Branchiobdellidans

Branchiobdellidans, or crayfish worms, are leech-like, clitellate annelids belonging to the Phylum Annelida and Order Brachiobdellida (single family Brachiobdellidae) that form an obligate, ectosymbiotic association primarily with astacoidean crayfishes. They have long been known as “branchiobdellid worms” because they were considered a separate family of the oligochaetes; however, more recent treatment of these worms as a separate taxonomic order technically renders their epithet more correctly as “branchiobdellidan worms” or simply “branchiobdellidans.” Branchiobdellidans are a monophyletic clade of more than 150 ectosymbiont species within twenty-one genera found throughout North and Central America, Europe, and eastern Asia, of which about fifteen genera and 107 species have been reported from North America, including in Arkansas. However, branchiobdellid fauna in Arkansas need further study.

In North America, these worms range from southern British Columbia across the Prairie Provinces to New Brunswick, Canada, and south to Costa Rica. Endemic distributions of most branchiobdellidan genera are found either to the east or west of the Continental Divide. The genera Cambarincola, Sathodilus, and Xironogiton occur on both sides of the divide, even though the respective species in these genera are endemic to one region or the other. Because of the introduction of crayfishes into other areas in the world, North American branchiobdellidans are now being reported in Japan, many countries in Europe, and possibly North Africa.

Branchiobdellidans have had a torturous taxonomic history, having been previously considered a family, thought to be an order, and ranked as high as a class. Currently, they are regarded as an order to reflect their independence from the equivalently ranked oligochaetes and leeches. Five previous families within this order were created earlier with the demotion of these five to subfamilies in 2001, namely, Branchiobdellinae, Cambarincolinae, Bdellodrilinae, Caridinophilinae, and Xironodrilinae. There now exists a more realistic systematic arrangement with the order Branchiobdellida, which contains a single family, the Branchiobdellidae, and four subfamilies. The former monotypic Chinese family, Caridinophilidae, was demoted and the genus placed in the Bdellodrilinae.

A close relationship among oligochaetes, branchiobdellidans, and hirudinids has been recognized for a number of years, but recent cladistic analysis using both morphological and molecular data suggests that these historically separate groups should be included within a larger taxonomic grouping, the Clitellata. The Clitellata are believed to have evolved in the Paleozoic seas over 500 million years ago.

The phylogenetic position of the Branchiobdellida within the Clitellata is generally accepted as being between the leeches and oligochaetes; however, the question of which of these two assemblages forms the sister group has not been resolved. The presence of a semiprosopore male duct in both branchiobdellidans and lumbriculid oligochaetes supports the branchiobdellidans being a sister group to the Lumbriculida. However, the constant segment number, loss of chaetae, development of anterior and posterior attachment organs, and jaws in branchiobdellidans are similar to those found in leeches.

Branchiobdellidans live on the external surface of their host, a type of crustacean. In Arkansas, this crustacean is usually a crayfish. A single host can be infected with over 1,800 individual worms, which can include up to eight species within five genera. Unfortunately, an understanding of the ecophysiological interactions of this complex symbiotic branchiobdellidan-crustacean association has progressed little in the 250 years since it was first discovered. While all branchiobdellidans require a live host in order for their embryonic development to be completed, these creatures have been reported to live independently on a nonliving substrate for several months. It seems all branchiobdellidans require their cocoons to be attached to a live host in order for embryonic development to be completed. With this in mind, these worms are considered obligate symbionts.

Interestingly, crayfish appear to tolerate the presence of these worms on their exoskeleton because the crustaceans can use their legs in grooming behavior to remove detritus and epibont accumulations from their body and gill surfaces. Crayfishes and other decapods have mechanoreceptors in their exoskeletons and are aware of these worms moving over their external surfaces.

The degree of dietary dependence of branchiobdellidans on their host is not consistent throughout the group. There are reports of that dietary range from herbivory to carnivory, with most species appearing to be opportunistic omnivores. So, it is incorrect to label all branchiobdellidans as parasitic.

