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

Pearlfish: A LIttle Known Fish Family Gem, by Jordan WIlliams

Did you know that there are approximately 33,788 discovered species of fishes living on this planet as of 2016? It is actually really incredible when you stop and think about it. To put that number in perspective for you, that is over six times more species of fish than there are of mammals. Both mammals and fish fall under the phylum Chordata, which means every member of has at least a notochord and a hollow dorsal nerve cord, pharyngeal slits, an endostyle, and a post-anal tail for at least some period of their life cycles. But which came first? Fish of course! They were swimming around at least 300 million years before the first mammal even came into existence! Fish have had about 510 million years to fine tune their evolutionary adaptations for living in their aquatic environments. That isn’t to say that time is everything; just look at the 950,000 species of insects we can observe! And they are 200 million years younger than the fish (Ramel)! But as far as chordate evolution is concerned, fish have had the advantage of time over us mammals. Which finally brings me to my point: fishes have used all this extra evolutionary time to adapt and diversify in order to best suit their numerous aquatic environments. Fish showed up only 90 million years after the earliest animals, so they are some of the most well adapted and diversified animals on the planet.

Atlantic pearlfish  Carapus bermudensis   Source 

            But getting more to the point, fish are taxonomically separated into hundreds of families, 515 if you were curious. Taxonomy simply classifies animals into groupings that share common, “homogeneous,” traits. Pearlfish make up just one of these families, which makes them distinct from any other. The same can be said for the 514 other families, but I have a suspicion that you may find pearlfish just a little more distinct from the rest. Now without further ado, I hope to show you that the morphological and behavioral characteristics of the pearlfish family, Carapidae, makes its members fascinating and distinct from any other fishes.

            Morphologically, you would think that all fish share the same basic layout, but this is not the case. The minute you start trying to describe fish is the minute you’ll think of an exception to the characteristics you’ve just laid out! Just take a look at pearlfish for example. They are shaped like an eel and have no scales. Along with that, their anal and dorsal fins fuse together at an acute tip. Speaking of fins, the caudal and pelvic fins are completely absent in this family. They also have translucent bodies. Put all this together and we are a long way from what we first thought of when we heard the word ‘fish.’ But even with that description, there are still 36 accepted species of pearlfish swimming around. They are taxonomically grouped in three main genera: Echinodon, Carapus, and Encheliophis. The distinction between the three comes by how dependent they are to invertebrate hosts. Echinodon species are free-living. So to fend for themselves out in the tropical waters of the Pacific, Atlantic, and Indian oceans, they must be the biggest and strongest of the bunch.

Star Pearlfish, Carapus mourlani (Petit 1934)  Photo by John E. Randall. Source

            Alternatively, Carapus species tend to be a little smaller because they commensally hide inside their hosts during the day and come out to feed only at night. This leaves the parasitic Encheliophis genus left. Its members are usually the smallest based because it has no real reason to leave its host. Being a small parasite makes it more likely that the host will survive, in turn, raising your own odds of survival. (FAMILY Details for Carapidae – Pearlfishes).

But since taxonomists break the family up into these three main genera only by their level of dependency, there has been a lot of back and forth between which species belongs to which genus. For example, the Silver Pearlfish was thought to be of the parasitic family Encheliophis up until very recently when scientists discovered crustaceans in its stomach contents (Luna). This indicated that it had been out feeding at night, as Carapus species are known to do. However, it is still debated whether or not these fish obtain the majority of their nutrition from their hosts or from nocturnal feeding.

Regardless, we now understand what pearlfish look like and that they are fall into their genus based on dependency on hosts. But it’s time we combine the two and find out just what is really going on with these fish, behaviorally. Pearlfish hosts include holothurians, bivalves, and starfishes (Simon 2014). Most likely the name pearlfish came from when the species were first discovered as people were harvesting oysters or another kind bivalve. Pearlfish that do utilize hosts are quite clever about it. My favorite example of this is how they get into sea cucumbers (holothurians). First, pearlfish will sniff out which end they want to enter from… which happens to be the rear, as sea cucumbers breath through their anus while ingesting sediment on the ocean floor. If the sea cucumber continues to breathe normally, which is often not the case when they sense pearlfish are nearby, the pearlfish can just swim on into its body cavity. But if the sea cucumber puckers up, then the pearlfish truly shows us why it is such a fascinating fish. Remember how the dorsal and anal fin come to a point and how pearlfish lack scales? Good, because you’re about to find out why. The pearlfish will stab the tip of these fins into the sea cucumber’s anus and wait for it to start suffocating. When this happens, the sea cucumber will gasp for breath. But, this allows just enough time for the pearlfish to wriggle backwards into the orifice (Miyazaki 2014). From there, it can hide, eat, or even reproduce all while inside the coelom. Parasitic pearlfish eat this coelom and the gonads, as if the sea cucumber wasn’t violated enough already (Nielsen 1999). Click here, to  see a pearlfish swimming into a host.

            As you can see, Carapidae is a fascinating fish family because of their morphology and behavior. They are one of the most striking examples of fish adaptation and live in a strange and intriguing manner.

References

"FAMILY Details for Carapidae - Pearlfishes." FAMILY Details for Carapidae - Pearlfishes. Accessed April 4, 2016. http://www.fishbase.org/summary/FamilySummary.php?ID=187.

Luna, Susan M. "Encheliophis Homei Summary Page." FishBase. Accessed April 4, 2016. http://www.fishbase.org/summary/SpeciesSummary.php?ID=4832.

Miyazaki, S., T. Ichiba, J. D. Reimer, and J. Tanaka. 2014. Chemoattraction of the pearlfish Encheliophis vermicularis to the sea cucumber Holothuria leucospilota. Chemoecology 24(3):121–126.

Nielsen, J. G., D. M. Cohen, D. F. Markle, and C. R. Robins. 1999. Ophidiiform fishes of the world (order Ophidiiformes): an annotated and illustrated catalogue of pearlfishes, cusk-eels, brotulas and other ophidiiform fishes known to date. FAO Rome.

Ramel, Gordan. "The Evolution of Mammals." The Evolution of Mammals. Accessed April 4, 2016. http://www.earthlife.net/mammals/evolution.html.

Simon, Matt. "Absurd Creature of the Week: This Fish Swims Up a Sea Cucumber’s Butt and Eats Its Gonads." Wired.com. February 21, 2014. Accessed April 4, 2016. http://www.wired.com/2014/02/absurd-creature-of-the-week-pearlfish/.