, 169, 354-370. Hunt, J. D., and Evans, R. M. (1997). Brood reduction and the insurance-egg hypothesis in double-crested cormorants. Colonial Waterbirds, 20(3), 485-491. Hutton, R. F. and Sogandares-Bernal, F. (1960). Studies on helminth parasites from the coast of Florida. II. Digenetic trematodes from shore birds of the west coast of Florida. Bulletin of Marine Science of the Gulf and Caribbean, 10(1), 40-54. Hutton, R. F. (1964). A second list of parasites from marine and coastal animals of Florida. Transactions of the American Microscopical Society, 83(4), 439-447. Isaksson, N., Evans, T. J., Shamoun-Baranes, J. and Åkesson, S. (2016). Land or sea? Foraging area choice during breeding by an omnivorous gull. Movement Ecology,

40

4(11), 1-14. Jacobson, E. R., Raphael, B. L., Nguyen, H. T., Greiner, E. C., and Gross, T. (1980). Avian pox infection, Aspergillosis and Renal Trematodiasis in a Royal Tern. Journal of Wildlife Diseases, 16(4), 627-631. Johnson, J. H., Ross, R. M., McCullough, R. D., and Mathers, A. (2010). A comparative analysis of double-crested cormorant diets from stomachs and pellets from two Lake Ontario colonies. Journal of Freshwater Ecology, 25(4), 669-672. Jones, A., Bray, R. A., and Gibson, D. I. (Eds.). (2005). Keys to the Trematoda (Vol. 2). London, UK: CABI Publishing and The Natural History Museum. Käkelä, R., Furness, R. W., Kelly, A., Strandberg, U., Waldron, S. and Käkelä, A. (2007). Fatty acid signatures and stable isotopes as dietary indicators in North Sea seabirds. Marine Ecology Progress Series, 342, 291-301. Kamiya, T., O’Dwyer, K., Nakagawa, S., and Poulin, R. (2014). What determines species richness of parasitic organisms? A meta-analysis across animal, plant and fungal hosts. Biological Reviews, 89(1), 123-134. Khalil, L. F., Jones, A. and Bray, R. A. (1994). Keys to the Cestode Parasites of Vertebrates. CAB International: Oxford, UK. Kim, S.-Y. and Monaghan, P. (2006). Interspecific differences in foraging preferences, breeding performance and demography in Herring (Larus argentatus) and Lesser Black-backed Gulls (Larus fuscus) at a mixed colony. Journal of Zoology, 270, 664-671. King, M. M. (1988). Osprey preys on tiger salamander. Journal of Raptor Research, 22(4), 121. Kinsella, J. M., Cole, R. A., Forrester, D. J. and Roderick, C. L. (1996). Helminth parasites of the Osprey, Pandion haliaetus, in North America. Journal of the Helminthological Society of Washington, 63(2), 262-265. Kleinertz, S., Klimpel, S. and Palm, H. W. (2012). Parasite communities and feeding ecology of the European sprat (Sprattus sprattus L.) over its range of distribution. Parasitology Research, 110(3), 1147-1157. Knoff, A. J., Macko, S. A., Erwin, R. M. and Brown, K. M. (2002). Stable isotope analysis of temporal variation in the diets of pre-fledged Laughing Gulls.

41

Waterbirds, 25(2), 142-148. Kuris, A. M., Hechinger, R. F., Shaw, J. C., Whitney, K. L., Aguirre-Macedo, L., Lafferty, K. D. et al. (2008). Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature, 454(7203), 515-518 Lafferty, K. D., Allesina, S., Arim, M. et al. (2008). Parasites in food webs: the ultimate missing links. Ecology Letters, 11, 533-546. Lafferty, K. D. and Morris, A. K. (1996). Altered Behavior of Parasitized Killifish Increases Susceptibility to Predation by Bird Final Hosts. Ecology, 77(5), 1390- 1397. Lamb, J. S. (2016). Ecological Drivers of Brown Pelican Movement Patterns and Reproductive Success in the Gulf of Mexico. Ph. D. Dissertation, Clemson University, Clemson, South Carolina. Lebedeva, D. I. and Yakovleva, G. A. (2016). Trematoda Nematostrigea serpens (Nitzch 1819) Sandground 1934, a New Species in the Parasite Fauna of Birds in Karelia. Biology Bulletin, 43(9), 1018-1023. Levin, I. I., and Parker, P. G. (2013). Comparative host-parasite population genetic structures: Obligate fly ectoparasites on Galapagos seabirds. Parasitology, 140(9), 1061-1069. Liccioli, S., Bialowas, C., Ruckstuhl, K. E and Massolo, A. (2015). Feeding ecology informs parasite epidemiology: prey selection modulates encounter rate with Echinococcus multilocularis in urban coyotes. PLOS ONE, 10(3), 1-14. Lochmann, S. E., Fenech, A. S., and Radomski, A. A. (2004). Seasonal diets of male and female double-crested cormorants from an Oxbow Lake in Arkansas, U.S. Waterbirds, 27(2), 170-176. Locke, S. A., McLaughlin, J. D. and Macrogliese, D. J. (2013). Predicting the similarity of parasite communities in freshwater fishes using the phylogeny, ecology and proximity of hosts. Oikos, 122, 73-83. Locke, S. A., Marcogliese, D. J. and Valtonen, E. T. (2014). Vulnerability and diet breadth predict larval and adult parasite diversity in fish of the Bothnian Bay. Oecologia, 174(1), 253-262. Loreau, M., Roy, J. and Tilman, D. (2001). Linking ecosystem and parasite ecology. In

42

E. A. Schreiber and J. Burger (Eds.), Biology of Marine Birds (pp. 13-177). Boca Raton, FL: CRC Press. Lounsbury-Billie, M. J., Rand, G. M., Cai, Y., and Bass, O. L. (2008). Metal concentrations in osprey (Pandion haliaetus) populations in the Florida Bay estuary. Ecotoxicology, 17(7), 616-622. Lowe, D., Matthews, J. R. and Moseley, C. J. (1990). The Official World Wildlife Fund Guide to Endangered Species of North America. Washington, D.C.: Beacham Pub. Marcogliese, D. J. (2002) Food webs and the transmission of parasites to marine fish. Parasitology, 124, S83-S99. Marcogliese, D. J. (2004) Parasites: Small Players with Crucial Roles in the Ecological Theater. EcoHealth, 1(2), 151-164. Marcogliese, D. J. and Cone, D. K. (1997). Food webs: a plea for parasites. Trends in Ecology and Evolution, 12(8), 320-325. Marini, G., Guzetta, G., Baldacchino, F., Arnoldi, D., Montarsi, F., Capelli, G., Rizzoli, A. et al. (2017). The effect of interspecific competition on the temporal dynamics of Aedes alopictus and Culex pipens. Parasites & Vectors, 10(102), 1-9. Martorelli, S. R., Fredensborg, B. L., Mouritsen, K. N. and Poulin, R. (2004). Description and proposed life cycle of Maritrema novaezealandensis n. sp. (Microphallidae) parasitic in Red-billed Gulls, Larus novaehollandiae scopulinus, from Otago Harbor, South Island, New Zealand. Journal of Parasitology, 90(2), 272-277. McDonald, M. E. (1969). Catalogue of Helminths of Waterfowl (Anatidae). Bureau of Sport Fisheries and Wildlife Special Scientific Report, 85, p. 359. McGinnis, T. W. and Emslie, S. D. (2001). The foraging ecology of Royal and Sandwich Terns in North Carolina, USA. Waterbirds, 24(3), 361-370. McLaughlin, J. D. (2001). Protocols for measuring biodiversity: parasites of birds. Department of Biology, Concordia University, Montreal, Quebec, Canada H3G 1MB and Parasitology Module Steering Committee Parasitology Section, Canadian Society of Zoologists. 36 pp. Montevecchi, W. A. and Myers, R. A. (1997). Centurial and decadal oceanographic influences on changes in northern gannet populations and diets in the north-west

43

Atlantic: implications for climate change. ICES Journal of Marine Science, 54, 608-614. Mutafchiev, Y., Halajian, A. and Georgiev, B. B. (2010). Two new nematode species of the genus Cosmocephalus Molin, 1858 (Spirurida: Acuariidae), with an amended generic diagnosis and an identification key to Cosmocephalus spp. Zootaxa, 2349 (1), 1-20. Muzaffar, S. B. (2009). Helminths of Murres (Alcidae: Uria spp.): Markers of Ecological Change in the Marine Environment. Journal of Wildlife Diseases, 45(3), 672-683. Nelson, J. B. (1978a). The Sulidae. Gannets and Boobies. Oxford, UK: Oxford University Press. Nelson, J.B. (1978b). The Gannet. Calton, UK: T. & A. D. Poyser. Nelson, B. (1979). Seabirds: Their Biology and Ecology. New York, NY: A & W Publishers. Peterson, R. T. (2008). Peterson Field Guide to Birds of North America. Boston, MA: Houghton Mifflin Harcourt. Pettex, E., Lorentsen, S.-H., Grémillet, D., Gimenez, O., Barrett, R., Pons, J.-B. et al. (2012). Multi-scale foraging variability in Northern gannet (Morus bassanus) fuels potential foraging plasticity. Marine Biology, 159(12), 2743-2756. Poole, A. (1985). Feeding and Osprey reproduction. The Auk, 102(3), 479-492. Poulin, R. (1995). Phylogeny, Ecology, and the Richness of Parasite Communities in Vertebrates. Ecological Monographs, 65(3), 283-302. Poulin, R. (1997). Species richness of parasite assemblages: evolution and patterns. Annual Review of Ecology and Systematics, 28, 341-358. Price, P. W. (1980). Evolutionary Biology of Parasites. Princeton, NW: Princeton University Press. Pritchard, M. H. and Kruse, G. O. (1982). The collection and preservation of animal parasites. Lincoln, NE: University of Nebraska Press. Reinhold, D. S., Mueller, A. J. and Ellis, G. (1998). Observations of nesting double- crested cormorants in the Delta Region of Mississippi. Colonial Waterbirds, 21(3), 450-451. Robinson, S. A., Forbes, M. R., and Hebert, C. E. (2009). Parasitism, mercury

