Annelids

The phylum Annelida consists of over 22,000 living species of segmented worms. They include earthworms, leeches, and ragworms. Annelids are bilaterally symmetrical, triploblastic invertebrates that inhabit a wide diversity of habitats, including marine environments such as tidal zones, hydrothermal vents, lotic and lentic freshwater habitats, and moist terrestrial habitats. The term “Annelida” originated in 1802 from French naturalist, Jean-Baptiste Lamarck’s (1744‒1829), annélides. Several species of annelids can be found in Arkansas.

The overall classification of the phylum is undergoing significant revisions and has not yet been stabilized completely. Phylogenomic and other molecular phylogenetic analyses have shown that taxonomic groupings previously based on morphology in many cases are invalid. The phylum was previously divided into three classes as follows: Polychaeta (marine, freshwater, and terrestrial polychaetes, about 12,000 species), Oligochaeta (earthworms, about 10,000 species), and Hirudinea (leeches, about 700 species). However, more recently, all three groups are no longer recognized. The Oligochaeta and Polychaeta are currently determined to be paraphyletic groups and no longer hold any systematic ranking. Instead, the terms “oligochaete” and “polychaete” are simply used as informal, common names. The closest relative of Hirudinea (Hirudinoidea) is actually found inside the Oligochaeta and is the family Lumbriculidae. Because of this finding, the Oligochaeta and the Hirudinea are now referred to as the Clitellata, an old taxon that dates back to 1919. To further complicate matters, Clitellata has been shown to have arisen from deep within the Polychaeta, thereby making “Polychaeta” synonymous with Annelida.

The Archiannelida, minute annelids that occur in the spaces between grains of marine sediment, were formerly treated as a separate class because of their simple body structure but are now regarded as polychaetes. Some other groups of organisms have been formerly classified in various ways (primarily as separate phyla) but are now widely regarded as annelids. They include Pogonophora/Siboglinidae, which has been reclassified as a family; the Siboglinidae, within the polychaetes; the Echiura, which was determined by a molecular phylogenetics analysis in 1997 to be annelids; the Myzostomida, which live on crinoids and other echinoderms, mainly as parasites now recognized as a sub-group of polychaetes; and the Sipuncula, which was confirmed by molecular analysis of their close relationship to the Myzostomida and Annelida (including echiurans and pogonophorans). In addition, branchiobdellids are an order of leech-like clitellates that are mostly ectoparasites of crayfish.

Characteristics of annelids include: (1) bilaterally symmetrical, vermiform protostomes that live in marine, freshwater, or terrestrial habitats; (2) development typically protostomous, with holoblastic, spiral, schizocoelous embryology; (3) segments arising by teloblastic growth (the Echiura and Sipuncula show no obvious signs of segmentation); (4) complete digestive tract with regional specializations; (5) closed circulatory system, with most adults having metanephridia, or protonephridia in some; (6) well-developed nervous system with dorsal cerebral ganglion and ventral ganglionated nerve cords; (7) lateral chetae present in most species; (8) head with a prostomium and peristomium; and (9) hermaphroditic or gonochoristic with development direct or indirect, often with a trochophore larva. Annelids range in size from microscopic to the Australian giant Gippsland earthworm (Megascolides australis) and the Mekong giant earthworm (Amynthas mekongianus), which can both grow up to 3 m (9.8 ft.) long.

Nearly all polychaete annelids possess parapodia (unjointed paired extensions of the body wall) that function as limbs, while other major annelid groups lack them. They are often supported internally by one or more large, thick chetae. Often, the parapodia of burrowing and tube-dwelling polychaetes are simple ridges whose tips bear hooked chetae. Many annelids move by peristalsis (waves of contraction and expansion that sweep along the body), or flex the body while using parapodia to crawl or swim.

Annelids are known from the early Cambrian (518 million years ago), although they may be slightly older, as some of the late Ediacaran fossils may represent annelids. Fossils of polychaete groups appear by the late Carboniferous (299 million years ago). Oligochaete fossils may appear in the mid-Ordovician (472 to 461 million years ago), although there is disagreement. The earliest indisputable oligochaete fossils come from the Paleogene period, which began 66 million years ago.

One major generalized annelid includes the earthworms. They have a complete digestive system: food passes through the mouth into the pharynx, which moistens the dirt, and it moves into the esophagus. From there the dirt moves into the crop (a temporary storage area) and then into a muscular gizzard. The gizzard secretes digestive enzymes to chemically break down organic matter contained in the dirt, as well as physically grinding up the dirt before it moves into the intestine where actual digestion occurs. After passing through the intestine the dirt is expelled through the anus. However, in tube-dwellers (family Siboglinidae), the gut is blocked by a swollen lining housing symbiotic bacteria, which can make up 15 percent of the worms’ total weight. These bacteria convert inorganic matter, such as carbon dioxide and hydrogen sulfide from hydrothermal vents, or methane from seeps, to organic matter that feeds themselves and their hosts, while the tubeworms extend their palps into the gas flows to absorb the gases needed by the bacteria.

