Parasitic Helminths of the American White Pelican ... - BioOne

Comp. Parasitol. 71(1), 2004, pp. 29–36

Parasitic Helminths of the American White Pelican, Pelecanus erythrorhynchos, from Florida, U.S.A. JOHN M. KINSELLA,1 MARILYN G. SPALDING,

AND

DONALD J. FORRESTER

Department of Pathobiology, College of Veterinary Medicine, University of Florida, Gainesville, Florida 32611, U.S.A. (e-mail: [email protected], [email protected], [email protected]) ABSTRACT: Thirty-three species of helminths (22 trematodes, 3 cestodes, 7 nematodes, and 1 acanthocephalan) were recovered from 29 American white pelicans, Pelecanus erythrorhynchos, collected in Florida, U.S.A., between 1982 and 2001. The number of helminth species per infected bird ranged from 3 to 17 (x ¼ 11). Three species of Contracaecum (Contracaecum rudolphii, Contracaecum multipapillatum, and Contracaecum micropapillatum) were the most prevalent and abundant helminths. One cestode species (Paradilepis longivaginosus) was considered a specialist in white pelicans, 9 species were considered generalists in pelicaniform birds, and the remainder of the species were considered true bird generalists. White pelicans shared 14 species of helminths with brown pelicans, Pelecanus occidentalis, and the most prevalent helminths appear to have been acquired in marine habitats. KEY WORDS: white pelican, Pelecanus erythrorhynchos, helminths, parasites, trematodes, cestodes, nematodes, acanthocephalan, Contracaecum, Florida, United States.

The American white pelican, Pelecanus erythrorhynchos Gmelin, 1789, is a large colonial water bird that breeds on islands of inland freshwater lakes in the north-central and northwestern United States and Canadian provinces and winters on the coasts of California (U.S.A.), Mexico, Nicaragua, and the Gulf of Mexico (Evans and Knopf, 1993). About 10,000– 12,000 white pelicans winter in Florida, U.S.A., both on the coasts and inland in the central and southern peninsula south of Florida Bay and the Lower Keys (Robertson and Woolfenden, 1992). No survey of helminths parasitizing the American white pelican has been conducted on the pelicans’ breeding range. Dronen et al. (2003) examined 6 specimens of Pel. erythrorhynchos on their wintering range near Galveston, Texas, U.S.A., and reported 10 species of helminths. There are a number of other isolated records and species descriptions for trematodes, cestodes, and nematodes. No acanthocephalans have been reported. In the winter of 1998–1999, large numbers of white pelicans were attracted to recently reflooded agricultural fields in the vicinity of Lake Apopka, Orange County, Florida, and began dying in large numbers (approximately 800–900) shortly thereafter. The cause of death of these birds is still being investigated. Many of the tissues tested contained elevated concentrations of organochlorine pesticides, but the role of these compounds in the death of the birds remains uncertain (Hoge et al., 2003). In the

course of the investigation, helminth parasites were collected from a subset of the Lake Apopka pelicans. Herein, we report on the helminths of these birds and an additional 13 birds examined from 1982 to 2002 from various localities in Florida.

MATERIALS AND METHODS In addition to the 16 Lake Apopka birds, 13 dead or dying white pelicans collected from 10 Florida counties (Brevard—1, Clay—1, Columbia—1, Dade—1, Lake—2, Marion—2, Monroe—1, Orange—2, Volusia—1, and Wakulla—1) from 1982 to 2002 were submitted to the Department of Pathobiology, College of Veterinary Medicine, University of Florida, to determine the cause of death. Carcasses were examined fresh or frozen within 4 hr of collection or death, transported to the laboratory, and examined at necropsy. All birds were subadults or adults. Techniques used for recovering, fixing, staining, and examining helminths followed the methods of Kinsella and Forrester (1972). Tissues collected were fixed in 10% neutral, buffered formalin, sectioned at 4-lm thickness, and stained with hematoxylin and eosin. Terminology used is taken from Bush et al. (1997). Intensities are presented as mean values with standard deviation followed by the range. Helminths were classified as host specialists (reported from only 1 species of host), pelican generalists (reported from only pelicaniform birds), and bird generalists (reported from more than 1 order of birds). Voucher specimens of helminths were deposited in the U.S. National Parasite Collection, Beltsville, Maryland, U.S.A.

