Biology 625
ANIMAL PARASITOLOGY
Fall semester lecture note outline

Updated: 24 September 1999

1. Male with copulatory bursa derived from cuticle
2. Five superfamilies and numerous families

Superfamily: Ancylostomoidea (hookworms)

1. In small intestine of mammals
2. Large, highly sclerotized buccal capsule with cutting teeth or plates
3. Various authors have proposed various taxonomic schemes. The following adopted for this class divides the hookworms into two groups
   1. Ancylostomatinae
      1. Duct of dorsal esophageal gland usually in a dorsal gutter on inner surface of the buccal capsule
      2. 1 dorsal ray on male copulatory bursa
      3. gubernaculum present
      4. female tail with terminal spine
      5. vulva posterior to mid-body
      6. predominately in carnivores and omnivores; few in herbivores
      7. representative genera
         1. Ancylostoma
         2. Arthrocephalus
         3. Arthrosoma
         4. Galoncus
         5. Globocephalus
         6. Placoconus
         7. Uncinaria
   2. Bunostominae
      1. Members have a tooth-like dorsal cone supporting the duct of the dorsal esophageal gland
      2. 2 dorsal rays on male copulatory bursa
      3. gubernaculum absent
      4. female tail without terminal spine
      5. with one exception, vulva in anterior one-half of body
      6. predominately in omnivores and herbivores; few in carnivores and primates
      7. representative genera
         1. Bunostomum
         2. Gaigeria
         3. Necator
   3. Life-cycles
      1. Adults in gut, attached to mucosa of small intestine. Suck blood.
      2. Unembryonated eggs produced after mating
      3. Out with feces; embryonate
      4. Hatch; rhabditiform L1s produced (free-living)
      5. L2 (free-living) - L3 (filariform)
      6. Penetrate skin (most can also be ingested)
      7. Through blood vessels; enter lungs
      8. Molt to L4
      9. Migrate up trachea; swallowed
      10. Attach to gut wall; molt into adults
   4. Some species have migrating L3s in tissues that can become dormant (arrested development). Can enter offspring via lactation.
   5. Representative species
      1. Ancylostoma braziliense (dogs and felids in tropics)
      2. Ancylostoma caninum (canids throughout world; common cause of cutaneous larval migrans)
      3. Ancylostoma ceylanicum (dogs, felids, humans in SE Asia)
      4. Ancylostoma duodenale (humans worldwide)
      5. Ancylostoma tubeforme (felids worldwide)
      6. Bunostomum phlebotomum (cattle and deer worldwide)
      7. Bunostomum trigonocephalum (sheep, goats, cervids, camelids worldwide)
      8. Globocephalus urosubulatus (swine worldwide)
      9. Necator americanus (humans worldwide)
      10. Placoconus lotoris (raccoons, skunks in North America; larvae are only infective if ingested)
      11. Uncinaria lucasi (seals and sea lion pups in Pacific)
      12. Uncinaria stenocephala (carnivores, mainly canids, in Northern hemisphere)

Superfamily: Strongyloidea (strongilids)

1. Species have large, complex buccal capsules
2. Some with corona radiata, which is a series of leaf-like structures surrounding mouth
3. No teeth or plates at mouth opening, but some with teeth at base of buccal capsule
4. Four families
   1. Chabertiidae (most notable, the nodular worms)
   2. Deletrocephalidae (in Rhea americanus)
   3. Strongylidae (most notable, the large equine strongyles)
   4. Syngamidae (most notable, the gapeworms of birds)
5. Typical life-cycle
   1. Adults produce unembryonated eggs that pass out with feces
   2. Embryonate rapidly in environment
   3. Most genera L1 hatches from egg and free-living until the L3 stage; in gapeworms L3 hatches
   4. In most species, L3s ingested; in gapeworms and the swine kidney worm (Stephanurus dentatus), L3s sequester in earthworm and gastropod paratenic hosts
   5. Strongylids exit gut and mature somewhat in extra-intestinal sites; often complete maturation in nodules in gut wall
   6. Mature into adults; some with odd migrations
6. Representative species of the family Strongylidae
   1. Strongylus edentatus (adults in caecum and colon of horses; some larval maturation in liver; final maturation in hemorrhagic nodules in gut; no buccal teeth)
   2. Strongylus equinus (adults in caecum and colon of horses; some maturation in liver; nodules in gut wall then emergence; 2 buccal teeth, separated)
   3. Strongylus vulgaris (adults in caecum and right ventral colon of horses; some larval maturation in submucosal arteries; nodules in gut wall then emergence; 2 buccal teeth, side-by-side)
7. Representative species of the family Chabertiidae
   1. Castorstrongylus castoris (adults in colon of beaver)
   2. Chabertia ovina (in large intestine of camelids, bovids, cervids)
   3. Oesophagostomum spp. (in ruminants, camelids, swine, primates, rodents. L3s encapsulate in gut (nodules), transform into L4s, emerge back into gut.
8. Representative species of the family Syngamidae
   1. Cyathostoma bronchialis (adults in capsules in wall of respiratory system in anseriforms)
   2. Mammomonogamus spp. (various species, encapsuled as adults in larynx, nasal cavities, pharynx, middle ear, etc. in ruminants, felids, elephants, and cervids in tropics)
   3. Stephanurus dentatus (adults in capsules in perirectal fat and walls of ureter of swine)
   4. Syngamus trachea (in trachea of galliforms, and some other species)