Interestingly, there is no respiratory system in segmented worms, but rather they breathe via the skin. This is often referred to as cutaneous respiration. Oxygen and carbon dioxide exchange both occur by simple diffusion at the site of the skin. However, in many polychaetes and in some clitellates (the group to which earthworms belong) gills are associated with most segments, often as extensions of the parapodia in polychaetes. Indeed, the gills of tube-dwellers and burrowers usually cluster around whichever end has the stronger water flow.

The circulatory system in an earthworm is a closed system and basically is a loop. Instead of a true heart, earthworms have five aortic arches that pump blood through the dorsal blood vessel; it then returns through the ventral blood vessel.

Annelids with blood vessels remove soluble waste products with metanephridia, while those without use protonephridia. Both of these nitrogenous waste systems use a two-stage filtration process, in which fluid and waste products are first extracted and then filtered again to reabsorb any reusable materials while dumping toxic and spent materials as urine.

Earthworms have no central brain structure, but rather possess two cerebral ganglia that are situated in the anterior portion of the body. The ganglia are attached to a ventral nerve cord that runs the length of the animal. Earthworms are able to sense chemicals, moisture, light, temperature, touch, vibrations, and tastes.

With regard to a reproductive system, most mature clitellates such as earthworms and leeches are fully hermaphroditic animals, and thus they possess both male and female reproductive organs on the same organism. The exception is that in a few leech species, younger adults function as males and then, at maturation, become females. Some oligochaetes, such as Dero (Aulophorus) furcatus, appear to reproduce entirely asexually, while some others reproduce asexually in the summer and sexually in fall. Polychaetes can reproduce asexually by dividing into two or more pieces or by budding off a new individual while the parent remains a complete organism. All clitellates have well-developed gonads, and all copulate. However, they cannot fertilize themselves and must reproduce with another earthworm. To accomplish this, two earthworms must line up opposite of each other and use their setae to grip one another before engaging in copulation. Earthworms are able to store the sperm of the partner. Sperm ducts release the sperm, and it travels through grooves located on segments 16 through 25 before being stored in spermathecal (“sperm stores”). The clitellum secretes mucous that becomes a cocoon in which the eggs remain for two to three weeks before hatching. The eggs of leeches are fertilized in the ovaries and then transferred to the cocoon. In addition, the cocoon also either produces yolk when the eggs are fertilized or nutrients while they are developing. Earthworms and leeches hatch as miniature adults rather than producing a larval stage.

Earthworms play an integral part in the ecology of the terrestrial environment. They generally burrow into the soil, but some live in moist leaf litter. They loosen the soil so that oxygen and water can penetrate it, and both surface and burrowing worms help to produce soil by mixing organic and mineral matter by accelerating the decomposition of organic matter and making it more quickly available to other organisms, and by concentrating minerals and converting them to forms that plants can use more easily. Earthworms function as valuable prey for a variety of vertebrates, including amphibians, reptiles, birds, and mammals. The burrowing of marine polychaetes encourages the development of ecosystems by enabling water and oxygen to penetrate the ocean floor.

Annelids have an important interplay with humans. By helping farmers and gardeners, they are best known for aerating the soil. In addition, earthworms have been used as fish bait since ancient times. Other annelids such as leeches have also been important to humans through the centuries. Leeches may attach to humans and animals and suck blood, in some cases transmitting flagellates that can be pathogenic. Since ancient times, there are accounts of using medicinal leeches (Hirudo medicinalis) in blood-letting. Interestingly, leeches are still being used in medicine in the twenty-first century, such as assisting in microsurgery, as their saliva has provided anti-inflammatory compounds and several important anticoagulants, one of which also prevents tumors from spreading.

Because of the ease in which anglers spread invasive terrestrial earthworms, numbers of North American native earthworms have been drastically reduced over the years. In the twenty-first century, throughout portions of North America, introduced earthworms are more common. For example, in the glaciated portions of North America, almost all native earthworms are thought to have been killed by the glaciers, and the worms currently found in those areas are all introduced from other areas, primarily from Europe, and, more recently, from Asia. Northern hardwood forests have especially been harmed by invasive worms through the loss of leaf duff, loss of soil fertility, changes in soil chemistry, and loss of ecological diversity. The introduced earthworm Amynthas agrestis is especially destructive, and one state (Wisconsin) has listed it as a prohibited species.