44

contamination, and stable isotopes in fish-eating double-crested cormorants: No support for the co-ingestion hypothesis. Canadian Journal of Zoology, 87(8), 740- 747. Robinson, S. A., Forbes, M. R. and Herbert, C. E. (2010). Mercury in parasitic nematodes and trematodes and their double-crested cormorant hosts: Bioaccumulation in the face of sequestration by nematodes. Science of the Total Environment, 408(22), 5439-5444. Rohde, K. (2013). Parasitism. In S. A. Levin (Eds.), Encyclopedia of Biodiversity (2nd Ed.) (pp. 656-673). Cambridge, MA: Academic Press. Pearson, T. H. (1968). The Feeding Biology of Sea-Bird Species Breeding on the Farne Islands, Northumberland. Journal of Animal Ecology, 37(3), 521-552. Santoro, M., Mattiucci, S., Kinsella, J. M. et al. (2011). Helminth community structure of the Mediterranean Gull (Ichthyaetus melanocephalus) in Southern Italy. Journal of Parasitology, 97(2), 364-366. Santoro, M., Kinsella, J. M., Galiero, G., Uberti, B. and Aznar, F. J. (2012). Helminth community structure in birds of prey (Accipitriformes and Falconiformes) in Southern Italy. Journal of Parasitology, 98(1), 22-29. SAS Institute Inc. (2015). Discovering JMP 12®. Cary, NC: SAS Institute Inc. Schmidt, G. D. and Huber, P. M. (1985). Two rare helminths in an Osprey, Pandion haliaetus, in Mexico. Proceedings of the Helminthological Society, 52(1), 139- 140. Schreiber, R. W. and Mock, P. J. (1988). Eastern Brown Pelicans: what does 60 years of banding tell us? Journal of Field Ornithology, 59(2), 171-182. Schreiber, E. A and Schreiber, R. W. (1977). Gulls wintering in Florida: Christmas bird count analysis. Florida Field Naturalist, 5(2), 35-40. Sepúlveda, M. S., Spalding, M. G., Kinsella, J. M., Bjork, R. D. and McLaughlin, G. S. (1994). Helminths of the Roseate Spoonbill, Ajaia ajaja, in Southern Florida. Journal of the Helminthological Society of Washington, 61(2), 179-189. Shealer, D. A. (2001). Foraging Behavior and Food of Seabirds. In E. A. Schreiber and J. Burger (Eds.), Biology of Marine Birds (pp. 137-177). Boca Raton, FL: CRC Press.

45

Shoji, A., Sugiyama, A. and Brazil, M. A. (2011). The status and breeding biology of Ospreys in Hokkaido, Japan. The Condor, 134(4), 762-767. Spear, K. A., Schweitzer, S. H., Goodloe, R., and Harris, D. C. (2007). Effects of management strategies on the reproductive success of least terns on dredge spoil in Georgia. Southeastern Naturalist, 6(1), 27-34. Stucker, J. H., Buhl, D. A., and Sherfy, M. H. (2012). Emergent sandbar construction for least terns on the Missouri River: effects on forage fishes in shallow-water habitats. River Research and Applications, 28, 1254-1265. Sukhdeo, M. V. and Hernandez, A. D. (2001). Food web patterns and the parasite’s perspective. In E. A. Schreiber and J. Burger (Eds.), Biology of Marine Birds (pp. 13-177). Boca Raton, FL: CRC Press. Sukhdeo, M. V. (2010). Food webs for parasitologists: a review. Journal of Parasitology, 96(2), 273-284. Swenson, J. E. (1979). The Relationship between Prey Species Ecology and Dive Success in Ospreys. The Auk, 96(2), 408-412. Threlfall, W. (1968). Studies on the helminth parasites of the American herring gull (Larus argentatus Pont.) in Newfoundland. Canadian Journal of Zoology, 46(6), 1119-1126. Threlfall, W. (1982). Endoparasites of the Double-crested Cormorant (Phalacrocorax auritus) in Florida. Canadian Journal of Zoology, 49(1), 103-108. Torres, L. G. (2009). A kaleidoscope of mammal, bird and fish: habitat use patterns of top predators and their prey in Florida Bay. Marine Ecology Progress Series, 375, 289-304. Ubelaker, J. E. (1965). A new nematode, Pharyngodon boulengerula, from the Caecilian Boulengerula uluguruensis. Journal of the Helminthological Society of Washington, 32(2), 113-115. Votier, S., Bearhop, S., Witt, M. J., Inger, R., Thompson, D., and Newton, J. (2010). Individual responses of seabirds to commercials fisheries revealed using GPS tracking, stable isotopes and vessel monitoring systems. Journal of Applied Ecology, 47, 487-497. Wagner, B. A., Hoberg, E. P., Somers, C. M., Soos, C., Fenton, H., and Jenkins, E. J.

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(2012). Gastrointestinal helminth parasites of Double-crested Cormorants (Phalacrocorax auritus) at four sites in Saskatchewan, Canada. Comparative Parasitology, 79(2), 275-282. Wambach, E. J., and Emslie, S. D. (2003). Seasonal and annual variation in the diet of breeding, known-age Royal Terns in North Carolina. The Wilson Bulletin, 115(4), 448-454. Wardle, W. J., Tehrany, M. R., and Dronen, N. O. (1999). Revision of Bursacetabulus (Diplostomidae: Diplostomidae) with the proposal of Bursatintinnabulus n. gen., and description of Bursatintinnabus bassanus n. sp. and Bursacetabulus morus n. sp. form Northern Gannet, Morus bassanus (Aves), from the Texas Gulf Coast. The Journal of Parasitology, 85(3), 531-533. Washburn, B. E., Bernhardt, G. E., Kutschbach-Brohl, L., Chipman, R. B., Francoeur, L. C. (2010). Temporal variation in terrestrial invertebrate consumption by Laughing Gulls in New York. American Midland Naturalist, 163(2), 442-454. Williams Jr., E. H., Dyer, W. G., Mignucci-Giannoni, A. A., Jiménez-Marrero, N. M., Bunkley-Williams, L., Moore, D. P. and Pence, D. B. (2002). Helminth and arthropod parasites of the Brown Pelican, Pelecanus occidentalis, in Puerto Rico, with a compilation of all metazoan parasites reported from this host in the Western Hemisphere. Avian Pathology, 31, 441-448. Withers, K., Brooks, T. S., and Brush, T. (2004). Diet of double-crested cormorants (Phalacrocorax auritus) wintering on the central Texas coast. Southwestern Naturalist, 49(1), 48-53. Wood, D. R. (2008). Royal Terns capture flying fish in midair. Waterbirds, 31(1), 149- 149. Zuria, I., and Mellink, E. (2005). Fish abundance and the 1995 nesting season of the least tern at Bahía de San Jorge, northern Gulf of California, México. Waterbirds, 28(2), 172-180.

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Appendix 1: Recorded prey items of studied seabird species. Table 4. Diet of the Pelecanus occidentalis (Pelecaniformes) from previous foraging studies. The table notes the geographic location of prey species foraged by the P. occidentalis. References: (1) Clapp et al. 1982 and (2) Hingtgen et al. 1985.

Family Species Prey Species Geographic Location Author Pelecanidae Pelecanus occidentalis Amphistichus argenteus California 1 Anchoa mitchilli Florida 1 Archosargus probatocephalus South Carolina to Texas 1 Brevoortia tyrannus South Carolina to Texas 1, 2 Brevoortia patronus South Carolina to Texas 1, 2 Carangidae sp. Louisiana and Texas 1 Caranx sp. South Carolina to Texas 1 Clupea sp. Netherlands Antilles 1 Cynoscion sp. Florida 1 Diplodus sp. South Carolina to Texas 1 Engraulis mordax California 1 Engraulis sp, Netherlands Antilles 1 Fundulidae sp. Florida 1 Gambusia sp. South Carolina to Texas 1 Gymnura sp. Florida 1 Jenkinsia lamprotaenia Netherlands Antilles 1 Lagodon rhomboides Florida 1, 2 Leiostomus xanthurus South Carolina to Texas 1 Menidia sp. South Carolina to Texas 1 Mugil cephalus Florida 1, 2 Mugil sp. Florida 1, 2 Opisthonema oglinum South Carolina to Texas 1 Orthopristis chrysoptera Florida 2 Polydactylus octonemus Florida 1 Sardinella aurita California 1 Sardinella sp. Netherlands Antilles 1 Sardinops sagax California 1 Scomber japonicas California 1 Symphurus sp. California 1 Urolophus halleri California 1 48 Urotrygon munda California 1

Table 5. Diets of Morus bassanus and Phalacrocorax auritus (Suliformes) from previous foraging studies. The table notes the geographic location of prey items foraged by the M. bassanus and P. auritus, respectively. References: (1) Clapp et al. 1982; (2) Montevecchi and Myers 1997; (3) Lochmann et al. 2004; (4) Withers and Brooks 2004; (5) Garthe et al. 2007; (6) Hamer et al. 2007; (7) Käkelä et al. 2007; (8) Johnson et al. 2010; (9) Dorr et al. 2012; and (10) Hundt et al. 2013.

