Tongue Biters and Deep Sea Giants: The Cymothoida (Crustacea: Isopoda)

The above picture shows a member of the Cymothoida suborder of isopod (Wägele, 1989), containing over 2700 species according to the Smithsonian’s world list of isopods. Cymothoidae (the family, not the suborder; notice the endings!) are well-known across the internet for their wacky parasitic lifestyle (some call it gruesome).

The one pictured at the top of this post is quite unique. It’s either a Ceratothoa or a Cymothoa species, the two most common genera with species exhibiting this tongue-biter phenotype, in which the female attaches to the tongue of the fish. It’s fascinating not only for its strangeness, but also because it’s the only known case of a parasite effectively replacing any of its host’s organs. What happens is the cymothoid attaches to the tongue to feed on blood, but ends up drinking so much that the tongue atrophies and falls off. The cymothoid stays, and the host uses it as its tongue (Brusca & Gilligan, 1983).

As all parasites, parasitic Cymothoida either converge at similar morphologies or get so simplified or convoluted that species recognition is very hard, and the possibility/number of cryptic species is very high. The tongue-biter phenotype described above is quite unique, but the majority of them are so similar even in lifestyle that they can only be recognised by detailed morphological analysis and host identification. If you need ID help with parasitics or non-parasitics, contact me or comment.

I will avoid a discussion of the higher-level relationships of the cymothoids within the isopods, as this is an area of the tree with a lot of confused history and disparate taxon names that have been extensively redefined or have faded into nonexistence. See the introduction in Brandt & Poore (2003) if you’re interested. Current consensus is that Cymothoida is a valid suborder characterised by carnivorous- and parasitic lifestyle-adapted mouthparts (particularly a thin, blade-like slicing mandibular molar process). It contains four superfamilies according to Ahyong et al. (2011) (which itself is most probably based on Brandt & Poore (2003)): Anthuroidea (6 fam., 600+ spp.), Bopyroidea (5 fam., 700+ spp.), Cryptoniscoidea (7 fam., 100+ spp.), and Cymothooidea (9 fam., 1300+ spp.).

I will highlight some of the more well-studied families now. Species numbers come from Ahyong et al. (2011). Here’s what you should look out for: the diversity of lifestyles evident in the Cymothoida. They’re not all parasitic, not even in the same superfamily. There is conservation of a certain lifestyle within each family, and this makes them potentially very interesting as a study system for the evolution of lifestyles at the higher level (and not just of parasitism); I’d be particularly interested in how they became associated with their particular hosts. Of course, this needs a solid phylogenetic framework that doesn’t yet exist. I’m not sure if there’s any ongoing project investigating this (anyone wanna hire me for it?), but it would make a neat research theme for an entire lab.

Cymothooidea

Gnathiidae is a 200+ species-rich family known from all depths, even down to the abyss (Cohen & Poore, 1994), although most species are shallow-marine. Their larvae are ectoparasitic on fish, feeding on blood and tissue fluids. They’re most notable for being the most common coral reef fish parasite (Grutter et al., 2000), and they play a large role in the cleaner fish-host fish mutualism (Grutter, 1999). Infection is always temporary, lasting a couple of minutes and maximum a couple of hours (Paperna & Por, 1977). Adults are non-feeding, often found in association with sponges, polychaete tubes, coral rubble, barnacle nests, or otherwise on the benthos (Wägele, 1988), where they reproduce. The resultant juveniles, the zuphea 1 stage, start the parasitic cycle, finding and feeding on the fish to become the bloated praniza 1 larvae. They detach, becoming the zuphea 2 stage, which finds another host, and the cycle continues until the praniza 3 stage, at which point they migrate to molt to the adult stage (Smit & Davis, 2004). You can tell adult males and females apart by the mandibles, which are greatly enlarged in the male.