Superfamily: Trichostrongyloidea (trichostrongylids)

1. Very large superfamily, with 14-15 families
2. Unlike the hookworms and strongylids, the buccal capsule is absent or greatly reduced, the lips and a corona radiata are absent or vestigial; teeth rare
3. Lateral lobes of bursa very highly developed; sometimes dorsal lobe reduced
4. Highly diverse, in many groups of terrestrial vertebrates (especially mammals and birds)
5. Mainly in host stomach and intestine as adults; few species in other areas
6. Typical life-cycle
   1. Adults in gut; produce thin-shelled eggs out with feces
   2. Embryonate; hatch
   3. L1 and L2 are free-living
   4. L3 ingested (in some species, penetrate skin or do both)
   5. In many species, L3 invade gut mucosa, molt to L4, and return to gut lumen; species that penetrate skin undergo lung migration where transformation to L4
   6. Mature into adults in gut
7. Representative genera and species
   1. Cooperia punctata (in cattle and other ruminants; cuticle striated anteriorly)
   2. Haemonchus contortus (abomasal barber-pole worm of ruminants and cervids)
   3. Dictyocaulus spp. (in ruminants and cervids)
   4. Heligmosomoides polygyrus (in wild mice)
   5. Hyostrongylus rubidus (in swine)
   6. Molineus barbatus (in small intestine of raccoons and skunks)
   7. Nematodirus spp. (in bovids, cervids, camelids)
   8. Nippostrongylus braziliensis (in small intestine of Rattus spp.)
   9. Obeliscoides cuniculi (in rabbits)
   10. Ostertagia ostertagi (stomach worm in cattle; dirty brown color)
   11. Oswaldocruzia pipens (in intestine of frogs, lizards)
   12. Trichostrongylus spp. (small reddish worms; many species; many hosts)

Superfamily: Metastrongyloidea (lungworms)

1. Seven families and about 45 genera
2. All species infect mammals (none in cattle or horses)
3. As adults, most species occupy lungs of host; some in veins distant from host or in pulmonary or mesenteric arteries; few in frontal sinuses.
4. Many species require an invertebrate intermediate host; some use vertebrate or invertebrate paratenic host
5. Buccal cavity reduced or absent
6. Bursal rays and lobes reduced
7. Life-cycle
   1. Species in lungs deposit unembryonated eggs in lungs; species not in lungs either deposit unembryonated eggs in blood vessels and eggs carried to lungs where they lodge in capillaries or have alternate route; some in lungs ovoviviparous
   2. Embryonation
   3. L1s hatch
   4. Most species, L1s up trachea and swallowed; few in mesenteric blood vessels have L1s that break through gut wall
   5. L1s passed in feces
   6. L1s ingested by gastropods (swine lungworm, use earthworms)
   7. Molt to L2, then L3
   8. Eaten; carnivores utilize paratenic hosts (i.e. amphibia, reptiles, rodents, shrews) that have ingested infected gastropods
   9. Migration of L3s through host; many diverse methods; i.e.
      1. Lymphatics - blood vessels - heart circulation - lungs
      2. Hepatic portal system - heart circulation- lungs
      3. Cross gut - crawl through peritoneum - cross diaphragm - enter lungs directly
      4. Cross gut - enter central nervous system - mature - migrate to other sites in body prior to laying eggs
      5. Mature in gut wall - cross gut - migrate to lungs or frontal sinuses
8. Representative genera and species
   1. Aelurostrongylus abstrusus (lungs of cats) and A. pridhami (lungs of mink)
   2. Crenosoma mephitidis (lungs of skunk); C. vulpis (in lungs of canids and mustelids)
   3. Didelphostrongylus hayesi (in lungs of opossum)
   4. Elaphostrongylus rangiferi (in meninges and muscles of reindeer)
   5. Filaroides decorus (lungs of sea lions), F. hirthi (lungs of beagles), and F. martis (lungs of mink)
   6. Halocerus lagenorhynchi (lungs of toothed whales)
   7. Metastrongylus apri (in lungs of swine; use earthworms as intermediate host)
   8. Muellerius capillaris (lungs of sheep and goats)
   9. Oslerus osleri (nodules in trachea and bronchi of canids) and O. rostratus (lungs of felids)
   10. Parastrongylus cantonensis (pulmonary arteries of rats) and P. costaricensis (mesenteric arteries of rodents)
   11. Parelaphostrongylus andersoni and P. odocoilei in blood vessels of the muscles of white-tailed (P. andersoni) and mule and black-tailed deer (P. odocoilei); Parelaphostrongylus tenuis (in meninges of white-tailed deer; neurologic disease in reindeer, caribou, elk, moose, mule and black-tailed deer)
   12. Protostrongylus boughtoni (in lungs of snowshoe hares in Canada)
   13. Protostrongylus rushi and P. stilesi (in lungs of bighorn sheep and mountain goats)
   14. Skrjabingylus chitwoodorum (frontal sinuses of skunks); S. lutrae (frontal sinuses of otter); S. nasicola (frontal sinuses of mustelids)