Exploring Pearlfishes (Carapidae) and the Pinhead Pearlfish Encheliophis boraborensis, by Jireh Clarington

 Considering the vast diversity of chordates, it may seem odd that few of them are parasitic. Particularly among fishes there are some parasitic groups, cookie cutter sharks and lampreys being the most common, but there is another group of fishes that is not as well understood: the pearlfishes. Although not all members of this family are parasitic. Commensalism is represented in this family as well.  Commensalism refers to a type of symbiotic relationships in which the individual interacts with and relies on its host for survival while the host is negligibly affected by said interaction. Pearlfish are a group of ophidiiforms in the family Carapidae with eight currently recognized genera and thirty-six species who represent each of these strategies. A pearlfish’s host often depends on the species of the fish. Some can be found parasitizing bivalves or living commensally inside tunicates others live in echinoderms like sea stars and sea cucumbers. The phylogeny of the Carapidae is still under debate as its genetic relatedness with other members of ifs genus and family are still being contested. We will be exploring the Carapidae family through the lens of one particular species: Encheliophis boraborensis formerly called Carapus boraborensis whose adult form is spent commensally inside sea cucumbers.

 

Illustration of the Pinhead Pearlfish Encheliophis boraborensis.   Source.

It may be necessary to provide a brief note on sea cucumber anatomy: sea cucumbers have a mouth on the anterior end and an anus on the posterior near the posterior is a pair of organs called a respiratory tree, these sticky organs are ejected by the cucumber when threatened and are able to produce toxins, however many pearlfish show increased resistance to these toxins compared to other reef dwelling fish. This allows the pearlfish to be protected by the cucumber without being poisoned by it. Additionally, the anal cavity is near the gonads, in the case of parasitic pearlfish these are the tissues most commonly found in pearlfish’s stomachs suggesting that parasitic pearlfish tend to eat the gonads of their host while still being able to exploit the cucumber for protection as its respiratory tree is left intact as the cucumber is able to remain healthy but the individuals fecundity could be severely reduced depending on the time needed until the gonads regrow (Parmentier and Vandewalle 2004).

Pearlfish are mainly found in the Pacific Ocean, specifically the tropics on reef habitats where their hosts can be most commonly found. The pinhead pearlfish, Encheliophis boraborensis, can be found near French Polynesia living in the cloacal vent of any number of local sea cucumber species and in some cases many pearlfish can be found in a single host (Parmentier and Vanderwalle 2004). Pearlfish such as the pinhead pearlfish rely on their sleek elongated body shapes to enter their hosts tail first to enter their host cucumbers. However, with species who inhabit hosts, such as tunicates or oysters, the orientation is less significant.

Click here to watch video of a pearlfish.  

Pinhead Pearlfish with leopard sea cucumber Bohadschia argus.  Source:  Project Noah.

When building a phylogeny, it is useful to use morphological traits as well as molecular analysis to form plausible hypotheses. Much can be said about a pearlfish’s life history based on morphology alone as, upon analysis, certain patterns arise that help distinguish the separate life strategies the fish employs. For example, jaw structure and size in the parasitic fishes tends to be weaker in comparison with commensal species. This weakening of their feeding apparatus can be attributed to the commensal species need to leave its host in order to hunt the small crustaceans on which it feeds as opposed to the pearlfish species who do not need to leave their host and are able to feed exclusively on their hosts soft tissues. Another useful morphological trait is the presence of sound generating structures connected to the pearlfish’s swim bladder (mainly used for communication with conspecifics) vary greatly (Lagardère et. al. 2005). The diversity of these mechanisms is emblematic of the speciation within the Carapidae family but offered very little in the way of clues to establish any evolutionary relationships within the taxa (Parmentier et.al. 2016). However, as previously mentioned a host may be inhabited by multiple individuals, but these may not necessarily all be members of the same species in a laboratory study by Garilao, interspecies competition was observed. Thus, it can be extrapolated that the variation in calls and sound generating structures unique to each species help distinguish one species from another and play a role in competition for a host.

To explain the relationship between parasitic and commensal pearlfish one must also consider their life history. Pearlfish larvae have two stages before reaching their final adult forms, these stages are the vexilifer larvae which are free swimming meroplankton until they reach the tenuis stage in which their bodies shorten in length and they begin to search for a host. It is believed that the parasitic species are derived from the commensal pearlfish as the result of pedomorphosis within the parasites. Pedomorphosis occurs when the adult form of a species retains traits from its juvenile forms in the case of the pearlfish this is reminiscent of the relationship between free living and parasitic lampreys where, once again, only the adult form becomes parasitic.

In conclusion, members of the family Carapidae are a diverse group of animals whose evolutionary strategy have led them to employ a fascinating range of survival tactics to live on tropical reefs. Some like Encheliophis boraborensis exhibit morphological and developmental differences that make it better suited for a commensal life with its host. While other members in different genera of the family are may have started commensal but have evolved to become parasitic rarely needing to leave their hosts body cavity. There is still more to be learned about the ecology of these fishes as little is known about their mating habits and the extent of damage their parasitism has on their hosts.
 

References

Froese, R. and D. Pauly. Editors. 2019. FishBase. Encheliophis boraborensis summary page.  World Wide Web electronic publication.   [accessed 2019 May 1]. http://www.fishbase.org/summary/Encheliophis-boraborensis.html.

Lagardère JP, Millot S, Parmentier E. 2005. Aspects of sound communication in the pearlfish Carapus boraborensis and Carapus homei (Carapidae). Journal of Experimental Zoology Part A: Comparative Experimental Biology. 303A(12):1066–1074.

Parmentier E, Castillo G, Chardon M, Vandewalle P. 2001. Phylogenetic analysis of the pearlfish tribe Carapini (Pisces: Carapidae). Acta Zoologica 81(4):293–306.  doi:10.1046/j.1463-6395.2000.00059.x

Parmentier E, Vandewalle P.  2004. Further insight on carapid —holothuroid relationships. Marine Biology 146(3):455–465.   doi:10.1007/s00227-004-1467-7

Parmentier E, Das K. 2004.  Commensal vs. parasitic relationship between Carapini fish and their hosts: some further insight through δ13C and δ15N measurements. Journal of Experimental Marine Biology and Ecology. 310(1):47–58. doi:10.1016/j.jembe.2004.03.019