Family Species Prey Species Geographic Location Authors Sulidae Morus bassanus Ammodytes sp. Funk Island 2 Ammodytes ammodytes Atlantic Ocean 1 Ammodytes marinus United Kingdom 7 Ammodytidae sp. Scotland 6 Callionymus lyra Scotland 6 Carangidae sp. Scotland 6 Clupea harengus Newfoundland, Scotland 1, 2, 5, 6 Clupeidae sp. Scotland 2 Cololabis adocetus Funk Island 2 Gadus morhua Funk Island 2, 5 Gadus sp. Newfoundland 2 Illex illecebrosus Funk Island 2 Loliginidae Atlantic Ocean 2 Mallotus villosus Newfoundland 5 Melanogrammus aeglefinus Scotland, United Kingdom 6, 7 Merlangius merlangus United Kingdom 7 Pleuronectiformes sp. Scotland 6 Pleuronectes platessa United Kingdom 7 Pollachius virens Atlantic Ocean 1 Salmo salar Newfoundland 2, 5 Sardina pilchardus United Kingdom 7 Sciaenidae sp. Scotland 6 Scomber scombrus Newfoundland, Scotland, United Kingdom 1, 5, 6, 7 Scomberesox saurus Funk Island 2 Scombridae sp. Scotland 6 Sprattus sprattus Scotland 6

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Family Species Prey Species Geographic Location Authors Phalacrocoracidae Phalacrocorax Alosa pseudoharengus Ontario 8 auritus Ambloplites rupestris Ontario 8 Ameiurus melas Minnesota 10 Ameiurus natalis Minnesota 10 Ammodytes hexapterus British Columbia 1 Anguilla rostrata Maine, New Hampshire 1 Aplodinotus grunniens Arkansas 3 Apodichthys flavidus British Columbia 1 Ariopsis felis Texas 4 Bagre marina Florida 1 Boleosoma nigrum Manitoba 1 Brevoortia patronus Texas 4 Catostomus commersoni Minnesota 10 Coregonus clupeaformis Alberta 1 Coregonus sp. Minnesota 10 Cottus cognatus Ontario 8 Cryptacanthodes maculatus Nova Scotia 1 Culaea inconstans Minnesota 10 Cymatogaster aggregata British Columbia 1 Cynoscion arenarius Texas 4 Cynoscion nebulosus Texas 4 Cyprinella lutrensis Arkansas 3 Cyprinidae spp. Manitoba, Ontario 8 Dorosoma cepedianum Arkansas, Atlantic and Gulf Coasts 1, 3 Etheostoma exile Minnesota 10 Etheostoma nigrum Minnesota 10 Esox lucius Alberta, Minnesota 1, 10 Fundulus heteroclitus New Hampshire 1 Gasterosteus aculeatus British Columba 1 Gila atraria Utah 1 Ictalurus punctatus Arkansas, Mississippi 3, 9 Leiostomus xanthurus Florida 1 Lepisosteus platyrhincus Florida 1 Lepomis cyanellus Arkansas 3 Lepomis gibbosus Minnesota, Ontario 8, 10 50 Lepomis gulosus Arkansas 3

Family Species Prey Species Geographic Location Authors Lepomis macrochirus Minnesota 10 Lepomis sp. Florida, Minnesota 1, 10 Leptocottus armatus British Columbia 1 Lota lota Minnesota 10 Lumpenus sagitta British Columbia 1 Luxilus cornutus Minnesota 10 Menidia beryllina Arkansas 3 Micropogonias undulatus Texas 4 Micropterus dolomieu Ontario 8 Micropterus salmoides Florida, Minnesota 1, 10 Morone mississippiensis Arkansas 3 Morone chrysops Ontario 3, 8 Moxostoma valenciennesi Minnesota 10 Mugil cephalus Florida, Texas 1, 4 Myoxocephalus aenaeus New Hampshire 1 Myoxocephalus scorpius Nova Scotia 1 Myrichthys breviceps Florida 1 Neogobius melanostomus Ontario 8 Notemigonus crysoleucas Minnesota 10 Notropis aterinoides Minnesota 10 Notropis dorsalis Minnesota 10 Notropis hudsonius Minnesota 10 Notropis sp. Minnesota 10 Noturus gyrinus Minnesota 10 Opsanus beta Florida, Texas 1, 4 Opsanus tau Atlantic and Gulf Coasts 1 Orconectes sp. Minnesota 10 Orthopristis chrysoptera Florida 1 Palemonetes vulgaris South Carolina 1 Perca flavescens Manitoba, Minnesota, Ontario 1, 8, 10 Percina caprodes Minnesota 10 Percopsis omiscomaycus Minnesota 10 Pholis gunnellus Maine, New Hampshire, Nova Scotia 1 Pholis laeta British Columbia 1 Pholis ornata British Columbia 1 51 Pimephales notatus Minnesota 10

Family Species Prey Species Geographic Location Authors Pimephales promelas Minnesota 10 Pitho anisodon Florida 1 Pogonias cromis Texas 4 Pollachius pollachius New Hampshire, Nova Scotia 1 Pomoxis annularis Arkansas 3 Pomoxis nigromaculatus Minnesota 10 Pseudopleuronectes americanus New Hampshire 1 Pungitius pungitius Minnesota 10 Roccus chrysops Utah 1 Sander vitreus Minnesota 10 Scombridae spp. Atlantic and Gulf Coasts 1 Sciaenops ocellatus Texas 4 Sparisoma spp. Florida 1 Tautogolabrus adspersus New Hampshire, Nova Scotia 1 Umbra limi Minnesota 10 Viviparus sp. Minnesota 10

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Table 6. Dietary list of the target species of Pandion haliaetus (Accipitriformes)from previous foraging studies. The table below notes the geographic locations of prey species foraged by the P. haliaetus. References: (1) Swenson 1979; (2) Glass and Watts 2009; (3) Torres 2009; and (4) Beja et al. 2011.

Family Species Prey Species Geographic Location Authors Pandionidae Pandion Abudefduf luridus Cape Verde 4 haliaetus Acanthurus monroviae Cape Verde 4 Alosa mediocris Chesapeake Bay 2 Alosa pseudoharengus Chesapeake Bay 2 Aluterus schoepfii Cape Verde 4 Ariopsis felis Florida 3 Aulostomus strigosus Cape Verde 4 Bagre marinus Florida 3 Brevoortia tyrannus Chesapeake Bay 2 Carangidae Florida 3 Catostomus catostomus Wyoming 1 Catostomus machrocheilus Montana 1 Catostomus tahoensis California 1 Centrarchidae Florida 1 Chelon labrosus Cape Verde 4 Chilomycterus reticulatus Cape Verde 4 Cynoscion nebulosus Chesapeake Bay, Florida 1, 2 Dactyloperus volitans Cape Verde 4 Decapterus macarellus Cape Verde 4 Diplodus fasciatus Cape Verde 4 Diplodus prayensis Cape Verde 4 Diplodus puntazzo Cape Verde 4 Diplodus sargus Cape Verde 4 Dorosoma cepedianum Chesapeake Bay, Florida 1, 2 Dorosoma petenense Chesapeake Bay, Florida 1, 2 Embiotocidae California 1 Esox lucius Norway 1 Etrumeus teres Chesapeake Bay 2 Eucinostomus melanopterus Cape Verde 4 53 Euthynnus alletteratus Cape Verde 4

Family Species Prey Species Geographic Location Authors Exocoetus volitans Cape Verde 4 Fistularia petimba Cape Verde 4 Galeichthys felis Florida 1 Galeoides decadactylus Cape Verde 4 Hemiramphus balao Cape Verde 4 Heteropriacanthus cruentatus Cape Verde 4 Hypomesus pretiosus California 1 Lagodon rhomboides Florida 3 Leiostomus xanthurus Chesapeake Bay 2 Lepomis sp. Florida 1 Leuciscus idus Norway 1 Leuciscus leuciscus Norway 1 Lithognathus mormyrus Cape Verde 4 Micropogonias undulatus Chesapeake Bay 2 Micropterus salmoides Florida 1 Monacanthidae Florida 3 Morone americana Chesapeake Bay 2 Morone saxatilis Chesapeake Bay 2 Mugil cephalus Florida 1, 3 Mugil curema Florida 3 Mulloidichthys martinicus Cape Verde 4 Mullus barbatus Florida 1 Myripristis jacobus Cape Verde 4 Opisthonema oglinum Chesapeake Bay 2 Paralichthys dentatus Chesapeake Bay 2 Perca fluviatilis Norway 1 Pomatomus saltatrix Chesapeake Bay 2 Pomoxis nigromaculatus Florida 1 Pomoxis sp. Florida 1 Prosopium sp. Montana 1 Pseudopleuronectus americanus Nova Scotia 1 Rypticus saponaceus Cape Verde 4 Salmo clarki Wyoming 1 Salmo gairdneri California 1 Salmonidae Oregon 1 54 Sardinella maderensis Cape Verde 4

Family Species Prey Species Geographic Location Authors Sargocentron hastatus Cape Verde 4 Scorpaena scrofa Cape Verde 4 Selar crumenophthalmus Cape Verde 4 Siphateles bicolor California, Oregon 1 Sparidae Florida 3 Sparisoma cretense Cape Verde 4 Spicara melanurus Cape Verde 4 Spirinchus starksi California 1 Trachinotus ovatus Cape Verde 4 Trinectes maculatus Chesapeake Bay 2 Tylosurus acus Cape Verde 4 Virididentex acromegalus Cape Verde 4

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Table 7. Diets of the order Charadriiformes from previous foraging studies. The table notes the geographic location of prey species foraged by Thalasseus maximus, Leucophaeus atricilla, and Larus argentatus, respectively. References: (1) Buckley and Buckley 1971; (2) Clapp et al. 1983; (3) Kim and Monaghan 2006; (4) Breton et al. 2008; and (5) Washburn et al. 2013.

