Parasites of Fishes: List of and Dichotomous Key to the Identification of Major Metazoan Groups

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1 Parasites of Fishes: List of and Dichotomous Key to the Identification of Major Metazoan Groups George W. Benz 1, and Stephen A. Bullard 2 1 Department of Biology, P.O. Box 60, Middle Tennessee State University, Murfreesboro, TN 37132; gbenz@mtsu.edu; 2 Gulf Coast Research Laboratory, Department of Coastal Sciences, The University of Southern Mississippi, 703 East Beach Dr., Ocean Springs, MS 39564; ash.bullard@usm.edu Goal: For Aquarists to Make Critical Distinction Between Dangerous and Benign Parasites Aquarium staff that can make the distinction between dangerous and benign parasites can better conserve resources (including money) and avoid disease problems. In this way, they can disregard some infections all together or rapidly initiate treatment to control or eradicate pathogens before infected fish suffer or die. The likelihood of a given metazoan infection harming a fish depends on factors related to the interaction of the parasite s life history (e.g., feeding mode and life cycle) and physical and chemical characteristics of the host s environment (Benz et al., 2001; Benz and Bullard, 2004). In closed environments such as aquaria, some parasites cause disease whereas others are benign under the same set of host and environmental conditions. Hence, money and time are well-spent in treating potentially problematic infections while those resources are unnecessary and/or wasted by focusing on benign infections (Benz and Bullard, 2004). Furthermore, unnecessary treatments are costly and may harm the infected host more than the target parasites could ever harm that host. Thus, aquarium staff should accurately identify parasites and understand the health risks associated with infections. To help aquarium staff make the critical distinction between dangerous and benign parasites, we presented a Fish Health Workshop, April, prior to the 2005 Eastern Regional Conference of the American Zoo and Aquarium Association. The workshop provided an overview of the major groups of metazoan parasites that infect freshwater, estuarine, and marine fishes in nature and captivity; including information to help husbandry staff diagnose infections and identify parasites, as well as to understand parasite life cycles, host-parasite interactions (including diseases caused by parasites), and special considerations linked to captivity such as quarantine, prophylaxis, parasite control, and general husbandry practices. While it is not possible to provide a comprehensive summary of the workshop, this report provides information on two major workshop themes, i.e., identification of metazoan parasites and assignment of parasites to functional or risk groups to simplify husbandry decisions. A list of the major groups of metazoan parasites that infect fishes is presented as is a dichotomous key to the identification of these same parasites. Assigning Metazoan Parasites to Functional Health-Risk Categories Twenty-one major metazoan groups (Hydrozoa, Myxozoa, Tricladida, Aspidogastrea, Digenea, Monogenea, Cestoda, Nematoda, Acanthocephala, Hirudinida, Gastropoda, Pelecypoda, Acari, Ostracoda, Copepoda, Argulidea, Porocephalida, Cirripedia, Isopoda, Amphipoda, Craniata) infect fishes. We assign the fish parasites of each group to one of three categories based on their potential for causing disease and the course of general action that should be triggered upon identifying them. The functional risk categories are: high risk group (i.e., organisms typically pathogenic or seemingly so and requiring immediate treatment), 2) medium risk group (i.e., organisms not typically pathogenic but worthy of cautious and close monitoring, or immediate mechanical removal if possible), and 3) low risk group (i.e., organisms benign and not worthy of treatment or monitoring) (Table 1). As per the foregoing risk category definitions, a review of the literature, and consideration of unpublished observations, we only consider monogeneans (Monogenea), leeches (Hirudinida), argulids (Argulidea), and isopods (Isopoda) to be high risk groups (Table 1). Copepods (Copepoda) and nematodes (Nematoda) are medium risk groups, and in lieu of other relevant information we consider all other major groups of metazoans as low risk groups (Table 1).