Pelecanus erythrorhynchos Gmelin, 1789 Twenty-nine American white pelicans were collected between 1982 and 2001 from 10 counties in Florida, ranging from 30.208N; 82.358W to 24.508N; 80.378W (Fig. 1).

1 Corresponding author. Present address: 2108 Hilda Avenue, Missoula, Montana 59801, U.S.A.

29

30

COMPARATIVE PARASITOLOGY, 71(1), JANUARY 2004

Ascocotyle (Phagicola) nana Ransom, 1920 (Syn. As. nana Ransom, 1920; Phagicola nanus (Ransom, 1920).) Prevalence and intensity: Hosts infected, 11 of 29 (38%, 144 6 233, 2–777). Site of infection: Small intestine. Specimens deposited: USNPC 92494 (1 slide). Remarks: New host record. Bolbophorus spp. Prevalence and intensity: Hosts infected, 9 of 29 (31%, 118 6 233, 1–670). Figure 1. Sample sizes and distribution of white pelicans, Pelecanus erythrorhynchos, examined for helminths in Florida, U.S.A.

Site of infection: Small intestine. Additional reports from Pel. erythrorhynchos: Louisiana, Mississippi, U.S.A. (Overstreet et al., 2002); Texas, U.S.A. (Dronen et al., 2003).

Trematoda

Specimens deposited: USNPC 92498 (1 slide).

Ascocotyle (Ascocotyle) gemina Font, Heard, and Overstreet, 1984

Remarks: Two taxa of Bolbophorus, Bolbophorus damnificus Overstreet and Curran, 2002, and Bolbophorus sp. near Bolbophorus confusus (Krause, 1914), were present. According to Overstreet et al. (2002), the only reliable character that distinguishes these taxa is egg size, 120–130 lm in B. damnificus and 109–113 lm in Bolbophorus sp., which they believe may be a new species. Because all the trematodes were not gravid, counts were combined. Earlier reports of B. confusus from the American white pelican (e.g., McNeil, 1949; Odlaug, 1954; Hugghins, 1956; Fox and Olson, 1965; Dubois, 1978) are all suspect and need to be reevaluated.

Prevalence and intensity: Hosts infected, 10 of 29 (34%, 69 6 199, 2–635). Site of infection: Ceca. Specimens deposited: USNPC 92496 (1 slide). Remarks: New host record. Ascocotyle (Ascocotyle) leighi Burton, 1956 Prevalence and intensity: Hosts infected, 8 of 29 (28%, 9 6 12.3, 1–38). Site of infection: Ceca, large intestine. Specimens deposited: USNPC 92502 (1 slide).

Bursacetabulus pelecanus Dronen, Tehrany, and Wardle, 1999

Remarks: New host record.

Prevalence and intensity: Hosts infected, 23 of 29 (79%, 475 6 1,386, 2–6,900).

Ascocotyle (Phagicola) longa (Ransom, 1920)

Site of infection: Ceca, small intestine.

(Syn. Phagicola longa Ransom, 1920; Phagicola longus Ransom, 1920.)

Additional reports from Pel. erythrorhynchos: Texas, U.S.A. (Dronen et al., 2003).

Prevalence and intensity: Hosts infected, 23 of 29 (79%, 310 6 412, 1–1,130).


Site of infection: Ceca, small intestine. Additional reports from Pel. erythrorhynchos: Texas, U.S.A. (Dronen et al., 2003); Washington, U.S.A. (McNeil, 1949). Specimens deposited: USNPC 92499 (1 slide).

Remarks: First record from the white pelican in Florida, U.S.A. Bursatintinnabulus bassanus Tehrany, Dronen, and Wardle, 1999 Prevalence and intensity: Hosts infected, 25 of 29 (86%, 55 6 54.6, 5–230).

