Biology 625
ANIMAL PARASITOLOGY
Fall semester lecture note outline

Updated: 16 November 2006

Although the majority of parasites in the world are invertebrates, it should be of no surprise that parasitism has arisen within the chordates as well. Classic examples include the remora, which attach to sharks and rays, the jawless fishes (lamprey and hagfish) which prey upon other fish, vampire bats, and brood parasitism among birds. However, additional examples of parasitism within the chordates exist, some of which I have outlined below.

1. Agnatha "jawless" (lamprey and hagfish)
   1. This class of chordates is similar to fish, but lack jaws, scales and paired fins. They have a simple two-chambered heart and external gill openings.
   2. Agnathans possess toothed outgrowths in the oral region where they bore into the sides of fish and suck out the blood and/or viscera
   3. Lampreys (Petromyzonidae)
      1. 8 genera and nearly 40 species of lamprey are known to exist. Most are free-living predators but a few are parasitic, attacking fish and weakening or killing them.
      2. Eggs hatch into ammocoetes larvae
      3. Mouth is round, with sucker-like mouth full of rows of teeth. The tongue is rasp-like
      4. Single nostril on dorsal surface of head
      5. Complete braincase
      6. Rudimentary vertebrae
      7. Extant parasitic species include (several others may also be found to be parasitic)
         1. Eudontomyzon danfordi (Carpathian lamprey)
         2. Ichthyomyzon bdellium (Ohio lamprey)
         3. Ichthyomyzon castaneus (Chestnut lamprey)
         4. Ichthyomyzon unicuspis (Silver lamprey)
         5. Lampetra ayresii (River lamprey)
         6. Lampetra fluviatilis (European river lamprey)
         7. Lampetra morii (Korean lamprey)
         8. Lampetra reissneri (Far Eastern brook lamprey)
         9. Lampetra similis (Klamath river lamprey)
         10. Lampetra spadicea (Mexican lamprey)
         11. Lampetra tridentata (Pacific lamprey)
         12. Lethenteron camtschaticum (Arctic lamprey)
         13. Mordacia lapicida (Chilean lamprey)
         14. Mordacia mordax (Australian lamprey)
         15. Petromyzon marinus (Sea lamprey)
   4. Hagfish (Myxinidae)
      1. Currently, there are 66 known species of hagfish in 5 genera (Eptatretus, Myxine, Nemamyxine, Paramyxine, Quadratus). A variety of species are yet to be named.
      2. More primitive than the lamprey.
      3. Direct development without larval stage.
      4. 4 pair sensory tentacles around the mouth.
      5. 3 accessory hearts
      6. Partial braincase
      7. Long, slender fish which produce copious amounts of slime.
      8. Generally found in cold oceans, often living on or in a muddy bottom and in large groups of individuals
      9. A large part of the diet consists of polychaetes
      10. Two pair of rasps on the tongue, used to tear off chunks of prey tissue
      11. Scavenge dead and dying fish; also feed on invertebrates. Occasionally target healthy fish. Rasp and bite into a fish, boring into the tissues and body cavity to feed.
2. Osteichthyes (teleost fish)
   1. Remoras
      1. Remoras are perciform fish within the family Echeneidae
      2. Measure 0.2-2 meters in length
      3. Atlantic, Indian, Pacific oceans
      4. Head flattened with adhesive disc with transverse, moveable lamina
      5. Feed on ectoparasites, small fish, and left overs from the host meals
      6. Considered by most authors to be commensals
      7. 8 species of remora are considered valid
         1. Echeneis naucrates (live sharksucker or slender suckerfish) is very common in warm marine waters and can be found up and down the western Atlantic coast from Nova Scotia to Uruguay. It associates with a variety of vertebrates including sharks, rays, whales, dolphins, large teleost fish, and turtles. It may also attach to ships and swim with divers. This remora feeds on remnants of host meals, on small fish, and host parasites. Juvenile remoras sometimes act as cleaner fish for parrotfish.
         2. Echeneis neucratoides (whitefin sharksucker) is found in subtropical regions of the Atlantic and Caribbean
         3. Phtheirichthys lineatus (slender suckerfish) occurs in tropical and subtropical regions of the Atlantic and Caribbean. Commonly attaches to barracuda, various other teleosts, and turtles. Clings to body and inside gill chambers.
         4. Remora australis (whalesucker) is worldwide, predominately a warm water species, and attaches only to whales and dolphins (Cetacea)
         5. Remora brachyptera (spearfish remora) is found in warm waters of the Atlantic. It attaches within the gill chambers of swordfish and several other species of fish
         6. Remora osteochir (marlin sucker) is a subtropical, cosmopolitan species which prefers sailfish and marlin. It attaches to either the gill chambers or body of the host.