2 Pigeon-holing major groups of metazoan parasites into the three aforementioned functional risk categories may seem arbitrary to some; however, we believe that these categories hold merit in light of the dearth of knowledge about specific parasite species and the great number of parasites that infect Table 1. Classification and common names of metazoan groups that include parasites of fishes. 1 Bold entries indicate major groups of taxa presented in the identification key provided in the text and risk assignments mentioned in the text. Asterisks indicate groups whose membership is entirely parasitic. Classification common name(s) (functional assignment) Kingdom Animalia animals Phylum Cnidaria cnidarians Class Hydrozoa hydrozoans (low risk group) Class Myxozoa* myxozoans, myxosporidians (low risk group) Phylum Platyhelminthes flatworms Superclass Turbellaria turbellarians Order Tricladida triclads, turbellarians (medium risk group) Superclass Cercomeria* Class Aspidogastrea* aspidogastreans, soleworms, aspidobothreans, aspidogastrids (low risk group) Class Digenea* digeneans, flukes, digenes, digenetic trematodes (low risk group) Class Monogenea* monogeneans, monogenoideans, monogenes, monogenetic trematodes (high risk group) Class Cestoda* cestodes, cestoideans: gyrocotylideans and eucestodes, tapeworms (low risk group) Phylum Nematoda nematodes, roundworms, threadworms (medium risk group) Phylum Acanthocephala* acanthocephalans, spiny-headed worms (low risk group) Phylum Annelida annelids, segmented worms Order Hirudinida true leeches (high risk group) Phylum Mollusca molluscs Class Gastropoda gastropods, snails (low risk group) Class Pelecypoda bivalves, clams, mussels, glochidia (larvae of many unionoids, Unionoidae) (low risk group) Phylum Arthropoda arthropods Subphylum Uniramia uniramians Subclass Acari mites (low risk group) Subphylum Crustacea crustaceans Class Maxillopoda maxillopodans Subclass Ostracoda ostracods, seed shrimp (low risk group) Subclass Copepoda copepods (medium risk group but see comments in text regarding anchor worms, sea lice, and gill maggots) Subclass Branchiura* branchiurans Order Argulidea* fish lice (high risk group) Order Porocephalida* pentastomes, tongue worms (low risk group) Subclass Cirripedia barnacles (low risk group) Class Malacostraca malacostracans Order Isopoda isopods (high risk group) Order Amphipoda amphipods (low risk group) Phylum Chordata chordates Subphylum Craniata craniates Superclass Agnatha jawless fishes Class Myxini hagfishes, slime eels (low risk group) Class Cephalaspidomorphi lampreys (low risk group) Superclass Gnathostomata jawed vertebrates Class Chondrichthyes chondrichthyans (low risk group) Class Actinopterygii ray-finned fishes (low risk group) 1 A universally-accepted classification scheme for taxa (groups) within Animalia does not exist. The classification used here is a mixture of several widely accepted schemes. fishes. Nevertheless, it should be noted that not all members of a major metazoan group pose an identical health risk to hosts and thus species-level information regarding some parasites or environmental information important to the progression of particular infections may require case-specific considerations of health risk. For example, some low risk parasites might require control under special circumstances. Unfortunately, the myriad of circumstances under which this may occur are beyond the scope of this report. Hence, husbandry staff and veterinarians should confer with parasitologists when assignment to a particular risk category is in question. Generally, we recommend that only high risk groups and several lower-taxonomic groups of pathogenic copepods such as anchor worms (Lernaea

Benz, G. W. & S. A. Bullard. 2006. Parasites of fishes: list and dichotomous key to identification of major metazoan groups. 9 spp.

evidence supports the routine control of any other major metazoan gr

, some ectoparasitic copepods) are large and their presence may upset patrons at public aquariums or they can be associated with unsightly lesions that may facilitate disease caused by opportunistic

Identifying Metazoan Parasites of Fishes Although parasite identification is a prerequisite for effective disease control, many metazoan parasites of fishes frequently are misidentified because they