KINSELLA ET AL.—HELMINTHS OF WHITE PELICANS

Site of infection: Ceca, small intestine. Additional reports from Pel. erythrorhynchos: Texas, U.S.A. (Dronen et al., 2003). Specimens deposited: USNPC 92495 (1 slide). Remarks: Although Dronen et al. (2003) reported Bursat. bassanus from the white pelican in Texas, they observed variability in the characteristics used to separate this species and Bursatintinnabulus macrobursus (Dronen et al., 1999) from the brown pelican, Pelecanus occidentalis Linnaeus, 1766. Our specimens are closer to Bursat. bassanus, but further study may prove these species to be synonymous. Clinostomum attenuatum Cort, 1913 Prevalence and intensity: Hosts infected, 8 of 29 (28%, 2 6 2.6, 1–8).

31

Remarks: This may be an undescribed species, but specimens are in very poor condition. Mesostephanus microbursa Caballero, Grocott, and Zerecero, 1953 Prevalence and intensity: Hosts infected, 4 of 29 (14%, 2 6 2.3, 1–10). Site of infection: Small intestine. Specimens deposited: USNPC 92508 (1 slide). Remarks: New host record. This trematode appears to be a pelican generalist, having been previously reported from the brown pelican in Florida and Texas, U.S.A., and Panama (Caballero et al., 1953; Courtney and Forrester, 1974; Dronen et al., 2003). Mesorchis denticulatus (Rudolphi, 1802)

Site of infection: Mouth cavity, trachea.

(Syn. Stephanoprora denticulata (Rudolphi, 1802).)


Prevalence and intensity: Hosts infected, 13 of 29 (45%, 123 6 268, 1–900).

Remarks: New host record. Clinostomum complanatum (Rudolphi, 1814) Prevalence and intensity: Hosts infected, 5 of 29 (17%, 4 6 3.1, 1–9).

Site of infection: Small intestine. Specimens deposited: USNPC 92504 (1 slide). Remarks: New host record.

Site of infection: Mouth cavity, trachea. Specimens deposited: USNPC 92503 (1 slide).

Microparyphium facetum Dietz, 1909


Prevalence and intensity: Hosts infected, 2 of 29 (7%, 2, 1–2).

Dendritobilharzia pulverulenta (Braun, 1901)

Site of infection: Cloaca.


Specimens deposited: USNPC 92510 (1 slide). Remarks: New host record.

Site of infection: Heart. Specimens deposited: USNPC 92509 (1 slide).

Posthodiplostomum minimum (MacCallum, 1921)



Echinochasmus dietzevi Issaitschikoff, 1927 Prevalence and intensity: Hosts infected, 7 of 29 (24%, 93 6 203, 1–550).

Site of infection: Small intestine.




Remarks: New host record. Galactosomum sp.

Pholeter anterouterus Fischthal and Nasir, 1974

Prevalence and intensity: Hosts infected, 1 of 29 (3%, 37).

Prevalence and intensity: Hosts infected, 1 of 29 (3%, 10).


Site of infection: Nodules in wall of small intestine.

32


Additional reports from Pel. erythrorhynchos: Florida, U.S.A. (Pearson and Courtney, 1977). Remarks: This heterophyid trematode lives within granulomatous cysts in the wall of the small intestine, usually 2 trematodes to a cyst. Because it is not found in the lumen of the small intestine, its prevalence has probably been underestimated. Pearson and Courtney (1977) reported Pho. anterouterus from 1 of 4 white pelicans and from 1 of 150 brown pelicans in Florida. Renicola spp. Prevalence and intensity: Hosts infected, 19 of 29 (66%, 30 6 38, 1–144). Site of infection: Kidney. Specimens deposited: USNPC 92506, 92507 (2 slides). Remarks: Two species of Renicola, Renicola thapari Caballero, 1953, and a species resembling Renicola secundus Skrjabin, 1924, were present, often in mixed infections. Because many were immature and unidentifiable, counts were combined. Both are new host records for the American white pelican. Ribeiroia ondatrae (Price, 1931) (Syn. Psilostomum ondatrae Price, 1931; Ribeiroia thomasi (McMullen, 1938); Cercaria thomasi McMullen, 1938; Ribeiroia insignis Travassos, 1939.) Prevalence and intensity: Hosts infected, 15 of 29 (52%, 96 6 185, 1–620). Site of infection: Proventriculus. Additional reports from Pel. erythrorhynchos: Washington, U.S.A. (McNeil, 1949). Specimens deposited: USNPC 92500 (1 slide). Unidentified schistosome Prevalence and intensity: Hosts infected, 8 of 10 (80%, intensity unknown). Site of infection: Blood vessels of the small intestine. Additional reports from Pel. erythrorhynchos: Florida, U.S.A. (Leigh, 1957, reported as Gigantobilharzia sp.). Remarks: Cross-sections of adult schistosomes were found in the blood vessels of the tunica muscularis of the small intestine and eggs in the lamina propria of 8 of 10 birds examined histologically. Leigh (1957)