Family Species Prey Species Geographic Location Authors Sternidae Thalasseus Alosa sp. Florida 2 maximus Ammodytes sp. North Carolina, Virginia 2 Anchoa hepsetus Florida 2 Anchoviella spp. Atlantic and Gulf Coasts 1, 2 Anguilla sp. North Carolina 1 Brevoortia tyranus Alabama, Atlantic and Gulf Coasts, Florida, Georgia, 1, 2 North Carolina, Virginia Callinectes sapidus Virginia 1, 2 Caranx sp. Florida, North Carolina, Virginia 1, 2 Chloroscombrus chrysurus Florida 2 Fundulus sp. North Carolina, Virginia 1, 2 Illex illecebrosus Florida 2 Loligo sp. North Carolina, Virginia 1, 2 Menidia spp. Florida, North Carolina, Virginia 1, 2 Micropogonias undulatus Florida 2 Ophidiidae Florida 2 Opsanus sp. North Carolina, Virginia 1, 2 Perca flavescens North Carolina 2 Penaeus spp. Atlantic and Gulf Coasts, Florida 1, 2 Pleuronectidae North Carolina, Virginia 1, 2 Pomatomus saltatrix Atlantic and Gulf Coasts, Florida 2 Syngnathus sp. North Carolina, Virginia 1, 2

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Family Species Prey Species Geographic Location Authors Laridae Leucophaeus Anchoa mitchilli New York 5 atricilla Carcinus maenas New York 5 Caridea Alabama 2 Catharus sp. Delaware 2 Coleoptera Alabama, New York 2, 5 Esox lucius New York 2 Formicidae Alabama, New York 2, 5 Limulidae New York 5 Passeriformes Delaware, Ecuador 2 Rallus longirostris New Jersey 2 Siluriformes sp. Alabama 2

Larus Actitis macularia North America 2 argentatus Aequipecten irradians New Jersey 2 Agelaius phoeniceus North America 2 Alauda arvensis Old World 2 Alca torda Old World 2 Alosa pseudoharengus Lake Ontario, Michigan 2, 4 Ambloplites ruprestris Michigan 2 Ameiurus sp. Michigan 2 Ammodytes americanus New York 2 Anas clypeata NG 2 Anas platyrhynchos Old World 2 Anas strepera Old World 2 Anguilla rostrata Connecticut, Maryland 2 Annelida Maine, New Hampshire 2 Anthus pratensis Old World 2 Arvicola terrestris Old World 2 Asterias forbesi Connecticut 2 Buccinum undatum New Brunswick 2 Bufo bufo North America 2 Busycyon contrarium Florida 2 Busycyon spiratum Florida 2 Calidris alpina NG 2 Calidris pusilla North America 2 57 Callinectes sapidus Connecticut, Florida 2

Family Species Prey Species Geographic Location Authors Cancer sp. Connecticut 2 Carcinus maenas Connecticut 2 Catostomus commersoni Maine 2 Catostomus sp. Manitoba 2 Cepphus grylle North America 2 Charadrius alexandrinus Old World 2 Charadrius hiaticula Old World 2 Clangula hyemalis North America 2 Clethrionomys rufocanus Old World 2 Clupea harengus New Brunswick 2 Coleoptera New Brunswick 2 Crepidula forniculata Connecticut 2 Crepidula plana Connecticut 2 Crex crex NG 2 Cricetus cricetus Old World 2 Cyanocitta cristata North America 2 Cyprinidae Michigan 2 Cyprinus carpio Manitoba 2 Dendroica sp. North America 2 Dendroica virens North America 2 Dinocardium robustum Florida 2 Diptera New Brunswick 2 Dumetella carolinensis North America 2 Echinoidea New Brunswick 2 Empetrum nigrum New Brunswick 2 Ensis directus Connecticut 2 Ephemeroptera Michigan 2 Esox lucius Manitoba 2 Falco sparverius North America 2 Fulica atra Old World 2 Fulmaris glacialis NG 2 Gadidae United Kingdom 3 Gadus morhua New Brunswick 2 Haematopus ostralegus Old World 2 Hirundo rustica NG 2 58 Hymenoptera New Brunswick 2

Family Species Prey Species Geographic Location Authors Ictalurus nebulosus Manitoba 2 Ictalurus spp. Maryland 2 Lacerta sp. North America 2 Lactophrys quadricornis Florida 2 Larus californicus North America 2 Larus canus Old World 2 Larus delawarensis North America 2 Larus fuscus Old World 2 Larus ridibundus Old World 2 Lemmus lemmus Old World 2 Lepidoptera New Brunswick 2 Lepomis auritus Maine 2 Lepomis gibbosus Maine 2 Lepomis sp. Maryland, Michigan 2 Lepus europaeus Old World 2 Libinia dubia Florida 2 Libinia emargina New York 2 Limosa limosa NG 2 Lucina floridana Florida 2 Lunatia heros Connecticut 2 Lytechinus variegatus Florida 2 Macrocallista nimbosa Florida 2 Mallotus villosus Newfoundland 2 Marine mollusc United Kingdom 3 Melanogrammus aeglefinus United Kingdom 3 Melongena corona Florida 2 Melospiza melodia North America 2 Mercenaria campechensis Florida 2 Mercenaria mercenaria Connecticut, New Jersey 2 Mergus serrator North America 2 Merluccius bilinearis Massachusetts 2 Micropterus dolomieui Maine 2 Microtus arvalis Old World 2 Microtus oeconomus Old World 2 Microtus pennsylvanicus North America 2 59 Microtus sp. Manitoba 2

Family Species Prey Species Geographic Location Authors Modiolus demissus Connecticut 2 Molothrus ater North America 2 Morone americana Maine 2 Morus bassanus Old World 2 Motacilla flava Old World 2 Moxostoma macrolepidotum Manitoba 2 Moxostoma sp. Manitoba 2 Mus sp. Old World 2 Mustela erminea Old World 2 Mustela nivalis Old World 2 Mya arenaria Connecticut 2 Mytilus edulis Connecticut, Newfoundland 2 Necturus maculosus North America 2 Nerodia sipedon North America 2 Notemigonus crysoleucas Maine 2 Notropis cornutus Maine 2 Numenius arquata NG 2 Oceanites oceanicus North America 2 Oceanodroma leucorhoa Newfoundland 2 Oceanodroma sp. North America 2 Ogcocephalus sp. Florida 2 Oryctolagus cunilus Old World 2 Osmerus mordax Michigan 2 Ostera virginica New York 2 Ovalipes ocellatus Connecticut 2 Pagurus sp. Connecticut 2 Panopeus herbstii New York 2 Pecten irradians Massachusetts 2 Pleuronectidae United Kingdom 2, 3 Perca flavescens Maine, Manitoba, Michigan 2 Perdix perdix Old World 2 Phalacrocorax auritus North America 2 Phasianus colchicus NG 2 Pholis gunnellus New Brunswick 2 Polinices duplicatus Connecticut 2 60 Pollachius sp. Maine, Massachusetts 2

Family Species Prey Species Geographic Location Authors Pollachius virens New Brunswick 2 Pomatomus saltatrix New York 2 Prionotus carolinus New York 2 Progne subis North America 2 Puffinus puffinus Old World 2 Quiscalus quiscula North America 2 Rana temporaria North America 2 Rangia cuneata North Carolina 2 Rattus norvegicus North America 2 Recurvirostra avosetta Old World 2 Refuse Maine, New Hampshire 2 Rissa tridactyla Old World 2 Salmonidae Maine 2 Sciaenidae United Kingdom 2, 3 Scomber scombrus New Brunswick 2 Scombridae Maine, Massachusetts 2 Sebastes morinus Massachusetts 2 Semotilus corporalis Maine 2 Sillaginidae United Kingdom 2, 3 Somateria mollissima North America 2 Sorex sp. Old World 2 Spisula solidissima New Jersey, New York 2 Steno chrysops New York 2 Sterna dougallii North America 2 Sterna paradisaea Old World 2 Stizostedion vitreum Manitoba 2 Sturnus vulgaris North America 2 Tadorna tadorna Old World 2 Talpa europaea Old World 2 Tamiasciurus hudsonicus North America 2 Tautogolabrus adspersus Connecticut 2 Trachycardium egmontianum Florida 2 Tringa totanus NG 2 Turdus merula Old World 2 Turdus migratorius North America 2 61 Turdus musicus Old World 2

Family Species Prey Species Geographic Location Authors Uria aalge Newfoundland, Old World 2 Vaccinium sp. Maine 2 Vanellus vanellus Old World 2 Viperus berus North America 2 Zenaida macroura North America 2

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Appendix 2: Previously described parasites of studied seabird species.

Table 8. Endoparasites found within the Pelecanus occidentalis (Pelecaniformes) from previous studies. Geographic location is included for each parasite species found in P. occidentalis. Infection site in host: AS = air sacs, BC = body cavity, BV = portal blood vessels, CE = ceca, CL = cloaca, ES = esophagus, GI = gizzard, GL = gizzard lining, GB = gallbladder, IN = intestines, KD = kidney, LI = large intestines, LU = lungs, LV = liver, NG = not given, PR = proventriculus, ST = stomach, SI = small intestines, SW= stomach wall, TR = trachea. References: (1) Dyer et al. 2002; (2) Dronen et al. 2003; and (3) Forrester and Spalding 2003.

Species Parasite species Geographic location Site of Infection Authors Pelecanus Acanthocephala occidentalis Andracantha gravida Florida, Louisiana, Texas SI 2, 3 Corynosoma sp. Florida, Texas SI 1, 2, 3 Southwellina breve Texas SI 2 Southwellina hispida Florida, Louisiana SI, CE, LI 1, 2, 3

Cestoda Cyclustera ibisae Florida SI, LI 1, 3 Glossocerus caribaensis Florida SI 3 Ligula intestinalus Germany NG 2 Paratetrabothrius orientalis Mexico NG 1, 2 Parvitaenia eudocimi Cuba NG 2 Parvitaenia heardi Florida, Louisiana NG 1, 2 Raillietina sp. Peru NG 2 Tetrabothrius sp. Florida, Louisiana SI, CL 1, 2, 3 Tetrabothrius sulae Mexico, Puerto Rico NG 1, 2 Trigonocotyle sp. Peru NG 2 Unidentified sp. Florida, Louisiana NG 2

Digenea Ascocotyle longa Florida, Louisiana, Texas CE, CL, LI, SI 2, 3 Ascocotyle sp. Florida SI 1, 2, 3 Austrobilharzia terrigalensis Florida, Louisiana NG 2