         7. Remora remora (common remora) is a very cosmopolitan species that prefers warmer waters. It commonly attaches to sharks, large teleosts, turtles, and sometimes ships. Feeds on ectoparasitic copepods.
         8. Remorina albescens (white suckerfish) is cosmopolitan in warm waters and prefers Manta rays, where it likes to attach inside the mouth and gill chambers. Occasionally it can be found associated with sharks and black marlin.
   2. Pearlfish (Ophidiiformes - Carapidae)
      1. Ophidiiformes represent the "Cusk eels" and some species within the family Carapidae (pearlfish) live symbiotically within benthic invertebrates. The relationship of the fish to the host is quasi-parasitic; only in a few cases is the parasitism overt. In most cases, the fish either consumes food that could be used by the host or, in most cases, simply takes up space
      2. Some representative species
         1. Carapus acus (pearl fish) is found in the Eastern Atlantic, residing within holothurians
         2. Carapus bermudensis (pearlfish) is found in the Western Pacific on reefs. This fish lives in the body cavity of sea cucumbers by day and forages at night
         3. Carapus borabornsis (pinhead pearlfish) lives in some species of sea cucumbers in the Indo-Pacific
         4. Carapus dubius (Pacific pearlfish) is found in the Eastern Pacific in the body cavity of cockles, pearl shells, and pen shells.
         5. Carapus homei (silver pearlfish) resides within some sea cucumbers in the Indo-Pacific
         6. Carapus mourlani (star pearlfish) is found in sea stars and holothurians in the Indo-Pacific
         7. Encheliophis gracilis (graceful pearlfish) lives in some sea stars and sea cucumbers in the Indo-West Pacific
         8. Encheliophis sagamianus (pearlfish) off the coast of Japan in deep water in holothurians
         9. Encheliophis vermicularis (worm pearlfish) in sea cucumbers in the Indo-Pacific
         10. Encheliophis vermiops (pygmy pearlfish) has been rarely found in the Indo-Pacific in burrowning holothurians
         11. Onuxodon fowleri (bivalve pearlfish) is found in the Indo-Pacific and prefers clams and oysters
         12. Onuxodon margaritiferae (bivalve pearlfish) occurs in marine waters off western Australia. It prefers to reside within sea cucumbers and the mantle cavity of bivalves
         13. Onuxodon parvibrachium (oyster pearlfish) resides within the giant oyster (Pycnodonta hyotis) in the Indo-Pacific
   3. Parasitic male fish (Lophiiformes)
      1. The order Lophiiformes (over 210 spp) contains a variety of families of fish commonly termed "anglerfish," "toadfish," "monkfish," "dreamers," and "sea-devils."
      2. Members from at least 4 families contain some deep sea species with parasitic males. Because the species are often poorly known, other species and families may eventually be found to have parasitic males.
      3. Males are small, and attach to a female with their teeth. The teeth and jaw then gradually recede and the circulatory systems of the two fish merge. They become irreversibly joined. Males then provide a constant supply of sperm to the female. Probably an adaptation because of the difficulty of finding a mate in some deep sea situations.
      4. Families containing one or more parasitic species (families may contain both parasitic and non-parasitic species and the number of species listed does not reflect the total number of parasitic species within each family)
         1. Caulophrynidae (fantails - 5 spp total in 2 genera)
         2. Ceratiidae (seadevils - 4 spp total in 2 genera)
         3. Linophrynidae (leftvents - 26 spp total in 5 genera)
         4. Oneirodidae (dreamers - 58 spp total in 13 genera)
   4. Vampire fish, Candiru, or Canero (Vandellia cirrhosa)
      1. The family Trichomycteridae (order: Siluriformes) contains 42 genera and 178 described species of freshwater fish commonly referred to as the "pencil catfish" or "parasitic catfish." Representative species are distributed throughout South America, Costa Rica, and Panama
      2. Most species are slender, sometimes transparent or nearly so, and only reach a few centimeters in length
      3. Most species inhabit sandy to muddy bottoms; some are nocturnal
      4. Most species are harmless, feeding on protozoa, rotifers, and insect larvae off the bottoms of rivers
      5. Some species are capable of burrowing through the body wall of fish and have been found in the body cavity. Whether this is incidental or common is not known.
      6. Some species are truly parasitic, however, entering the gill chambers of larger fish, erecting a spine (or series of spines) to hold them into place, and feeding off blood from the gill filaments for a minute or two
      7. Rarely, in the Amazon, members of the genus Vandellia (and perhaps a few closely related species in other genera) accidently enter the urethra of humans urinating in the water. Even more rarely, the anus and vagina have been reported to serve as suitable orifices. Apparently, the adage states, the urine is mistaken for urea given off in low quantity by fish gills (but at least one paper disputes this hypothesis). The species most commonly reported as intraurethral is Vandellia cirrhosa.