reported a species of Gigantobilharzia in white pelicans from the Everglades region of south Florida and said that the species resembled Gigantobilharzia huttoni (Leigh, 1953), a marine species described from experimental infections of parakeets. It is probable that this is the parasite found here, but further collections should be made to confirm the species identification. Cestoda Cyclustera ibisae (Schmidt and Bush, 1972) (Syn. Parvitaenia ibisae Schmidt and Bush, 1972; Parvitaenia eudocimi Rysavy and Macko, 1973.) Prevalence and intensity: Hosts infected, 3 of 29 (10%, 3 6 2.1, 1–5). Site of infection: Small intestine. Additional reports from Pel. erythrorhynchos: Texas, U.S.A. (Dronen et al., 2003). Specimens deposited: USNPC 92513 (1 slide). Remarks: This cestode was present in small numbers, and several of the strobila were immature. Its primary host appears to be the white ibis, Eudocimus albus (Linnaeus, 1758) (Schmidt and Bush, 1972; Rysavy and Macko, 1973). Paradilepis longivaginosus (Mayhew, 1925) (Syn. Oligorchis longivaginosus Mayhew, 1925.) Prevalence and intensity: Hosts infected, 23 of 29 (79%, 71 6 148, 1–666). Site of infection: Small intestine. Additional reports from Pel. erythrorhynchos: Wyoming, U.S.A. (Mayhew, 1925); South Dakota, U.S.A. (Hugghins, 1956); California and Nevada, U.S.A. (Matthias, 1963); Manitoba, Canada (McLaughlin, 1974). Specimens deposited: USNPC 92512 (1 slide). Remarks: This cestode appears to be a widespread and common specialist in the white pelican. The Hymenolepis sp. reported by McNeil (1949) from white pelicans from Washington, U.S.A., is probably the same species. Larval cestode Prevalence and intensity: Hosts infected, 1 of 29 (3%, 5, 5). Site of infection: Subcutaneous. Specimens deposited: USNPC 92511 (1 slide).


33

Remarks: Five larval cestodes resembling plerocercoids were found subcutaneously in 1 bird. Because subcutaneous tissues were examined in only a few birds, prevalence may be greatly underestimated. Similar larvae were found in great egrets, Ardea alba Linnaeus, 1758, from Florida by Sepulveda et al. (1999), who speculated that they might be immature stages of the pseudophyllidean Spirometra mansonoides (Mueller, 1935), a common parasite of carnivores in Florida (Forrester, 1992).

Site of infection: Proventriculus.

Nematoda

Prevalence and intensity: Hosts infected, 16 of 29 (55%, 9 6 8.8, 1–29).

Capillaria mergi Madsen, 1945

Remarks: New host record. Both specimens found were fourth-stage larvae, so this nematode may not mature in white pelicans. Microtetrameres pelecani (Johnston and Mawson, 1942) (Syn. Tetrameres pelecani Johnston and Mawson, 1942; Microt. pelecani Skrjabin, 1949.)

Prevalence and intensity: Hosts infected, 21 of 29 (72%, 18 6 30, 1–130).

Site of infection: Proventriculus.


Prevalence and intensity: Hosts infected, 29 of 29 (100%, 583 6 494, 26–1,575).