3 Benz, G. W. & S. A. Bullard Parasites of fishes: list and dichotomous key to identification of major metazoan groups. 9 spp.) and some species of sea lice (Caligidae) and gill maggots (Lernaeopodidae) be addressed with eradication or control protocols aimed at prophylaxis. Nevertheless, although no compelling evidence supports the routine control of any other major metazoan group for health purposes, some parasites (e.g., some ectoparasitic copepods) are large and their presence may upset patrons at public aquariums or they can be associated with unsightly lesions that may facilitate disease caused by opportunistic pathogens. Given that these parasites are usually easy to mechanically remove or eradicate using various parasiticides, we encourage their elimination when this poses minimal risk to the host. Identifying Metazoan Parasites of Fishes Although parasite identification is a prerequisite for effective disease control, many metazoan parasites of fishes frequently are misidentified because they are small, anatomically complex, and delicate organisms that require extensive preparation techniques. With that in mind and to help reduce the frequency of misidentifications, we developed an identification key to the metazoan parasites of fishes that is userfriendly in the sense that it requires very little preparation of study samples and the use of a lowmagnification microscope only. Although the key is geared for identifying adult parasites, it also facilitates the identification of many parasite larvae and juveniles. Parasite groups are not arranged by ancestry within the key, and some parasite characteristics used in the key pertain to species that infect fishes only. Although one can identify a parasite to a major metazoan group by using this key, species-, genus- or family-level identifications depend on reference to scientific literature (e.g., peer-reviewed or synoptic literature) or assistance from a taxonomic authority. The risk group assignment for each major group presented in the key is listed in Table 1. Readers that are curious about parasite diseases, prophylaxis, and control may benefit by reading Benz et al. (2001) and Benz and Bullard (2004) and the cited literature therein. Dichotomous Identification Key to Major Groups of Metazoans that Infect Fishes Illustrations correspond to key couplets immediately above them, and all features or organisms underlined in couplets are illustrated. Illustrations depict typical examples but not all variations. 1. a. Organism (one species, Polypodium hydriforme) only associated with eggs of sturgeon and paddlefish (Acipenseriformes); infected fish eggs enlarged and containing parasite in form of macroscopic, light-colored stolon or microscopic planula; stolon with tentacles that may emerge from egg..hydrozoa tentacle stolen freed from sturgeon egg b. Organism not as described immediately above but may be associated with eggs of fishes a. Organism appearing as a microscopic, symmetrical spore; spores may reside outside of or within cyst-like capsules (plasmodia); individual spores typically microscopic and amassed; spores may be within or outside of plasmodium and they may or may not be encapsulated by host...myxozoa plasmodia spore b. Organism visible to naked eye (may nonetheless be tiny and larvae may be microscopic); may or may not be aggregated into clusters of individuals a. Organism a fish; endoskeleton made of cartilage or bone..craniata

hagfish lamprey cookiecutter shark snubnose eel b. Organism not a fish; endoskeleton of cartilage or bone lacking...4 4. a. Organism a snail that possess a snail shell.gastropoda b.

4 hagfish lamprey cookiecutter shark snubnose eel b. Organism not a fish; endoskeleton of cartilage or bone lacking a. Organism a snail that possess a snail shell.gastropoda b. Organism lacking snail shell a. Organism a tiny bivalve with two shells that clamp shut on host gills, fins or general body surface; lacking jointed appendages; may be encysted.pelecypoda b. Organism not a tiny bivalve with two shells.6 6. a. Organism worm-like; lacking exoskeleton articulated with segmented appendages 7 b. Organism with exoskeleton articulated with segmented appendages; appendages may be microscopic a. Organism segmented along main body axis (segmentation may be nonexistent or unapparent in some larval tapeworms) 8 b. Organism not segmented along main body axis a. Organism with anterior sucker surrounding oral opening; digestive tract and blind posterior sucker present; with or without distinctive eyespots...hirudinida anterior sucker shell shell oral opening eyespots posterior sucker b. Organism without anterior sucker and blind posterior sucker; digestive tract may or may not be present a. Organism with digestive tract; four anterior claws longitudinally arranged as two pairs; may be encysted. Porocephalida

Benz, G. W. & S. A. Bullard. 2006. Parasites of fishes: list and dichotomous key to identification of major metazoan groups. 9 anterior claws b.

5 Benz, G. W. & S. A. Bullard Parasites of fishes: list and dichotomous key to identification of major metazoan groups. 9 anterior claws b. Organism lacking gut; may have anterior hooks or tentacles with spines but not as described above; larvae may be encysted or encapsulated...segmented members of Cestoda scolex neck hooks strobila tentacles 10. a. Organism with spiny proboscis (possibly inverted) at anterior end of body; lacking digestive tract.acanthocephala proboscis proboscis b. Organism without spiny proboscis a. Organism lacking gut. Caryophyllideae and Spathebothriidea (Cestoda)

b. Organism with digestive tract.. 12 12. a.