63 Austrobilharzia sp. Florida BV 1, 2, 3

Bolbophorus confusus Arkansas, Texas, Louisiana, Mississippi SI 1, 2

Species Parasite species Geographic location Site of Infection Authors Bursacetabulus pelecanus Texas SI 1, 2 Bursatintinnabulus macrobursus Texas CE, SI 1, 2 Carneophallus turgidus Florida, Texas CE, SI 1, 2, 3 Echinochasmus dietzevi Florida NG 2 Echinochasmus donaldsoni Texas SI 2 Echinochasmus sp. Dominica, Florida, Louisiana, Texas, Puerto Rico CE, SI 1, 2, 3 Galactosomum darbyi Florida NG 1, 3 Galactosomum fregatae Florida CL, SI 1, 2, 3 Galactosomum puffini Panama, Puerto Rico, Texas SI 1, 2 Galactosomum sp. Florida NG 1, 2, 3 Gigantobilharzia sp. Florida NG 1 Mesostephanus appendiculatoides Florida, Louisiana, Panama, Puerto Rico, Dominica CE, CL, LI, SI 1, 2, 3 Mesostephanus microbursa Florida, Lousiana, Panama, Puerto Rico, Texas CE, CL, LI 1, 2 Mesostephanus yedeae Florida SI 1, 2, 3 Mesostephanus sp. Texas NG 2 Microparyphium facetum Florida SI 1, 2, 3 Paracoenogonimus ovatus Germany NG 1, 2 Phagicola minutus Florida, Louisiana NG 1, 2 Pholeter anterouterus Florida NG 1, 2 Prohemistomum appendiculatoides Dominica NG 2 Renicola thapari Florida SI 1, 2, 3 Ribeiroia ondatrae Puerto Rico NG 1, 2 Stephanoprora denticulata Florida, Louisiana NG 1, 2, 3

Nematoda Anisakis sp. Chile NG 2 Capillaria contorta Florida, Louisiana NG 1, 2, 3 Capillaria mergi Florida NG 1, 2, 3 Capillaria sp. Texas CE, CL, LI, SI 2 Contracaecum mexicanum Mexico NG 1, 2 Contracaecum microcephalum Florida ST 3 Contracaecum multipapillatum Florida, Louisiana, Mississippi, Puerto Rico ST 1, 2, 3 Contracaecum ruldolphii Florida, Louisiana, Mississippi, Puerto Rico ST 1, 2, 3 Contracaecum spiculigerum Florida, Louisiana, Puerto Rico ST 2

64 Contracaecum spp. Florida, Louisiana, Peru NG 1, 2, 3

Species Parasite species Geographic location Site of Infection Authors Cosmocephalus obvelatus Florida, Louisiana, Texas ES, PR, ST 1, 2, 3 Cyathostoma phenisci Florida LU, TR 1, 2, 3 Eustrongylides sp. Florida, Puerto Rico PR 1, 2, 3 Gnathostoma spinigerum Mexico NG 2 Paracuaria tridentata Florida, Louisiana ES, PR 1, 2, 3 Physaloptera maxillaris Mexico NG 1, 2 Physaloptera sp. Florida SI 1, 2, 3 Syngamus sp. Peru NG 1, 2 Synhimantus invaginatus Louisiana NG 1, 2 Synhimantus sp. Florida NG 3 Tetrameres inerme Florida PR 1, 2, 3 Tetrameres sp. Texas ST 2

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Table 9. Endoparasites found within Morus bassanus and Phalacrocorax auritus (Suliformes) from previous studies. Geographic location is included for each parasite species found in M. bassanus and P. auritus. Infection site in host: AS = air sacs, BC = body cavity, BV = portal blood vessels, CE = ceca, CL = cloaca, ES = esophagus, GA = gastrointestinal, GI = gizzard, GL = gizzard lining, GB = gallbladder, IN = intestines, KD = kidney, LI = large intestines, LU = lungs, LV = liver, NG = not given, PR = proventriculus, ST = stomach, SI = small intestines, SW= stomach wall, TR = trachea. References: (1) Threlfall 1982; (2) Wardle et al. 1999; (3) Dronen et al. 2003; (4) Forrester and Spalding 2003; (5) Robinson et al. 2009; (6) Wagner et al. 2012; and (7) Mendes et al. 2013.

Species Parasite species Geographic location Site of Infection Authors Morus Cestoda bassanus Tetrabothrius bassani Portugal IN 7

Digenea Ascocotyle sp. Florida IN 4 Bursacetabulus morus Texas SI 2 Bursatintinnabulus bassanus Florida, Texas SI 2, 4 Cryptocotyle lingua Germany NG 2 Diplostomum spathaceum NG NG 2 Echinostoma sp. Florida IN 4 Galactosomum cochleariforme Florida IN 4 Galactosomum sp. Florida IN 4 Mesostephanus sp. Florida IN 4 Stephanoprora sp. Florida IN 4

Nematoda Capillaria sp. Florida IN 4 Contracaecum sp. (imm) Florida ST 4 Contracaecum sp. Florida IN 4 Cosmocephalus sp. Florida IN 4

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Species Parasite species Geographic location Site of Infection Authors Phalacrocorax Acanthocephala auritus Andracantha gravida Florida SI 4 Andracantha spp. Florida CE, LI, SI 1, 4 Corynosoma sp. Florida LI 4 Polymorphus obtusus Florida LI 4 Pomphorhynchus bulbocolli Canada ST 6

Cestoda Cyclustera sp. Florida SI 4 Diphyllobothrium sp. Canada GA 6 Ligula colymbi Canada PR 6 Paradilepsis caballeroi Canada IN 6 Paradilepsis sp. Canada IN 6 Parvitaenia eudocimi Canada GA 1 Schistocephalus solidus Canada IN 6

Digenea Ascocotyle longa Canada, Florida SI 1, 4 Clinostomum attenuatum Florida TR, LU 4 Clinostomum marginatum Florida SI 1, 4 Drepanocephalus spathans Canada, Florida SI 1, 4, 6 Drepanocephalus sp. Florida SI 4 Hysteromorpha triloba Florida SI 4 Hysteromorpha sp. Florida SI 4 Mesostephanus appendiculatoides Florida SI 1, 4 Mesostephanus sp. Florida SI 4 Ornithobilharzia sp. Florida BV 1, 4 Parorchis acanthus Canada, Florida CL 1, 4 Phagicola diminuta Florida SI 4 Phagicola sp. Florida NG 4 Renicola thapari? Florida KD 1, 4 Ribeiroia ondatrae Canada, Florida SI 6 Ribeiroia sp. Florida SI 4

67

Species Parasite species Geographic location Site of Infection Authors Nematoda Capillaria carbonis Florida CE, LI, SI 1, 4 Capillaria contorta Florida ES 1, 4 Contracaecum multipapillatum Florida ST 4 Contracaecum rudolphii Canada, Florida ES, ST 4, 6 Contracaecum spp. Florida ES, GI, PR 1, 4, 5 Desmidoercella incognita Florida AS, LU, TR 1, 4 Desmidoercella sp. Florida LU, TR 4 Eustrongylides sp. Florida NG 4 Skrjabinocara squamatum Florida ES, ST 1, 4 Syngamus trachea Florida TR 4 Syncuaria squamata Canada, Florida PR 6 Tetrameres microspinosa Florida ES, ST 1, 4 Tetrameres sp. Florida PR 4

68

Table 10. Endoparasites found within Pandion haliaetus (Accipitriformes) from previous studies. Geographic location is included for each parasite species found in P. haliaetus. Site of infection in host: AS = air sacs, BC = body cavity, BV = portal blood vessels, CE = ceca, CL = cloaca, CS = conjunctival sac, DU = duodenum, ES = esophagus, GB = gallbladder, GI = gizzard, GL = gizzard lining, GB = gallbladder, IN = intestines, KD = kidney, LI = large intestines, LU = lungs, LV = liver, NM = nictitating membrane, NS = nasal sinuses, NG = not given, OR = orbit, OS = orbital sinuses, PR = proventriculus, RE = rectum, ST = stomach, SI = small intestines, SW= stomach wall, TR = trachea. References: (1) Schmidt and Huber 1985; (2) Kinsella et al. 1996; and (3) Forrester and Spalding 2003.

Species Parasites Found Geographic location Site of Infection Authors Pandion Acanthocephala haliaetus Andracantha mergi Florida, Maryland SI 2, 3 Neoechinorhynchus chrysemydis Florida SI 3 Polymorphis brevis Florida SI 3

Cestoda Cyclustera ibisae Florida SI 3 Paradilepis rugovaginosus Florida, Maryland SI 2, 3 Paradilepis simoni Montana SI 2

Digenea Ascocotyle angrense Florida SI 3 Ascocotyle longa Florida, South Carolina SI 2 Ascocotyle sp. Florida, South Carolina SI 2, 3 Clinostomum complanatum Florida PR 3 Cryptocotyle lingua Massachusetts SI 2 Echinochasmus dietzevi Florida SI 2, 3 Mesoophorodiplostomum pricei Florida, Massachusetts, Montana, Virginia SI 2, 3 Mesostephanus appendiculatoides Florida SI 3 Nematostrigea serpens Virginia SI 2 Neodiplostomum sp. Maryland SI 2 Neogogatea pandionis Florida, Virginia SI 2, 3 Pandiontrema ryjikovi Washington SI 2 Posthodiplostomum minimum Florida SI 3 Pygiodopsis pindoramensis Florida SI 2, 3

69

Renicola ralli Florida KD 2, 3

Species Parasites Found Geographic location Site of Infection Authors Ribeiroia ondatrae Florida, Massachusetts, Virginia PR 2, 3 Scaphanocephalus expansus Africa, Asia, Europe, Florida, Iowa, Mexico SI 1, 2, 3 Stephanoprora denticulata Florida SI 2, 3

Nematoda Capillaria falconis Florida SI 2, 3 Cardiofilaria pavlovskyi Florida BC 2, 3 Contracaecum multipapillatum Florida, South Carolina PR 2, 3 Contracaecum pandioni Florida PR 2, 3 Contraecaecum sp. Florida PR 3 Contracaecum spiculigerum Massachusetts, Montana, Virginia PR 2 Sexanoscara skrjabini Florida, Georgian SSR, Maryland, Mexico, ES 1, 2, 3 Russia Tetrameres microspinosa Florida PR 3 Tetrameres sp. Virginia PR 2

70

Table 11. Endoparasites found within the order Charadriiformes from previous studies. Geographic location is included for each parasite species found in Thalasseus maximus, Leucophaeus atricilla, and Larus argentatus. Parasites are noted by the geographic location and infection site found within host species. Infection site in host: AS = air sacs, BC = body cavity, BV = portal blood vessels, CE = ceca, CL = cloaca, CS = conjunctival sac, DU = duodenum, ES = esophagus, GB = gallbladder, GI = gizzard, GL = gizzard lining, GB = gallbladder, IN = intestines, KD = kidney, LI = large intestines, LU = lungs, LV = liver, NM = nictitating membrane, NS = nasal sinuses, NG = not given, OR = orbit, OS = orbital sinuses, PR = proventriculus, RE = rectum, ST = stomach, SI = small intestines, SW= stomach wall, TR = trachea. References: (1) Hutton and Sogandares-Bernal 1960; (2) Hutton 1964; (3) Dubois 1968; (4) Threlfall 1968; (5) Ubelaker 1965; (6) Jacobson et al. 1980; (7) Sepúlveda et al. 1994; (8) Bustnes and Galaktionov 1999a; (9) Bustnes and Galaktionov 1999b; (10) Forrester and Spalding 2003; (11) Dronen et al. 2007; and (12) Santoro et al. 2011.