Remarks: This is the first record of this species from the white pelican and from North America. Previous records are from the great white pelican, Pelecanus onacrotalus Linnaeus, 1758, from Russia by Skrjabin et al. (1949) and from the Australian pelican, Pelecanus conspicillatus Temminck, 1824, from Australia by Mawson (1979), so it is apparently a cosmopolitan parasite of pelicans.

Site of infection: Esophagus, proventriculus, ventriculus, small intestine.

Paracuaria adunca (Creplin, 1846)

Specimens deposited: USNPC 92517 (1 vial). Remarks: New host record. Contracaecum spp.

Additional reports from Pel. erythrorhynchos: South Dakota, U.S.A. (Hugghins, 1956); Florida, U.S.A. (Oglesby, 1960; Owre, 1962); California, U.S.A. (Liu and Edward, 1971); Manitoba, Canada (McLaughlin, 1974); Mississippi, U.S.A. (Deardorff and Overstreet, 1980); Texas, U.S.A. (Cram, 1927; McDaniel and Patterson, 1966; Dronen et al., 2003). Specimens deposited: USNPC 92516, 92519, 92520 (3 vials). Remarks: Based on the presence of males, 3 species were present: Co. rudolphii Hartwich, 1964 (76%), Co. multipapillatum (von Drasche, 1882) (66%), and Co. micropapillatum (Stossich, 1890) (55%). Of the 29 birds infected, 2 (7%) were infected with 1 species, 21 (72%) with 2 species, and 6 (21%) with 3 species. Because larvae and females could not be identified to species, intensities were combined. Dronen et al. (2003) reported 2 unidentified species of Contracaecum from white pelicans in Texas. We examined their vouchers (USNPC 92311) and were able to identify males of Co. rudolphii and Co. multipapillatum. Eustrongylides ignotus Ja¨gerskiold, 1909 Prevalence and intensity: Hosts infected, 2 of 29 (7%, 1, 1).

Specimens deposited: USNPC 92515 (1 vial).

Prevalence and intensity: Hosts infected, 1 of 29 (3%, 1). Site of infection: Proventriculus. Specimens deposited: USNPC 92522 (1 vial). Remarks: New host record. Strongyloides sp. Prevalence and intensity: Hosts infected, 1 of 29 (3%, 1). Site of infection: Small intestine. Specimens deposited: USNPC 92521 (1 vial). Remarks: New host record. Acanthocephala Polymorphus brevis (Van Cleave, 1916) (Syn. Southwellina breve Van Cleave, 1916; Arhythmorhynchus brevis (Van Cleave, 1916).) Prevalence and intensity: Hosts infected, 5 of 29 (17%, 15 6 19, 1–45). Site of infection: Small intestine. Specimens deposited: USNPC 92514 (1 slide).

34


Remarks: This is the first record of an acanthocephalan from this host. However, all specimens found were immature, so white pelicans may be only accidental hosts of this common parasite of herons and egrets in Florida (Sepulveda et al., 1996, 1999). DISCUSSION Thirty-three species of helminths (22 trematodes, 3 cestodes, 7 nematodes, and 1 acanthocephalan) were collected from 29 white pelicans. The number of helminth species per infected bird ranged from 3 to 17 (x ¼ 11). These birds were collected over a period of 19 yr, and most died of acute illness or trauma and are thus not a random sample of the wintering pelican population. However, it is the largest sample of white pelicans examined to date, and some conclusions can be drawn. The only helminth species that appears to be a host specialist in the white pelican is the cestode Parad. longivaginosus. Nine species (Bolbophorus spp., Bursac. pelecanus, Bursat. bassanus, Mesos. microbursa, Microt. pelecani, Pho. anterouterus, Renicola spp.) are considered generalists in pelicaniform birds, and the remaining 22 species are considered true generalists, most having been reported previously from spoonbills, herons, egrets, and ospreys in Florida (Sepulveda et al., 1994, 1996, 1999; Kinsella et al., 1996). The unidentified schistosome remains to be classified. The proventricular trematode, Ri. ondatrae, causes widespread limb deformities in frogs and toads from the western United States in both natural and experimental infections (Johnson et al., 2001, 2002). This species was common in our sample (prevalence ¼ 52%, mean intensity ¼ 96). It has also been reported from the white pelican in the state of Washington, U.S.A. (McNeil, 1949). Although this fluke is extremely non–host specific, the white pelican may prove to be an important factor in its geographical distribution. The white pelican shares much of its winter range with resident brown pelicans, which have been surveyed much more extensively for parasites (Courtney and Forrester, 1974; Humphrey et al., 1978; Dyer et al., 2002; Dronen et al., 2003). Brown pelicans are primarily marine, whereas white pelicans are found in both marine and freshwater habitats. Of the helminths reported here, 9 trematodes (Bursat. bassanus, Bursac. pelecanus, As. longa, Mesor. denticulatus, Re. thapari, Ec. dietzevi, Microp. facetum, Mesos. microbursa, and Pho. anterouterus), 1 cestode (Cy. ibisae), and 4 nematodes (Co. rudolphii, Co. multi-