The Cymothoidae (380+ spp.) contains the species most commonly pictured on the internet, including the one from the beginning of the post. They’re ectoparasites attaching themselves to the skin, fins, gills or mouth of fish, both marine and freshwater (Brusca, 1981); sometimes they also drill into the musculature, to feed on blood (Trilles, 1991). What fish is infected and where depends on the cymothoid species – they are highly host- and site-specific. The juveniles (mancae; these shouldn’t be confused with larvae, which don’t exist in Cymothoidae) produce anticoagulants to help their blood-feeding, and temporarily attach themselves to any fish they find to feed, since they can only feed on blood (they can’t hunt or scavenge). In effect, they use any fish as intermediate hosts (although some are not so loose, see Tsai et al. (1999)) until they find the correct host fish species, on which they will stay and develop into the male. Cymothoids are protandrous hermaphrodites, so if a female isn’t also present, the male will subsequently turn into a female. Once female, a cymothoid can’t deattach from the host. An environmental sexual determination system is also found, whereby females can secrete pheromones that prolong the masculinity of nearby males by stimulating androgen production (Raibaut & Trilles, 1993). The damage done by cymothoids on their host can be considerable: from decreased growth, weight and size (Lester & Roubal, 1995), through to anemia and tissue damage (Bunkley-Williams & Williams, 1998a), to death (Williams & Bunkley-Williams, 1994). As with the Gnathiidae, a cleaning mutualism exists to get rid of them, except here it’s with cleaner shrimp (Bunkley-Williams & Williams, 1998b). They’ve also radiated in some freshwater rivers, most notably the Amazon.

Aegidae (150+ spp.) are large, opportunistic parasites, attaching themselves to fish temporarily to feed on blood then deattaching and digesting on the benthos. Otherwise, they act as carnivorous scavengers.

Cirolanidae (480+ spp.) includes another famous-on-the-internet creature, the enormous Bathynomus giganteus, pictured above. Bathynomus lives in the deep sea, where it feeds on fish, cephalopods, crabs, and polychaetes. Other cirolanids are also scavengers or predators, most notably attacking trapped fish in nets (I doubt this is of any great economic importance).

Corallanidae (80+ spp.) are predominantly marine, coral reef inhabitants (cf. name), but some are also known from brackish and fresh waters. They attach themselves to turtles, fish, shrimp, and rays, but are predators, not parasites.

Bopyroidea

The Bopyridae (600+ spp.) are ectoparasites, similar to the various Cymothoidea, except they infect decapod crustaceans instead of fish. They attach to the branchial chamber, below the carapace. They can be very effectively used to demonstrate the drastic effects of parasitism on morphological evolution, with the miniaturisation effect extending all the way to the heart, which is reduced to nothing more than a tiny globular organ in the first pleonal segment (Dohrn, 1870). They also lack all lateral cardiac arteries (other isopods have 3-6 of them). It should be noted that similar reductions can also be seen in other parasitics (Cymothoidea also have a smaller heart size), but bopyrids are the most extreme.

The Dajidae (50+ spp.) also infect crustaceans, but have a wider scope than the bopyrids by infecting euphausiids and mysids in addition to shrimp. They also differ by attaching to the carapace, although some will also attach on gills. Examining the Dajidae and Bopyridae alone in the context I mentioned previously would make for a cool study, since they’re closely related and have similar hosts.

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References:

Ahyong ST, Lowry JK, Alonso M, Bamber RN, Boxshall GA, Castro P, Gerken S, Karaman GS, Goy JW, Jones DS, Meland K, Rogers DC & Svavarsson J. 2011. Subphylum Crustacea Brünnich, 1772. In: Zhang Z-Q (ed.) Animal biodiversity: An outline of higher-level classification and survey of taxonomic richness.

Brandt A & Poore GCB. 2003. Higher classification of the flabelliferan and related Isopoda based on a reappraisal of relationships. Invertebrate Systematics 17, 893-923.

Brusca RC. 1981. A monograph on the Isopoda Cymothoidae (Crustacea) of the eastern Pacific. Zoological Journal of the Linnean Society 73, 117-199.