In Arkansas, two species of endogeic segmented worms (earthworms that build complex lateral burrow systems in all layers of the soil) that are endemic in the state include Means’ giant earthworm (Diplocardia meansi) and D. sylvicola. Restricted to the drier soils of rocky talus slopes on Rich Mountain in Polk County, D. meansi is the second-largest known earthworm (at nearly 0.6 m [2 ft.] in length) in the eastern United States and is also bioluminescent. It is considered to be possibly extirpated. Diplocardia sylvicola was used in a study of residue and burning interaction with tillage to influence earthworm densities in the Lower Mississippi River Valley (Delta) region of eastern Arkansas.

Except for numerous recent studies on leeches that included twenty-two species from five families reported from the northern part of the state, Arkansas has been scarcely studied for other annelids. Two early publications in the 1950s listed twenty-one species within nine genera of earthworms from Arkansas. Of these, ten species were regarded as native to the United States, eight were introduced European forms, and three were Asiatic in origin. Another study, published in 1953, reported on the Microndrili oligochaetes of the state. Also, a survey of benthic macroinvertebrates of Flat Bayou (Wabbaseka Bayou) in northeastern Lincoln County reported a few annelids. A 2011 dissertation included research on the evolutionary origin and ecological niche and how that might impact how earthworm species affect nitrogen cycling in the state. However, there are no additional surveys that list the annelids of the state, and additional research is sorely needed on this group of invertebrates of the state.

For additional information:
Anderson, F. E., Bronwyn W. Williams, K. M. Horn, C. Erséus, K. M. Halanych, S. R. Santos, and S. W. James. “Phylogenomic Analyses of Crassiclitellata Support Major Northern and Southern Hemisphere Clades and a Pangaean Origin for Earthworms.” BMC Evolutionary Biology 17 (2017):123.

Brusca, Richard C., W. Moore, and S. M. Shuster. Invertebrates. 3rd ed. Sunderland, MA: Sinauer Associates, 2016.

Budd, Graham E., and Soren Jensen. “A Critical Reappraisal of the Fossil Record of the Bilaterian Phyla.” Biological Reviews of the Cambridge Philosophical Society 75 (2000): 253–295.

Causey, David. “Additional Records of Arkansas Earthworms.” Proceedings of the Arkansas Academy of Science 6 (1953): 47‒48. Online at https://scholarworks.uark.edu/cgi/viewcontent.cgi?article=1175&context=jaas (accessed February 10, 2020).

———. “Earthworms of Arkansas.” Proceedings of the Arkansas Academy of Science 5 (1952): 31‒41. Online at https://scholarworks.uark.edu/cgi/viewcontent.cgi?article=1140&context=jaas (accessed February 10, 2020).

———. “On Arkansas Microndrili.” Proceedings of the Arkansas Academy of Science 6 (1953): 53‒60. Online at https://scholarworks.uark.edu/cgi/viewcontent.cgi?article=1178&context=jaas (accessed February 10, 2020).

Dunn, Casey W., Gonzalo Giribet, Gregory D. Edgecombe, and Andreas Hejnol. “Animal Phylogeny and its Evolutionary Implications.” Annual Review of Ecology and Evolutionary Science 45 (2014): 371‒395.

Dunn, Casey W., et al. “Broad Phylogenomic Sampling Improves Resolution of the Animal Tree of Life.” Nature 452 (2008): 745‒749.

Eldredge, Niles, and S. M. Stanley, eds. Living Fossils. New York: Springer-Verlag, 1984.

Erséus, Christer. “Phylogeny of Oligochaetous Clitellata.” Hydrobiologia 535 (2005): 357‒372.

Gates, Gordon E. “Check List and Bibliography of North American Earthworms.” American Midland Naturalist 27 (1942): 86‒108.

———. “Farewell to North American Megadriles.” Megadrilogica 4 (1982): 12‒78.

———. “More on the Earthworm Genus Diplocardia.” Megadrilogica 3 (1977): 1‒49.

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.

Glasby, Christopher J., and Timmo Tarmo. “Global Diversity of Polychaetes (Polychaeta: Annelida) in Freshwater.” Hydrobiologia 595 (2008): 107‒115.

Halanych, K. M. “The New View of Animal Phylogeny.” Annual Review of Ecology, Evolution, and Systematics 35 (2004): 229–256.

Halanych, K. M., T. G. Dahlgren, and D. McHugh. “Unsegmented Annelids? Possible Origins of Four Lophotrochozoan Worm Taxa.” Integrative and Comparative Biology 42 (2002): 678–684.

Hensley, Carlee. “Earthworm Dynamics in Tallgrass Prairies in the Ozark Highlands Region of Northwest Arkansas.” MS thesis, University of Arkansas, 2020. Online at https://scholarworks.uark.edu/etd/3806/ (accessed July 6, 2022).