papillatum, Ca. mergi, and Parac. adunca) have been reported from brown pelicans from marine habitats (Courtney and Forrester, 1974; Pearson and Courtney, 1977; Dronen et al., 1999, 2003). Other species with known or probable marine intermediate hosts are As. nana, As. gemina, and Renicola spp. (Font, Heard, et al., 1984; Font, Overstreet, et al., 1984). Thus, the most prevalent helminths found here in white pelicans appear to have been acquired in marine habitats, even though many of the birds were collected inland. The prominent exceptions are Ri. ondatrae and Bolbophorus spp., which have freshwater life cycles (Johnson et al., 2002; Overstreet et al., 2002). Larvae of Co. rudolphii and Co. multipapillatum have been reported from both freshwater and marine fish (Deardorff and Overstreet, 1980). The life cycles of Parad. longivaginosus and Microt. pelecani are unknown. Mean intensities for Contracaecum spp. in white pelicans (583) were considerably higher than those reported for brown pelicans in Florida (59) by Courtney and Forrester (1974). Brown pelicans are diving feeders, preying on larger fish, whereas white pelicans are ‘‘bill dippers,’’ feeding on smaller fish as they swim (Evans and Knopf, 1993), and this difference in feeding habits probably accounts for the differences in their helminth faunas both in diversity of species and in mean intensities of shared species. Much remains to be learned about the helminths of white pelicans, particularly those helminth species endemic to white pelican breeding grounds. Because the birds sampled in this study were collected mostly from freshwater sites and many died of acute illness with evidence of regurgitation, the prevalence and intensity of many helminths, especially Contracaecum spp., might differ from those of a normal population. It is also desirable to obtain more data from wintering birds collected in marine habitats. ACKNOWLEDGMENTS We thank Elizabeth Dusenbery, Garry Foster, and Teresa de le Fuente for assistance with necropsies and helminth collection. This research was supported by the Florida Agricultural Experiment Station and grants from the St. John’s River Water Management District and the Florida Fish and Wildlife Conservation Commission. This is Florida Agricultural Experiment Station Journal Series No. R-09239. LITERATURE CITED Bush, A. O., K. D. Lafferty, J. M. Lotz, and A. W. Stostak. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83:575–583.