Brusca RC & Gilligan MR. 1983. Tongue replacement in a marine fish (Lutjanus guttatus) by a parasitic isopod (Crustacea: Isopoda). Copeia 3, 813-816.

Bunkley-Williams L & Williams Jr EH. 1998a. Isopods associated with fishes: a synopsis and corrections. Journal of Parasitology 84, 893-896.

Bunkley-Williams L & Williams Jr EH. 1998b. Ability of Pederson Cleaner Shrimp to Remove Juveniles of the Parasitic Cymothoid Isopod, Anilocra haemuli, from the Host. Crustaceana 71, 862-869.

Cohen BF & Poore GCB. 1994. Phylogeny and biogeography of the Gnathiidae (Crustacea: Isopoda) with descriptions of new genera and species, most from south-eastern Australia. Memoirs of the Museum of Victoria 54, 271-397.

Dohrn A. 1870. Untersuchungen über Bau und Entwicklung der Arthropoden, 5. Zur Kenntniss des Baues von Paranthura costana. Zeitschrift für wissenschaftliche Zoologie 20, 81-93.

Grutter AS. 1999. Cleaner fish really do clean. Nature 398, 672-673.

Grutter AS, Lester RJG & Greenwood J. 2000. Emergence rates from the benthos of the parasitic juveniles of gnathiid isopods. Marine Ecology Progress Series 207, 123-127.

Lester RJG & Roubal FR. 1995. Phylum Arthropoda. In: Woo PTK (ed.). Fish Diseases and Disorders, Vol 1. Protozoan and metazoan infections.

Paperna I & Por FD. 1977. Preliminary data on the Gnathiidae (Isopoda) of the Northern Red Sea, the Bitter Lakes, and the Mediterranean and the biology of Gnathia piscivora n. sp. Rapports et Proces-Verbaux des Reunions – Commission Internationale pour l’Exploration Scientifique de la Mer Mediterranee 24, 195–197.

Raibaut A & Trilles JP. 1993. The Sexuality of Parasitic Crustaceans. Advances in Parasitology 32, 367-444.

Romestand MB. 1979. Étude écophysiologique des parasitoses à Cymothoadiens. Annales de Parasitologie 54, 423-448.

Smit NJ & Davies AJ. 2004. The Curious Life-Style of the Parasitic Stages of Gnathiid Isopods. Advances in Parasitology 58, 289-391.

Trilles JP. 1991. Present researches and perspective on Isopoda (Cymothoidae and Gnathiidae) parasites of fishes (systematics, faunistics, ecology, biology and physiology). Wiadomosci Parazytologiczne 37, 141-143.

Tsai M-L, Li J-J & Dai C-F. 1999. Why selection favors protandrous sex change for the parasitic isopod, Ichthyoxenus fushanensis (Isopoda: Cymothoidae). Evolutionary Ecology 13, 327-338.

Wägele JW. 1988. Aspects of the life-cycle of the Antarctic fish parasite Gnathia calva Vanhöffen (Crustacea: Isopoda). Polar Biology 8, 287-291.

Wägele JW. 1989. Evolution und phylogenetisches System der Isopoda: Stand der Forschung und neue Erkenntnisse. Zoologica 140, 1-262.

Williams Jr EH & Bunkley-Williams L. 1994. Four cases of unusual crustacean-fish associations and comments on parasitic processes. Journal of Aquatic Animal Health 6, 202-208.

Research Blogging necessities :)
N. J. Smit, & A. J. Davies (2004). The Curious Life-Style of the Parasitic Stages of Gnathiid Isopods Advances in Parasitology DOI: 10.1016/S0065-308X(04)58005-3
Lucy Bunkley-Williams, & Ernest H. Williams, Jr. (1998). Isopods Associated with Fishes: A Synopsis and Corrections The Journal of Parasitology DOI: 10.2307/3284615