      8. Surgical removal of the catfish is necessary. Reputed are a couple of local plant remedies (the Xagua plant and Buitach apple), which are inserted into the affected area and are supposed to kill and dissolve the fish.
      9. See also 1973, Urology 1: 265-267
      10. All members of the family are banned from import into the U.S.
3. Birds
   1. Brood parasitism
      1. This is an association where one bird (the parasitic bird) lays its eggs within the nest of another bird (the host or foster bird). The foster bird then cares for the offspring of the invader. Most of this is interspecific parasitism.
      2. About 1% of all birds (103 species) are known to practice brood parasitism
      3. Some species of birds reject the eggs of a brood parasite, whereas others will accept the egg.
      4. Some foster hosts raise the parasite along with their own young. In other cases, such as in cuckoo parasitism, either the female cuckoo will remove or damage a host egg when laying her own or the offspring will evict all other eggs from the nest upon hatching.
      5. Some representatives
         1. Anatidae - A number of anatids display various types of brood parasitism, both intra- and inter-specific. Because the young are precocial (up and around soon after hatching), the impact of the parasitism on the host tends to be low.
            1. the South American black-headed duck (Heteronetta atricapilla) lays its eggs within the nests of other waterfowl, especially red-fronted coots and rosy-billed pochards. The offspring are capable of running around soon after hatching so they do not need to be fed by the foster parent. Their parasitism is considered to be fairly benign.
            2. the female goldeneye duck (Bucephala clangula) can double her reproductive output by combining brood parasitism with normal nesting. She will lay her eggs within other goldeneye nests, and also nests of a variety of other species of waterfowl.
            3. The redheaded duck (Aythya americana) will lay eggs not only in their own nests, but also the nests of conspecifics and other types of waterfowl.
            4. other known brood parasites include ruddy ducks, canvasbacks, black teal, blue-winged teal, northern shovelers, whistling-ducks, mallards, gadwalls, norther pintails, and others.
         2. Cuculidae - Of the 143 known species of cuckoo, 50 old world species (Cuculinae, Centropinae, Coccyzinae) and 3 new world species (Neomorphinae) are known to be parasitic.
            1. European cuckoo (Cuculus canorus) eggs are often very similar to host eggs, both in size and markings. Many hosts are very good at detecting foreign eggs within the nest.
            2. Female cuckoos know which species of host she will have the most success parasitizing, apparently based on past experience with that host as a brood parasite herself.
            3. Cuckoo eggs require 0.5-1.5 days shorter incubation than host eggs. Once the hatchling is about 10 hours old, it pushes any solid object it contacts out of the nest including unhatched eggs and host offspring
            4. Foster parents continue to feed the oversized offspring, which has mouth markings very similar to host hatchlings.
         3. Estrildidae - All 19 species within the genus Vidua are brood parasites. Other estrildids raise the offspring as their own.
         4. Indicatoridae - All 17 species of African honeyguides (Indicator, Melichneutes, Melignomon, Prodotiscus) are parasitic. Preferred hosts include barbets, although some utilize nests of woodpeckers and bee-eaters. Upon hatching, the offspring uses a sharp mandibular hook to punch holes in the host eggs. This hook drops off as the bird grows older.
         5. Icteridae - Of the 6 known species of cowbirds, 5 are known to be parasitic. Brown-headed cowbirds tend to use neotropical migrant birds as hosts and parasitism has been so successful that populations of some of these migrants are declining with up to 70% of the nests of some hosts being parasitized.
            1. Molothrus aeneus (bronzed cowbird) - South, Central, and North America
            2. Molothrus ater (brown-headed cowbird) - North America
               1. the female cowbird will lay an egg within a nest after the host has already laid two or more eggs, but before incubation has begun. This usually occurs just before sunrise.
               2. the female cowbird usually removes one or more of the host eggs by piercing the egg with her bill and carrying it away to be eaten.
               3. if the cowbird egg is too dissimilar to the host eggs, some birds will abandon their nest or remove the cowbird eggs.
            3. Molothrus badius (bay-winged cowbird) - South America (non-parasitic)
            4. Molothrus bonariensis (shiny cowbird) - South, Central, and North America
            5. Molothrus rufoaxillaris (screaming cowbird) - South America
            6. Scaphidura oryzivora (giant cowbird) - South, Central, and North America
         6. Ploceidae - Of the 117 known species, only Anomalospiza imberbis (cuckoo-weaver or cuckoo-finch) South of the Sahara is known to be parasitic where it lays its eggs in the nests of some species of warblers, especially cisticolas and prinias.