Caballero y Caballero, E., R. G. Grocott, and M. C. Zerecero y Diaz. 1953. Helmintos de la Repu´blica de Panama´. IX. Algunos trema´todos de aves marinas del Oceano Pacifico del Norte. Anales del Instituto de Biologia, Universidad Nacional Autońoma de Me´xico 24:391–414. Courtney, C. H., and D. J. Forrester. 1974. Helminth parasites of the brown pelican in Florida and Louisiana. Proceedings of the Helminthological Society of Washington 41:89–93. Cram, E. B. 1927. Bird parasites of the nematode suborders Strongylata, Ascaridata, and Spirurata. United States National Museum Bulletin No. 140. 465 pp. Deardorff, T. L., and R. M. Overstreet. 1980. Contracaecum multipapillatum (¼ C. robustum) from fishes and birds in the northern Gulf of Mexico. Journal of Parasitology 66:853–856. Dronen, N. O., C. K. Blend, and C. K. Anderson. 2003. Endohelminths from the brown pelican, Pelecanus occidentalis, and the American white pelican, Pelecanus erythrorhynchos, from Galveston Bay, Texas, U.S.A., and checklist of pelican parasites. Comparative Parasitology 70:140–154. Dronen, N. O., M. R. Tehrany, and W. J. Wardle. 1999. Diplostomes from the brown pelican, Pelecanus occidentalis (Pelecanidae), from the Galveston, Texas area, including two new species of Bursacetabulus gen. n. Journal of the Helminthological Society of Washington 66:21–24. Dubois, G. 1978. Notes helminthologiques IV: Strigeidae Railliet, Diplostomidae Poirier, Proterodiplostomidae Dubois et Cyathocotylidae Poche (Trematoda). Revue Suisse de Zoologie 85:607–615. Dyer, W. G., E. H. Williams Jr., A. A. MignucciGiannoni, N. M. Jimeńez-Marrero, L. BunkleyWilliams, D. P. Moore, and D. B. Pence. 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. Evans, R. M., and F. L. Knopf. 1993. American White Pelican. In A. Poole and F. Gill, eds. The Birds of North America. No. 57. Academy of Natural Sciences of Philadelphia, Philadelphia, Pennsylvania. 21 pp. Font, W. F., R. W. Heard, and R. M. Overstreet. 1984. Life cycle of Ascocotyle gemina n. sp., a sibling species of A. sexdigita (Digenea: Heterophyidae). Transactions of the American Microscopical Society 103:392–407. Font, W. F., R. M. Overstreet, and R. W. Heard. 1984. Taxonomy and biology of Phagicola nana (Digenea: Heterophyidae). Transactions of the American Microscopical Society 103:408–422. Forrester, D. J. 1992. Parasites and Diseases of Wild Mammals in Florida. University Press of Florida, Gainesville, Florida. 459 pp. Fox, A. C., and R. E. Olson. 1965. The life cycle of the digenetic trematode Bolbophorus confusus, and effects of water temperature on the developmental stages. Transactions of the American Microscopical Society 84:153–154. Hoge, V. R., R. Conrow, D. L. Stites, M. F. Coveney, E. R. Marzolf, E. F. Lowe, and L. E. Battoe. 2003. SWIM

35

Plan for Lake Apopka. St. Johns River Water Management District, Palatka, Florida. 5 pp. Hugghins, E. J. 1956. Further studies on Hysteromorpha triloba (Trematoda: Strigeida), and some parasites of a white pelican. Journal of Parasitology 42:26. Humphrey, S. R., C. H. Courtney, and D. J. Forrester. 1978. Community ecology of the helminth parasites of the brown pelican. Wilson Bulletin 90: 587–598. Johnson, P. T. J., K. B. Lunde, R. W. Haight, J. Bowerman, and A. R. Blaustein. 2001. Ribeiroia ondatrae (Trematoda: Digenea) infection induces severe limb malformations in western toads (Bufo boreas). Canadian Journal of Zoology 79:370–379. Johnson, P. T. J., K. B. Lunde, E. M. Thurman, E. G. Ritchie, S. N. Wray, D. R. Sutherland, J. M. Kapfer, T. J. Frest, J. Bowerman, and A. R. Blaustein. 2002. Parasite (Ribeiroia ondatrae) infection linked to amphibian malformations in the western United States. Ecological Monographs 72:151–168. Kinsella, J. M., R. A. Cole, D. J. Forrester, and C. L. Roderick. 1996. Helminth parasites of the osprey, Pandion haliaetus, in North America. Journal of the Helminthological Society of Washington 63:262– 265. Kinsella, J. M., and D. J. Forrester. 1972. Helminths of the Florida duck, Anas platyrhynchos fulvigula. Proceedings of the Helminthological Society of Washington 39:173–176. Leigh, W. B. 1957. Brown and white pelicans as hosts for schistosomes of the genus Gigantobilharzia. Journal of Parasitology 43:35–36. Liu, S. K., and A. G. Edward. 1971. Gastric ulcers associated with Contracaecum spp. (Nematoda: Ascaroidea) in a stellar sea lion and a white pelican. Journal of Wildlife Diseases 7:266–271. Matthias, D. V. 1963. Helminths of some waterfowl from western Nevada and northeastern California. Journal of Parasitology 49:155. Mawson, P. M. 1979. Some Tetrameridae (Nematoda: Spirurida) from Australian birds. Transactions of the Royal Society of South Australia 103:177–184. Mayhew, R. L. 1925. Studies on the avian species of the cestode family Hymenolepididae. Illinois Biological Monographs 10:1–125. McDaniel, B., and I. Patterson. 1966. Nematode infestation of a white pelican found along the gulf coast of Texas. Southwestern Naturalist 11:312. McLaughlin, J. D. 1974. A redescription of Paradilepis longivaginosus (Mayhew, 1925) (Cestoda: Dilepididae) and a comparison with Paradilepis simoni Rausch, 1949 and Paradilepis rugovaginosus Freeman, 1954. Canadian Journal of Zoology 52:1185–1190. McNeil, C. W. 1949. Notes on the parasites of a white pelican (Pelecanus erythrorhynchos). Northwest Science 23:11. Odlaug, T. O. 1954. Parasites of some birds of Minnesota. An annotated bibliography. The Flicker 26:59–65. Oglesby, L. C. 1960. Heavy nematode infestation of white pelican. Auk 77:354. Overstreet, R. M., S. S. Curran, L. M. Pote, D. T. King, C. K. Blend, and W. D. Grater. 2002. Bolbophorus damnificus n. sp. (Digenea: Bolbophoridae) from the channel catfish Ictalurus punctatus and American white