Branchiobdellidans are characterized by a lack of anatomical and ecological diversity in comparison with equivalent clitellate taxa. They range in size from 0.8 to 10 millimeters in length with a distinct head from the body and, by definition, no protostomium. Body shape is primarily rod or spindle-shaped with some species having a pyriform or flask-like shape with either ventral or dorso-ventral flattening. The body has a consistent fifteen segments and is based on the number of paired ganglia in the ventral nerve cord. Two methods have been previously used to number the body segments of branchiobdellidans. First, the oligochaete system numbers each segmental ganglion using Roman numerals (I–XV) and is necessary for comparative studies in the Clitellata. For the last fifty years, a second system has been commonly used which recognizes the head and then numbers only the body segments, which are given in Arabic numerals (1–11). The head has a peristomium which is divided into dorsal and ventral lips with the dorsal lips occasionally supporting tentacles or lobes. The mouth is in the center of the peristominal surface and is usually surrounded by sixteen oral papillae. Each body segment is divided into a major anterior and a minor posterior annulus, while a few species have the major annulus divided further into two. Interestingly, segment 11 is modified into the posterior, disk-shaped attachment organ (sucker) and contains a single pair of ganglia (on XV).

Branchiobdellidans have an alimentary canal that consists of a pair of sclerotized jaws that are situated in the anterior pharynx, a short esophagus, a stomach, an intestine, and an anus that opens dorso-medially onto segment 10. Body movements are leech-like with anterior and posterior attachment organs that function to provide a strong attachment for the worm to the substrate. Most branchiobdellidans feed on detritus, algal filaments, diatoms, ciliates, nematodes, oligochaetes, insect larvae, and other branchiobdellidans. They tend to be opportunistic feeders, feeding on detached fragments of the host’s food and/or ingesting exposed host tissues if a break in the cuticle of the host occurs. These breaks often occur in the gill region—thus, their presence there. Many of these gill-dwelling worms have previously been mistakenly assumed to be parasites, although this has not been proven.

A vascular system is in place consisting of dorsal and ventral longitudinal vessels that are connected by four paired lateral branches in the head and a single pair of branches in other segments. Blood is circulated via peristaltic contractions of the dorsal vessel wall.

The central nervous system consists of a dorsal “brain,” circumesophageal connectives, and a paired ventral cord that extends to the last segment. The head contains four pairs of ganglis ventrally, and each body segment has its own single pair of ganglia.

Reproductively speaking, a pair of testes occurs in segments five and six. Oddly, there is a tremendous diversity in morphology of spermatozoa greater than currently known in any comparable clitellate taxon. A pair of ovaries is located in the coelom, and eggs are then released through a pair of short ducts in the body wall of that segment.

Unfortunately, Arkansas has received relatively little treatment of its branchiobdellid fauna. The first report of branchiobdellidans from the state listed nine species within four genera (Branchiobdella americana, Cambarincola chirocephala, C. elevata, C. macropdonta, C. vitrea, Pterodrilus mexicanus, Xironorilus dentatus, X. formosus, and X. pulcherrinus). A later revision of the genus Cambaricola listed the presence of Cambarincola restans in Sugar Creek, near Avoca (Benton County); Cambarincola mesochorea from three sites including Crittenden, Greene, and Marion counties in northern Arkansas; and Cambarincola vitrea in Benton, Crittenden, and Greene counties. In addition, Cambarincola chirocephala Ellis is listed from seven localities, including Benton, Carroll, Crittenden, Fulton, Logan, Newton, and Sharp counties. A detailed updated study of the crayfish worms of Arkansas is badly needed to elucidate the species currently known from the state and to further document the distributions of the species that inhabit Arkansas.

For additional information:
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Creed, Robert P., J. D. Lomonaco, M. J. Thomas, A. Meeks, and B. L. Brown. “Reproductive Dependence of a Branchiobdellidan Annelid on its Crayfish Host: Confirmation of a Mutualism.” Crustaceana 88 (2015): 385–396.