Species Parasites Found Geographic Location Site of Infection Authors Thalasseus Cestoda maximus Angularella sp. Texas IN 11 Dilepis sedowi Antarctica IN 11 Tetrabothrius cylindraceus North America IN 11

Digenea Cardiocephaloides brandesii Columbia, Texas IN 11 Cardiocephaloides medioconiger Cuba, Florida SI 11 Cardiocephaloides megaloconus Florida, Puerto Rico IN 10, 11 Galactosomum cochleariforme Puerto Rico IN 11 Galactosomum puffini Columbia, Puerto Rico IN 11 Mesostephanus fajardensis Texas IN 11 Natterophthalmus andersoni California, Florida, Texas OR 11 Natterophthalmus hegeneri Florida OR 11 Natterophthalmus lacrymosus Brazil CS 11 Opisthovarium elongatum Puerto Rico IN 11 Ornithobilharzia canaliculata Brazil, Florida BV 10, 11 Pachytrema sanguineum Florida GB 10, 11 Pachytrema sp. Florida GB 2, 10, 11 Parorchis acanthus Sierra Leone, Texas CL 11 Philophthalmus andersoni Florida NM 10 71 Philophthalmus hegeneri Florida NM 10

Species Parasites Found Geographic Location Site of Infection Authors Renicola cruzi Brazil KD 6, 11 Renicola glandoloba Florida KD 2, 10, 11 Renicola sp. Florida KD 11 Retevitellus spinetus Puerto Rico IN 11 Stephanoprora brachyrhynchos Columbia IN 11 Stephanoprora conciliata Texas IN 11 Stephanoprora denticulata Louisiana, Texas IN 11 Stephanoprora sp. Florida IN 10, 11 Stictodora acanthotrema Brazil, Puerto Rico IN 11 Strictodora cablei Texas IN 11 Strictodora johnsoni Puerto Rico IN 11 Stictodora lariformicola Florida RE 5, 10, 11 Stictodora sp. Florida, Puerto Rico IN 2, 10, 11

Nematoda Capillaria sp. Florida IN 10 Contracaecum sp. Texas ST 11

Leucophaeus Cestoda atricilla Paricterotaenia sp. Florida SI 10

Digenea Cardiocephaloides medioconiger Panama NG 3 Cardiocephaloides megaloconus Florida SI 10 Cotylurus aquavis Florida SI 10 Diplostomum spathaceum Newfoundland SI 4 Galactosomum fregatae Florida CL 1, 10 Galactosomum spinetum Florida SI 10 Galactosomum sp. Florida NG 1, 2 Gymnaecotyla adunca Florida SI 2, 10 Microphallus pygmaeus Experimental NG 2 Pachytrema sanguineum Florida SI 1, 2, 10 Philophthalmus hegeneri Florida NM 10 Philophthalmus larsoni Florida NM 10

72 Renicola glandoloba Florida KD 2, 10

Species Parasites Found Geographic Location Site of Infection Authors Stephanoprora denticulata Florida NG 1 Stictodora lariformicola Florida SI 10

Nematoda Synhimantus diacantha Florida NG 7

Larus Acanthocephala argentatus Arhythmorhynchus longicollis Newfoundland IN 4 Falsifilicollis kenti Newfoundland SI 4 Plagiorhynchus formosus Newfoundland IN 4

Cestoda Diphyllobothrium sebago Newfoundland NG 4 Anomotaenia larina Newfoundland IN 4 Anomotaenia micracantha Newfoundland DU 4 Hymenolepis arguei Newfoundland SI 4 Hymenolepis cirrosa Newfoundland SI 4 Hymenolepis lateralis Newfoundland NG 4 Microsomacanthus ductilis Newfoundland DU 4 Tetrabothrius cylindraceus Italy SI 4, 12 Tetrabothrius erostre Newfoundland SI 4

Digenea Brachylaima fuscatus Newfoundland SI 4 Cryptocotyle lingua Florida, Newfoundland SI, DU 1, 2, 4, 8, 9, 10 Diplostomum spathaceum Newfoundland SI 4 Gymnophallus deliciosus Florida, Newfoundland SI, GB 2, 4, 10 Himasthla compacta Newfoundland IN 4 Himasthla elongata Newfoundland IN 4 Himasthla sp. Kirkenes, Novaya Zemiya, Tromsø IN 8, 9 Mesoophorodiplostomum pricei Newfoundland, U.S.A. NG 4 Microparyphium facetum Florida NG 7 Microphallus piriformes Kirkenes, Novaya Zemiya, Tromsø NG 8, 9 Microphallus pygmaeus Kirkenes, Novaya Zemiya, Tromsø NG 9

73 Microphallus similis Kirkenes, Novaya Zemiya, Tromsø NG 8, 9

Species Parasites Found Geographic Location Site of Infection Authors Parorchis acanthus Newfoundland NG 4 Plagiorchis maculosus Newfoundland NG 4 Renicola sp. Kirkenes, Novaya Zemiya, Tromsø NG 9 Ornithobilharzia lari Newfoundland BV 4 Stephanoprora pseudoechinata Newfoundland NG 4 Stephanoprora denticulata Florida SI 1, 2, 7, 10 Stictodora lariformicola Florida, Newfoundland LI 10

Nematoda Capillaria contorta Newfoundland GI, PR 4 Contracaecum spiculigerum Newfoundland GI, PR 4 Contracaecum sp. Newfoundland GI, PR 4 Cosmocephalus aduncus Newfoundland GI, PR 4 Cosmocephalus firlottei Newfoundland GI, PR 4 Cosmocephalus obvelatus Newfoundland GI, PR 4 Cyatostoma lari Newfoundland NS, OS 4 Paracuaria macdonaldi Newfoundland GI, PR 4 Paracuaria tridentata Newfoundland GI, PR 4 Porrocaecum semiteres Newfoundland GI, PR 4

74

Table 12. Parasite species diversity of targeted seabird species. Parasite taxa are listed by class Cestoda and Digenea and phylum Nematoda and Acanthocephala. Numbers for each parasite taxa represent the total number of identified parasite species within the seven seabird hosts. The N-values represent the number of seabird specimens examined as of January 2018.

Brown Double-crested Northern Laughing Herring gull Royal tern Osprey Parasite Taxa pelican cormorant gannet gull (N=12) (N=30) (N=27) (N=33) (N=33) (N=31) (N=40) Cestoda 1 1 1 0 1 1 1 Digenea 9 9 14 3 4 9 8 Nematoda 4 3 1 1 1 1 1 Acanthocephala 2 2 1 0 0 0 1 Total parasite 16 15 17 4 6 11 11 taxa

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Table 13. Resemblance matrix values for host phylogeny. Host taxonomy for each of the seven studied seabird hosts includes the categories of genus, family, order, and class. Taxonomic rankings were used to determine if similarity existed among each studied species and if host phylogeny influenced the structure and composition of parasite communities.

Host Taxonomy Genus Family Order Class Pelecanus occidentalis Pelecanus Pelecanidae Pelecaniformes Aves Morus bassanus Morus Sulidae Suliformes Aves Phalacrocorax auritus Phalacrocorax Phalacrocoracidae Suliformes Aves Pandion haliaetus Pandion Pandionidae Accipitriformes Aves Thalasseus maximus Thalasseus Laridae Charadriiformes Aves Leucophaeus atricilla Leucophaeus Laridae Charadriiformes Aves Larus argentatus Larus Laridae Charadriiformes Aves

76

Table 14. Resemblance matrix values for host feeding range. Distance from shore is represented as inshore (1), coastal (2), and offshore (3) for each of the seven seabird species. Species feeding inshore (e.g., ospreys, cormorants, and gulls) were calculated as two units away from species feeding offshore (e.g., northern gannets), while species feeding coastal (e.g., pelicans and terns) were one unit away from both inshore and offshore feeders. Distance from shore values were used in RELATE to determine if feeding range influenced parasite communities within the targeted seabird species.

Avian Hosts Distance from shore Brown pelican 2 Northern gannet 3 Double-crested cormorant 1 Osprey 1 Royal tern 2 Laughing gull 1 Herring gull 1

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Table 15. Resemblance matrix values for host feeding technique. Feeding techniques used by each seabird species is listed below with an absence (0) or presence (1) approach. Seabird species that displayed feeding techniques (noted from observational literature) were given a 1, while absence of feeding techniques was denoted as 0. Values were calculated through RELATE to determine if feeding techniques influenced the structure and composition of parasite communities within the studied seabirds.