Holt, T. C. 1968. “The Branchiobdellida: Epizootic Annelids.” Biologist 1 (1968): 79‒94.

Jenner, R. A. “Challenging Received Wisdoms: Some Contributions of the New Microscopy to the New animal Phylogeny.” Integrative and Comparative Biology 46 (2006): 93–103.

Klemm, Donald J. Leeches (Annelida: Hirudinea) of North America. EPA-600/3 – 82/025. Cincinnati, OH: United States Environmental Protection Agency, Environmental and Support Laboratory, 1982.

Martin, P. “On the Origin of the Hirudinea and the Demise of the Oligochaeta.” Proceedings of the Royal Society of London B268 (2001): 1089‒1098.

McAllister, Chris T., William E. Moser, Dennis J. Richardson, and Henry W. Robison. “New Host and Geographic Distribution Record for the Leech, Myzobdella reducta (Annelida: Hirudinida: Rhynchobdellida: Piscicolidae), from Arkansas.” Journal of the Arkansas Academy of Science 66 (2012): 190–192. Online at http://scholarworks.uark.edu/cgi/viewcontent.cgi?article=1326&context=jaas (accessed February 10, 2020).

McHugh, D. “Molecular Evidence that Echiurans and Pogonophorans are Derived Annelids.” Proceedings of the National Academy of Sciences of the United States of America 94 (1997): 8006–8009.

Moser, William E., Donald J. Klemm, Dennis J. Richardson, Benjamin A. Wheeler, Stanley A. Trauth, and Bruce A. Daniels. “Leeches (Annelida: Hirudinida) of Northern Arkansas.” Journal of the Arkansas Academy of Science 60 (2006): 84–95. Online at http://scholarworks.uark.edu/cgi/viewcontent.cgi?article=1502&context=jaas (accessed February 10, 2020).

Rickett, John D. “Abundance, Diversity and Distribution of Benthic Macro-Invertebrates in the Flat Bayou Drainage Area, Jefferson County, Arkansas.” Proceedings of the Arkansas Academy of Science 33 (1979): 67‒70. Online at https://scholarworks.uark.edu/cgi/viewcontent.cgi?article=2709&context=jaas (accessed February 10, 2020).

Robison, Henry W., and Robert T. Allen. Only in Arkansas: A Study of the Endemic Plants and Animals of the State. Fayetteville: University of Arkansas Press, 1995.

Robison, Henry, Chris McAllister, Christopher Carlton, and Robert Tucker. “The Arkansas Endemic Biota: With Additions and Deletions.” Journal of the Arkansas Academy of Science 62 (2008): 84–96. Online at http://scholarworks.uark.edu/jaas/vol62/iss1/14/ (accessed February 10, 2020).

Sawyer, R. T. “Leeches (Annelida: Hirudinea).” In Pollution Ecology of Freshwater Invertebrates, edited by C. W. Hart Jr and S. L. H. Fuller. New York: Academic Press, 1974.

Sket, Boris, and Peter Tronteli. “Global Diversity of Leeches (Hirudinea) in Freshwater.” Hydrobiologia 595 (2007): 129‒137.

Smith, F. “North American Earthworms of the Family Lumbricidae in the Collections of the United States National Museum.” Proceedings of the United States National Museum 52 (1917): 157‒182.

Struck, T. H., C. Paul, N. Hill, S. Hartmann, C. Hösel, M. Kube, B. Lieb, A. Meyer, R. Tiedemann, G. N. Purschke, and C. Bleidorn. “Phylogenomic Analyses Unravel Annelid Evolution.” Nature 471 (2011): 95–98.

Thomason, Jill E., Mary C. Savin, Kristofor R. Brye, and Edward E. Gbur. “Native Earthworm Population Dominance after Seven Years of Tillage, Burning, and Residue Level Management in a Wheat-Soybean, Double-Crop System.” Applied Soil Ecology 120: 211‒218.

Tomlison, Peter J. “Earthworms of Arkansas and Contributions of Earthworm Evolutionary Origin and Ecological Group to Nitrogen Cycling in a Model Soil and Tall Fescue System.” PhD diss., University of Arkansas, 2011. Online at https://scholarworks.uark.edu/etd/223 (accessed February 10, 2020).

Williams, J. I., and Eugene M. Burreson. “Gonimosobdella klemmi n. gen. sp. (Hirudinida: Piscicolidae) from Cyprinid Fishes in Arkansas, Illinois, and Missouri, U.S.A.” Comparative Parasitology 72 (2005): 166–172.

Henry W. Robison
Sherwood, Arkansas

Chris T. McAllister
Eastern Oklahoma State College