Gelder, Stuart R., H. C. Carter, and D. N. Lausier. “Distribution of Crayfish Worms or Branchiobdellidans (Annelida: Clitellata) in New England.” Northeastern Naturalist 8 (2001): 79–92.

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Gelder, Stuart R., Nicole L. Gagnon, and Kerri Nelson. “Taxonomic Considerations and Distribution of the Branchiobdellida (Annelida: Clitellata) on the North American Continent.” Northeastern Naturalist 9 (2002): 451–468.

Gelder, Stuart R., and Bronwyn W. Williams. “Clitellata: Branchiobdellida.” In Thorp and Covich’s Freshwater Invertebrates, 4th ed., Vol. I: Ecology and General Biology, edited by James H. Thorp and D. Christopher Rogers. New York: Academic Press, 2014.

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Hobbs, Horton H., Jr., Perry C. Holt, and M. Walton. “The Crayfishes and Their Epizootic Ostracod and Branchiobdellid Associates of the Mountain Lake, Virginia, Region.” Proceedings of the United States National Museum 123 (1967): 1–84.

Hoffman, Richard L. “A Revision of the North American Annelid Worms of the Genus Cambarincola (Oligochaeta: Branchiobdellidae).” Proceedings of the United States National Museum 114 (1963): 271–371.

Holt, Perry C. “Four New Species of Cambarincolids (Clitellata: Branchiobdellida) from the Southeastern United States with a Redescription of Oedipodrilus macbaini (Holt, 1955).” Proceedings of the Biological Society of Washington 101 (1988): 794–808.

———. “The Genus Pterodrilus (Annelida: Branchiobdellida).” Proceedings of the United States National Museum 125 (1968): 1–44.

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———. “A New Branchiobdellid of the Genus Cambarincola (Oligochaeta, Branchiobdellidae) from Virginia.” Virginia Journal of Science 5 (1954): 168–172.

———. “New Genera and Species of Branchiobdellid Worms (Annelida: Clitellata).” Proceedings of the Biological Society of Washington 81 (1968): 291–318.

———. “Newly Established Families of the Order Branchiobdellida (Annelida: Clitellata) With a Synopsis of the Genera.” Proceedings of the Biological Society of Washington 99 (1986): 676–702.

———. “On Ankyrodrilus, a New Genus of Branchiobdellid Worms (Annelida).” Virginia Journal of Science 16 (1965): 9–21.

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———. “Status of the Genera Branchiobdella and Stephanodrilus in North America with Description of a New Genus (Clitellata: Branchiobdellida).” Proceedings of the United States National Museum 124 (1967): 1–10.

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Holt, Perry C., and B. D. Opell. “A Checklist of and Illustrated Key to the Genera and Species of the Central and North American Cambarincolidae (Clitellata: Branchiobdellida).” Proceedings of the Biological Society of Washington 106 (1993): 251–295.

Larson, Eric R., and Bronwyn W. Williams. “Historical Biogeography of Pacifastacus Crayfishes and Their Branchiobdellidan and Entocytherid Ectosymbionts in Western North America.” In Freshwater Crayfish: A Global Overview, edited by T. Kawai, Z. Faulkes, and G. Scholtz. New York: CRC Press, 2015.

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Skelton, James, Robert P. Creed, Lukas Chandler, Kevin M. Geyer, and Bryan L. Brown. “Geographic Patterns of Crayfish Symbiont Diversity Persist Over a Half Century Despite Seasonal Fluctuations.” Freshwater Crayfish 22 (2016): 9–18.

Skelton, James, Kaitlin J. Farrell, Robert P. Creed, Bronwyn W. Williams, C. Ames, B. S. Helms, J. Stoekel, and Bryan L. Brown. “Servants, Scoundrels, and Hitchhikers: Current Understanding of the Complex Interactions Between Crayfish and their Ectosymbiotic Worms (Branchiobdellida).” Freshwater Science 32 (2013): 1345–1357.

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Henry W. Robison
Sherwood, Arkansas

Chris T. McAllister
Eastern Oklahoma State College