Techniques Surface seizing Plunge diving Kleptoparasitism Pursuit diving Dipping Scavenging Brown pelican 1 1 1 0 0 0

Northern gannet 0 1 0 1 0 0

Double-crested cormorant 0 0 0 1 0 0

Osprey 1 0 0 0 0 0

Royal tern 0 1 1 0 1 0

Laughing gull 1 0 1 0 1 1

Herring gull 1 0 1 0 1 1

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Table 16. Resemblance matrix values for host prey preference. Host prey preference was calculated using an absence (0) or presence (1) approach. Presence of food items was noted with a 1, while absence of prey items was denoted by a 0. Prey items were based on previous literature (e.g., gut content analyses of studied species and observational recordings). Values were calculated through RELATE to determine if prey preference influenced the structure and composition of parasite communities within the seven studied seabirds.

Food Teleosts Amphibians Arthropods Vegetation Reptiles Birds Molluscs Echinoderms Garbage preference Brown 1 0 0 0 0 0 0 0 0 pelican

Northern 1 0 0 0 0 0 1 0 0 gannet Double- crested 1 1 1 1 0 0 0 0 0 cormorant

Osprey 1 1 0 0 1 1 0 0 0

Royal tern 1 0 1 0 0 0 1 0 0

Laughing gull 1 0 1 1 0 0 0 0 1

Herring gull 1 1 1 1 1 1 1 1 1

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Appendix 3: Descriptions of Identified Helminth Species

Digenea

Ascocotyle longa Ransom, 1920 Synonymized: Ascocotyle arnaldoi Travassos, 1928; Parascocotyle longa Ransom, 1920; Phagicola longus Ransom, 1920

Description: Body is small and pyriform. Oral sucker long and well-developed with sinuous posterior appendage (ends at anterior of pharynx). Single row of 14-17 circumoral spines around oral sucker. Prepharynx very long; pharynx present and muscular in mid-body. Ventral sucker symmetrical and subspherical. Numerous eggs. Vitelline fields in two lateral rows. Reproductive organs were not able to be distinguished due to vitelline follicles.

Host: P. occidentalis, M. bassanus, P. auratus

Location: Intestines

Images are of original content unless otherwise stated.

80

Austrobilharzia sp. Johnston, 1917

Description: Total body length 4.34 mm and 4.05 mm long based on two obtained samples. Moderately long prepharynx. Oesophagus bifurcates in front of acetabulum. Gynaecophoric canal beginning at posterior edge of acetabulum to posterior end of body. Oral and ventral sucker well-developed. Oral sucker 123mm long by 85.7 mm wide. Ventral sucker 158 mm long by 193 mm wide. Unable to determine characteristics of reproductive organs due to closed gynaechophoric canal.

Host: M. bassanus

Location: Intestinal blood vein

81

Cardiocephaloides medioconiger Dubois and Perez-Vigueras, 1949

Description: Body is distinctly bipartite with moderate constriction at neck. Total body length approximately 9.49 mm. Forebody small compared to hindbody and pear-shaped. Vitellaria located in hindbody only; not situated in posterior end. Testes tandem. Copulatory bursa evaginable and voluminous, moderate to small across all samples, 0.66 to 1.60 mm long; occasional terminal ends with sphincters. Numerous eggs.

Host: L. atricilla, T. maximus

Location: Intestines

82

Cardiocephaloides brandesii Szidat, 1928 Synonymized: Cardiocephalus brandesii Szidat, 1928

Description: Body distinctly bipartite. Body length ranges from 3.25 mm to 7.30 mm long. Forebody smaller than hindbody and cup-shaped, 0.49 mm to 0.79 mm long. Testes mildly lobed; anterior 0.39 mm by 0.24 mm, posterior 0.39 mm by 0.25 mm. Ovary 0.20 mm by 0.18 mm. Eggs numerous, 17 to 46.

Host: L. atricilla, L. argentatus smithsonianus

Location: Intestines

83

Clinostomum sp. Leidy, 1856

Description: Relatively large body; linguiform shape. Collar-like fold at oral sucker, similar to hood of a jacket. Prepharynx and oesophagus either extremely poorly developed or absent. Large, well-developed, muscular ventral sucker. Vitelline fields are lateral near extreme posterior end to almost anterior/level of ventral sucker. Uterus in intercaecal space between vitelline follicles.

Host: P. haliaetus

Location: Trachea

84

Drepanocephalus spathans Dietz, 1909 Synonym: Drepanocephalus auritus Kudlai, Kostadinova, Pulis and Tkach, 2015

Description: Body elongate. Head collar falciform, muscular, but not distinct from body. 27 collar spines; 19 collar spines single row and 2x2 angled spines. Oral sucker subterminal, circular. Short prepharynx. Pharynx elongate-oval and muscular. Oesophagus long. Ventral sucker well developed, muscular, and deep cavity (cup- shaped); located mid-body. Genital pore terminating at posterior.

Host: P. auritus

Location: Intestines

85

Galactosomum cochleariforme (Rudolphi, 1819) Pratt, 1911 Synonymized: Galactosomum cochleariformum (Rudolphi, 1819) Pratt, 1911; Microlistrum cochleariforme (Rudolphi, 1819) Braun, 1901

Description: Body elongate. Forebody short and spatulate-shaped. Oral sucker subterminal. Prepharynx short and wide. Ventral sucker sinistral to gonotyl, but smaller compared to oral sucker. Testes lobed and slightly diagonal from each other; surrounded by arms of uterus. Ceca terminates near posterior end.

Host: M. bassanus, T. maximus, P. haliaetus

Location: Intestines

86

Galactosomum darbyi Price, 1934 Synonymized: Sobelephya darbyi (Price, 1934) Yamaguti, 1958; Stictodora darbyi Price, 1934

Description: Body elongate. Prepharynx long. Oesophagus short. Caeca slender. Ventrogenital sac median/mid-body. Gonads found 3/4th of body (ovary and testes). Testes large, rounded, and diagonal; anterior testis sinistral and posterior testis dextral. Ovary dextral and opposite of posterior end of seminal vesicle. Seminal vesicle one- chambered, large, and slightly inclined to the right with thin walls. Vitelline follicles scattered throughout (dorsal to ventral), but extends anteriorly to ovary and beyond length of caeca. Uterus does not reach posterior end.

Host: P. occidentalis

Location: Intestines

87

Galactosomum puffini Yamaguti, 1941

Description: Bottle-shaped with posterior end more pointed than anterior. Cuticle spinose beginning at anterior end to beginning of anterior testes. Prepharynx slightly longer than pharynx. Pharynx is oval in shape. Esophagus is short, about as wide as long. Vitelline follicles are roseatte-shaped near posterior end to seminal receptacle (immediately posterior to and larger than ovary). Uterus extends from below ventral sucker (close to ventrogenital sac); right field at same level as ovary, left field is middle of seminal receptacle. Forebody slender (not displayed due to mounting). Anterior testis oval and posterior testis round (difficult to accurately determine due to heavy presence of eggs); slightly separated by uterus. Numerous eggs.

Host: M. bassanus

Location: Intestines

88

Galactosomum spinetum Braun, 1901 Synonymized: Microlistrum spinetum Braun, 1901

Description: Body flattened and lanceolate. Widest at ovary level. Tapering at both ends with posterior being more pointed. Oral sucker large with short prepharynx. Pharynx almost equal in length to prepharynx and well-developed; almost as long as oral sucker. Ventrogenital sac around 40/100ths from anterior end and situated far behind caeca bifurcation; small, median, and obscured by terminal coils of uterus. Seminal vesicle wide, broadly joined sacculations; proximal end sinistral to ovary. Caeca straight and end slightly before posterior end. Ventral sucker small, but lacks thick, circular muscle fibres; rows of spines present (~5-8 rows) encircling apex with central small spineless area. Oesophagus about 1/4th of pharynx, difficult to determine due to sudden appearance of caeca bifurcation. Ovary rounded, medial range, and dextral. Seminal receptacle contiguous and tandem with ovary. Testes large and tandem (separation by uterus). Vitellaria mostly lateral arrangement and beginning between ovary and ventral sucker to behind posterior testis; follifular, in rosettes; descends right of anterior testes, crosses between testes, passes ovary on left, loops across seminal vesicle. Numerous eggs throughout coils of uterus.

Host: L. atricilla

Location: Intestines

89

Hysteromorpha corti Hughes, 1929

Description: Body shape pyriform and triangular. Greatest diameter level with ventral sucker. Ventral sucker well developed and elongate, and slightly below caeca. Prepharynx absent. Pharynx muscular and spherical. Oesophagus short. Anterior trilobate; oral sucker situated on median lobe with lateral lobes as pseudosuckers. Testes tandem. Vitelline fields in fore- and hindbody.

Host: P. auritus

Location: Intestines

90

Ichthyocotylurus erraticus (Rudolphi, 1809) Odening, 1969

Description: Body bipartite; forebody cup-shaped, hindbody less than six times the length of forebody. Neck region extremely short or absent. Hindbody cylindrical, curved dorsally. Bulb size 1.02 mm long. Hindbody 3.65 mm long.Testes tandem. Genital bulb present. Average number of eggs 28. Egg size 103 µm long by 64.2 µm wide.

Host: M. bassanus

Location: Intestines

91

Mesoophorodiplostomum pricei Krull, 1934

Description: Body distinctly bipartite. Absent pseudosuckers near anterior region. Vitellarium in fore- and hindbody (in front of ventral sucker for forebody and at the level of posterior border of second testis). Oral and ventral sucker weakly developed; holdfast organ almost almond shaped, median slit slightly distorted. Pharynx small. Forebody slightly concaved resembling lanceolate shape. Hindbody resembling claviform (club- like) shape. Genital cone surrounded by prepuce. Extrusability of bursa copulatrix.

Host: P. haliaetus

Location: Intestines

92

Mesostephanus appendiculatoides Price, 1934

Description: Body shape alternates between linguiform and foliform. Tribocytic organ distinct and well developed, slit-like, surrounded by vitellaria. Vitellaria encircling posterior to ventral sucker, surrounding holdfast organ and gonads, but not confluent posterior; does not enter conical extension. Prepharynx short to absent. Pharynx and mouth almost contiguous. Cirrus sac well developed, located next to genital opening on right side. Sphincter at distal end distinct (metraterm). Testes present and oval-shaped. Few eggs.