Organism with two or fewer sucker-like attachment organs; if

along longitudinal body axis Aspidogastrea rugae b.

four pairs of suckers with hooks and associated sclerites.

a. Organism with attachment organ occupying extreme posterior end

Organism having an attachment organ not occupying extreme

6 b. Organism with digestive tract a. Organism with more than two suckers or rugae 13 b. Organism with two or fewer sucker-like attachment organs; if circular or disc-like the attachment organ may be subdivided a. Organism with suckers (rugae) arranged in one to several ranks along longitudinal body axis Aspidogastrea rugae b. Organism with posterior attachment organ (haptor) having three or four pairs of suckers with hooks and associated sclerites....polyopisthocotylea (Monogenea) suckers haptor sclerites egg 14. a. Organism with attachment organ occupying extreme posterior end of body...15 b. Organism having an attachment organ not occupying extreme posterior-most end of body, i.e., the attachment organ is subterminal a. Organism with haptor (each circumscribed below) in form of simple saucer-like sucker with hooks or lappet-like sucker without hooks...monopisthocotylea (Monogenea)

of a well-delineated posterior attachment organ such as that depicted for 15a...16 16. a. Organism

d external cilia...gyrocotylidea (Cestoda) 17. a.

7 egg hooks b. Organism with poorly defined, indiscrete posterior attachment organ that lacks hooks and is not in form of a well-delineated posterior attachment organ such as that depicted for 15a a. Organism typically with eyespots; external body surface ciliated; having complete digestive tract; may be embedded....tricladida eyespots b. Organism lacking complete digestive tract, eyespots and external cilia...gyrocotylidea (Cestoda) 17. a. Organism with two suckers (an oral sucker and acetabulum) 1 ; monoecious; typically capable of extension with non-sigmoidal, worm-like movements; larvae of many species encysted in flesh, gill, eye (may or may not be encysted), brain, or heart of fishes.....digenea 1 Except sanguinicolids (Sanguinicolidae) that lack a ventral sucker ( acetabulum ) and obvious oral sucker.

8 oral sucker acetabulum b. Organism lacking suckers; dioecious; body tube-like and cuticularized; movement via sigmoidal wriggling and thrashing; larvae encysted or encapsulated or not; adult with lips and tail; adult typically not encapsulated...nematoda anterior end lips tail tail 18. a. Organism with three or four pairs of walking legs; all appendages unbranched; pedipalps present; body compact and possibly tick-like; larvae may be encapsulated...acari pedipalp walking legs b. Organism with biramous crawling appendages; body not tick-like; may penetrate host a. Organism bivalved, with laterally compressed carapace enclosing head, body, and most appendages...ostracoda b. Organism lacking bivalve carapace as described immediately above a. Organism sessile; attached by peduncle that may or may not be embedded...cirripedia

Benz, G. W. & S. A. Bullard. 2006. Parasites of fishes: list and dichotomous key to identification of major metazoan groups. 9 barnacle on fish peduncle b. Organism not attached to host by peduncle.

9 Benz, G. W. & S. A. Bullard Parasites of fishes: list and dichotomous key to identification of major metazoan groups. 9 barnacle on fish peduncle b. Organism not attached to host by peduncle a. Organism lacking compound eyes, but may possess obvious non-compound eyes..copepoda b. Organism with compound eyes a. Organism with dorsoventrally compressed body; four pairs of biramous, cirriform legs; some species (genus Argulus) with two conspicuous sucker-like appendages on ventral body surface Argulidea suckers cirriform legs b. Organism lacking sucker-like appendages a. Organism with laterally compressed body... Amphipoda b. Organism with dorsoventrally compressed body or uncompressed body.isopoda

10 References Benz, W. W., S. A. Bullard, and A. D. M. Dove Metazoan parasites of fishes: synoptic information and portal to the literature for aquarists. Pp In: Regional Conference Proceedings Anonymous (ed.). American Zoo and Aquarium Association, Silver Spring, MD. Benz, G. W., and S. A. Bullard Metazoan parasites and associates of chondrichthyans with emphasis on taxa harmful to captive hosts. Pp In: The elasmobranch husbandry manual: captive care of sharks, rays and their relatives. Smith, M., D. Warmolts, D. Thoney, and R. Hueter (eds.). Special Publication, Ohio Biological Survey, Columbus, OH.

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