         7. Some other avian species actually practice intraspecific brood parasitism, where they place eggs within the nests of members of their own species. These include snow geese and cliff swallows.
   2. Oxpeckers "tick birds" (Buphagidae)
      1. Considered quasi-parasitic, with both parasitic and mutualistic attributes
      2. Two species of oxpeckers exist. Buphagus erythrorhynchus (red-billed oxpecker) and Buphagus africanus (yellow-billed oxpecker). The former species prefers thicker haired animals like antelope and giraffe, whereas the latter likes thinner haired animals like buffalo or rhinoceros. However, considerable overlap in feeding preference occurs.
      3. Some host species, for instance elephants, are reputed not to tolerate oxpeckers
      4. They often occur in small flocks, eating ectoparasites such as ticks, lice, flies, and fleas. However, they also readily consume secretions (earwax, sweat, tears, saliva, mucus), dead skin, wound tissues, and blood.
      5. Birds cannot survive simply on insects. The ticks they eat are engorged, and it is actually the blood within the ticks that is the predominate source of energy for the birds. However, studies have suggested that the birds only spend about 5% of their time foraging for ticks and that other sources of food may be more important
      6. Recent studies suggest that oxpeckers do little to reduce the number of ticks per host animal. However, even eliminating low numbers of engorged females may greatly affect the number of larval ticks that eventually end up in the environment
      7. One study (2000, Behavioral Ecology 11: 154-166) noted that oxpeckers will actually enlarge a break in the skin caused either by ticks or a scratch, and that animals without oxpeckers had fewer wounds and a faster wound healing time. Most foraging by oxpeckers seems to be in obtaining blood and secretions from a host, rather than in removing ticks
   3. Arctic skua or parasitic jaeger (Stercorarius parasiticus)
      1. These (Charadriiformes) birds are holoarctic (arctic and subarctic Canada, Russia) and breed in grassy or mossy tundra near water
      2. They tend to be opportunistic feeders, predominately predatory, with a diet that includes fish, insects, rodents, carrion, other birds, and bird eggs
      3. These birds are noted for robbing food from other birds (ingested or otherwise). They will sometimes pursue and hound other fish-eating birds to a point causing the victim to regurgitate a recently ingested meal which the Skua will then steal. Perhaps not parasitism per sec, but along with its name its interesting enough to be included on this page
   4. Sharp-beaked finch or Vampire bird (Geospiza nebulosa)
      1. 13 species of finches in the genus Geospiza occur within the Galapagos
      2. Many species eat ectoparasitic arthropods found in the plummage of other birds
      3. The sharp-beaked finch lives in the highlands of some of the central and western islands. It commonly pecks open the eggs of boobies (or sometimes rolls an egg around until it cracks open from a fall) to feed on the contents
      4. On Wolf Island, populations of sharp-beaked finches have also developed a habit of pecking at the skin of the legs of boobies until blood is drawn. The birds then drink the blood and have been given the name "Vampire finch."
   5. Galapagos mockingbirds (Nesomimus spp.)
      1. Three species, N. macdonaldi (Espanola mockingbird), N. melanotis (San Cristobal mockingbird), and N. parvulus (Galapagos mockingbird) all drink blood from living hosts which may include land iguanas, marine iguanas, tortoises, lava lizards, geckos, sea lions, seabirds, boobies, Waved albatross chicks, and/or goats.
      2. In many (but not all) cases, wounds are already established by other causes prior to the birds targeting the host.
      3. Mockingbirds on some islands drink blood, whereas birds on other islands do not seem to drink blood.
      4. Birds have also attempted to drink blood from minor wounds of researchers (1987, Auk 104: 517-521).
4. Mammals
   1. Vampire bats
      1. Vampire bats are native to Central and South America and can often be found in caves during the day either singly or in groups
      2. Small bats, 6-8 cm in length
      3. Three species exist (Desmodus rotundus, Diaemus youngi, Diphylla ecaudata)
      4. Species tend to be timid, but eventually chisel out a piece of skin of sleeping animals such as cattle, goats, swine, horses, and even large birds. The bat then laps up the blood over a 15-20 minute period of time
      5. A potent anticoagulant ("draculin") is found within the saliva. It is a noncompetitive inhibitor of activated factor X
      6. Vampire bats need to ingest about 2 tablespoons of blood each day to stay healthy. Failure to feed will result in rapid deterioration. These bats will also regurgitate a blood meal and share with a roostmate
      7. Although many cases of vampire bats feeding on humans are probably myth, there are numerous true documented cases. These cases even include whole families being parasitized on a nightly basis