Host: P. occidentalis, P. auritus, M. bassanus

Location: Intestines

93

Mesostephanus fajardensis Price, 1934

Description: Body shape alternates between linguiform and foliform. Body measurements 1.30 long by 0.76 wide. Tribocytic organ distinct and well-developed, slit-like, surrounded by vitellaria. Vitellaria encircling posterior to ventral sucker, surrounding holdfast organ and gonads, but not confluent posterior; does not enter conical extension. Prepharynx short to absent. Pharynx and mouth almost contiguous. Cirrus sac well- developed, located next to genital opening on right side. Sphincter at distal end distinct (metraterm). Testes present and oval-shaped. Numerous eggs measuring 0.06 by 0.04 mm.

Host: P. occidentalis, P. auritus, M. bassanus

Location: Intestines

94

Nematostrigea serpens Nitzsch 1819

Description: Body elongated with clear distinction of anterior and posterior segments from pronounced “neck” region. Total body length 14.2 mm long. Anterior end funnel- shaped, 1.16 mm long. Neck length 7.59 mm long. Oral sucker small, 0.13 mm long by 0.08 mm wide. Unable to determine measurements of pharynx due to poor condition of specimen sample. Acetabulum 0.18mm long by 0.20 mm wide. Testes tandem with posterior larger than anterior, 0.74 mm long by 0.53 mm wide and 0.57 mm long by 0.44 mm wide, respectively. Testes not lobed. Ovary oval to round and tandem to anterior testes, 0.20 mm long by 0.21 mm wide. No visible eggs present. Obligate parasites of ospreys.

Host: P. haliaetus

Location: Intestines

95

Ornithobilharzia sp. Odhner, 1912

Description: Male longer than female, but both genders can be of equal length. Male was twice as long as female. Male exhibits well-developed gynaecophoric canal; forms in- fold of lateral edges of body. Female elongate, slender, and flattened. Ovary elongated and loosely coiled; situated in anterior third of body. Vitellaria extensive (extends two- thirds of body length), following immediately after ovary. Oral sucker and acetabulum distinct and of near equal size in male; unable to accurately determine oral sucker of female, which may be due to distortion during mounting. Acetabulum of female not visibly present. Cuticle covered with spines for both sexes. Male approximately 12mm long; female 7.5-8mm long (not described in taxonomic keys).

Host: L. argentatus smithsonianus

Location: Intestinal vein

96

Pachytrema sanguineum Linton, 1928

Description: Body broadly oval. Tegument unspined. Oral sucker small. Numerous eggs in uterus. Uterus with extensive coils. Vitellarium acinous bunches of smaller follicles, extends slightly below bifurcation to caecal ends. Ovary small and medial.

Host: T. maximus

Location: Intestines

97

Ribeiroia ondatrae Looss, 1907

Description: Medium body size. Oral sucker subterminal and globular. Muscular ventral sucker, spherical, 2nd quarter of body. Pharynx muscular and elongate-oval. Prepharynx and oesophagus short. Testes tandem, contiguous, and postequatorial. Cirrus-sac elongate-oval, antero-dorsal to ventral sucker. Ovary oval. Vitellaria compact lateral fields, overlapping caeca. Excretory pore present and terminal.

Host: P. haliaetus

Location: Intestines

98

Renicola sp. Cohn, 1904

Description: Body oval or subpyriform. Total body length 1342 µm long by 543 µm wide. Unable to assess reproductive organs due to poor condition of the sample and numerous eggs scattered throughout body. Numerous eggs measuring 106 µm long by 67.4 µm wide.

Host: L. argentatus smithsonianus

Location: Kidneys

99

Scaphanocephalus expansus Creplin, 1842

Description: Expansion of anterior: wing-like appearance, scaly in horizontal layers. Oral sucker located in anterior portion: subterminal. Prepharynx virtually absent. Pharynx muscular, elongate-oval. Oesophagus short. Ventral sucker first quarter of body. Caeca extends to posterior; incomplete loops within anterior, wing-like expansion. Seminal vesicle long and tubular: winding. Testes tandem and slightly lobed. Vitelline glands extending from inside cecal loop towards posterior extremity; symmetrical and in the lateral fields. Specialists found in ospreys.

Host: P. haliaetus

Location: Intestines

100

Stephanoprora denticulata Rudolphi, 1802

Description: Body elongate. Testes longitudinally oval and contiguous. Posterior testes greater in diameter, longitudinally. Vitelline fields from posterior of anterior testes to posterior end. Ceca long, terminates at posterior end. Long oesophagus. Numerous eggs, ~27, large, and operculate.

Host: P. occidentalis and M. bassanus

Location: Intestines

101

Acanthocephala

Andracantha mergi Lundström, 1942

Description: 10 proboscis hooks in each longitudinal row; 18 longitudinal row of spines. Anterior trunk swollen with two fields of spines separated by small, un-spined gap. Posterior field of trunk spines extends down ventral side towards posterior end. Testes bilateral within swollen anterior trunk. 8 cement glands present.

Host: P. auritus

Location: Intestines

102

Corynosoma strumosum (Rudolphi, 1802) Lühe, 1904 Synonymized: Corynosoma ambispinigerum Harada, 1935; Corynosoma carchariae Linton, 1891; Corynosoma incrassatus Linton, 1891; Corynosoma osmeri Fujita, 1921; Corynosoma striatus Villot, 1875; Corynosoma ventricosum Rudolphi, 1809; Echinorhynchus strumosum Rudolphi, 1802

Description: Anterior end slanted to ventral side to middle. Body length 5-8 mm long. Anterior trunk inflated about 1/3 of entire trunk with single row of spines. 18 longitudinal rows with 10-11 hooks per row. Double walled at proboscis receptacle with cylindrical proboscis; proboscis mean length 519 µm long with hooks approximately 42.4 µm. Six cement glands. No genital spines.

Host: P. auritus

Location: Intestines

103

Southwellina hispida Van Cleave, 1925 Synonymized: Arhythmorhynchus tigrinus Moghe and Das, 1953

Description: Two anterior fields of trunk spines, male. No genital spines present. Anterior trunk slightly swollen. Trunk long and slender. 4 cement glands. Lemnisci flat and about same length as proboscis receptacle, not bound to walls at distal ends. Neck short, proboscis slightly short and appears damaged near tip. 8 proboscis hooks present; proboscis not fully extended. Unable to assess number of longitudinal rows or spines.

Host: P. auritus

Location: Intestines

104

Cestoda

Ascodilepis sp. Guildal, 1960

Description: Rostellar apparatus cyclusteroid. Hooks in two circles. Strobila very small. Genital pores unilateral on left side. Cirrus narrow with delicate spines and small apical tuft of fine spines.

Host: P. auritus

Location: Intestines

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Tetrabothrius sp. Rudolphi, 1819

Description: Scolex rectangular with four flat or cup-shaped rectangular bothridia. Unable to determine remaining characteristics due to missing sample slide.

Host: M. bassanus

Location: Intestines

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Nematoda

Contracaecum microcephalum Rudolphi, 1809 Synonymized: Ascaris microcephala (Rudolphi, 1809)

Description: Head localization small in size. Lips consist of three equal labia which is large and rounded with deep depression. Interlabia equal, approximately the same height as labia with a free curved internal part. Cuticle annulated directly behind the head in lateral seperations. Unable to determine internal features due to ineffective clearing process. Spicules of sub-equal length. Numerous pre-anal papillae with six pairs of post- anal papillae.

Host: P. occidentalis, P. auritus, M. bassanus

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Contracaecum multipapillatum (Drasche, 1882) Lucker, 1941 Synonymized: Ascaris multipapillata (Drasche, 1882); Contracaecum multipapillosum Skrjabin, 1916; Contracaecum philomultipapillatum Labriola and Suriano, 1996; Contracaecum robustum Chandler, 1935

Description: Lips without dentigerous ridges with hexagonal shape. Interlabia present and well developed. Unable to determine internal features due to lack of effective clearing process. Numerous pre-anal papillae with several pairs of post-anal papillae. Spicules of sub-equal length. Unable to determine internal features due to lack of effective clearing process. Caudal extremity slightly bent ventrally.

Host: P. haliaetus, P. occidentalis, P. auritus

108

Contracaecum rudolphii Rudolphi, 1809 Synonymized: Ascaris spiculigerum Rudolphi, 1809; Contracaecum spiculigerum Rudolphi, 1809; Contracaecum umiu Yamaguti, 1941

Description: Three labia present without dentrigerous ridges and often of hexagonal shape. Interlabia present and well developed with bifid distal ends. Amphidial pore present on labia at anterior end. Spicules of sub-equal length at end of conic tail. Numerous proximal papillae with two pairs of adcloacal papillae.

Host: P. occidentalis, P. auritus

Interlabia Labia

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Cosmocephalus sp. Molin, 1858

Description: Medium-sized acuariid. Anterior end possessing two triangular pseudolabia with each bearing single amphid and pair of prominent papillae. Cordons form dorsally and ventrally between pseudolabia with each cordon forming loop adjacent to base and continuing along longitudinal body axis. Cordons recurrent in anterior and reach level of anterior quarter of buccal cavity where they anastomose laterally. Unable to determine further characteristics due to missing sample.

Host: L. argentatus

Taxonomic/Image Reference: Mutafchiev et al. 2010. Page 11, Figure 5A-5H.

110

Paracuaria adunca Creplin, 1846

Description: Cordons very short, not recurrent or anastomosing. Well-developed interlabia, divided into two lobes with pointed ends projecting into oral opening. Spicule length 580 µm. Four pre-anal papillae and five post-anal papillae present. Tail tapered and ending in nipple-like appendage. Previously described in ring-billed gulls.

Host: L. atricilla

Interlabia

Nipple-like projection

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Tetrameres sp. Creplin, 1846

Description: Body twisted in a tight spiral. Swollen region between head and tail region. Located in stomach.

Host: P. occidentalis

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