36


pelican Pelecanus erythrorhynchos in the USA based on life-cycle and molecular data. Systematic Parasitology 52:81–96. Owre, O. T. 1962. Nematodes in birds of the order Pelecaniformes. Auk 79:114. Pearson, J. C., and C. H. Courtney. 1977. Pholeter anterouterus Fischthal & Nasir, 1974 (Digenea: Opisthorchiidae) redescribed, together with remarks on the genera Pholeter Odhner, 1914 and Phocitrema Goto & Ozaki, 1930 and their relationship to the centrocestine heterophyids. Parasitology 74:255–271. Robertson Jr., W. B., and G. E. Woolfenden. 1992. Florida Bird Species: An Annotated List. Special Publication No. 6. Florida Ornithological Society, Gainesville, Florida. 260 pp. Rysavy, B., and J. K. Macko. 1973. Bird cestodes of Cuba 1. Cestodes of birds of the orders Podicipediformes, Pelecaniformes, and Ciconiiformes. Anales del Instituto de Biologia Universidad Nacional Autońoma de Me´xico, Zoologia. 42:1–28. Schmidt, G. D., and A. O. Bush. 1972. Parvitaenia ibisae sp. n. (Cestoidea: Dilepididae), from birds in Florida. Journal of Parasitology 58:1095–1097.

Sepulveda, M. S., M. G. Spalding, J. M. Kinsella, R. D. Bjork, and G. S. McLaughlin. 1994. Helminths of the roseate spoonbill, Ajaja ajaja, in southern Florida. Journal of the Helminthological Society of Washington 61:179–189. Sepulveda, M. S., M. G. Spalding, J. M. Kinsella, and D. J. Forrester. 1996. Parasitic helminths of the little blue heron, Egretta caerulea, in southern Florida. Journal of the Helminthological Society of Washington 63:136–140. Sepulveda, M. S., M. G. Spalding, J. M. Kinsella, and D. J. Forrester. 1999. Parasites of the great egret (Ardea albus) in Florida and a review of the helminths reported for the species. Journal of the Helminthological Society of Washington 66:7–13. Skrjabin, K. I., N. P. Schikhobalova, and A. A. Sobolev. 1949. Key to the Parasitic Nematodes. Vol. 1: Spirurata and Filariata. Academy of Sciences of the U.S.S.R., St. Petersburg. Translated from Russian for the U.S. National Science Foundation and Department of Agriculture by the Israel Program for Scientific Translations. Office of Technical Services, U.S. Department of Commerce, Washington, D.C. 497 pp.