Haplorchis pumilio in Texas

In my previous post I discussed how the introduction of the invasive snail species Melanoides tuberculata led to the subsequent introduction of the trematode parasite Centrocestus formosanus into Texas Spring systems.  Well in that post, I sort of glossed over the part where an additional species of Heterophyid trematode had been inadvertently introduced as well, this one called Haplorchis pumilio.  It seems that while Haplorchis pumilio had been known to be present in Texas at least as long as C. formosanus, this particular trematode really never received the attention it deserved.  In a project that resulted in my second publication, I found out why no one had paid attention to H. pumilio and why we probably should.  Before I get started, let me throw out a little self promotion and provide you a link to the paper: 

Huston, D. C., Worsham, M. D., Huffman, D. G., & Ostrand, K. G. (2014). Infection of fishes, including threatened and endangered species by the trematode parasite Haplorchis pumilio (Looss, 1896)(Trematoda: Heterophyidae). BioInvasions Records, 3(3), 189-194. PDF

So, remember in my last post where I provided a diagram of the life-cycle for C. formosanus in Texas?  The life-cycle for H. pumilio is pretty much the same, with two important differences.  The first of these differences is the 1st intermediate host snail.  While C. formosanus only seems to exploit Melanoides tuberculata in Texas, Haplorchis pumilio is known to utilize both Melanoides tuberculata and a related snail (also invasive) Tarebia granifera (Tolley-Jordan and Owen, 2008).

The second difference is the anatomical location of where the metacercariae are encysted in the 2nd intermediate host.  While Centrocestus formosanus metacercariae are found in the gills of the fish host, Haplorchis pumilio metacercariae are found in the cartilage where the fins attach to the body (fin insertions).

Haplorchis pumilio metacercariae encysted in the caudal peduncle of a shiner, Cyprinella venusta.

The above photograph is the tail of a minnow which I made a sort of cut out in order to see the metacercariae encysted there.  See those little brownish orange ovals?  Those are Haplorchis pumilio metacercariae!  By my eyes I count around 20 of them.  They look like this under higher magnification:

Haplorchis pumilio metacercaria.

The fin insertions are a pretty unusual place to find parasites, and is not included in most general parasitology examinations, so its not surprising that these little cysts went unnoticed in Texas spring fishes for around 15 years.  I probably wouldn't have even noticed them myself if I wasn't in the habit of exposing random animals to trematode cercariae.  Truth be told, in this case I knew that Haplorchis pumilio metacercariae HAD to be present Texas fishes, or I wouldn't keep finding infections in the snails I was collecting.  However, no one had ever reported the metacercariae in North America, and not knowing what the metacercariae really looked like, besides the general descriptions and figures provided by Sommerville (1982a; b), I decided to expose some common minnows (Cyprinella venusta) to Haplorchis pumilio cercariae from infected Melanoides tuberculata.  It turned out it was pretty easy to figure out where the cercariae were encysting as metacercariae:

A Cyprinella venusta mortality due to a rapid accumulation of Haplorchis pumilio metacercariae.

So I guess I have to admit I exposed the fish to a little bit more cercariae than was probably necessary, but I definitely didn't expect this kind of result.  The day after exposure, the fish developed these massive blood blisters on the caudal peduncle, and by the third day the blisters had burst.  All of the minnows perished, presumably due to hemorrhage.  Their noble sacrifice allowed me to find all the anatomical locations where the Haplorchis pumilio metacercariae might encyst: all the fin insertions (caudal, pectoral, pelvic, anal, dorsal) as well as the cartilaginous portions of the head.  I also learned from doing little tiny fillets, that the cercariae penetrate the epidermis of the fish all over the body, and actually travel under the skin to these preferred locations before encysting.  Quite peculiar.  

I think that its extremely important for me to point out that the infection pressure experienced by the fish in these exposure experiments would be many many orders of magnitude higher than what any fish would experience in the wild.  It is highly unlikely that an individual fish would acquire more than a few metacercariae per day in a natural setting.  The real concern is compound effects of continuous metacercarial acquisition over a fish's lifetime, coupled with additional stressors.

From there the story and the resulting project were very straightforward.  My colleagues and I acquired a small sample of various fishes across Texas spring systems (including archived specimens that I had previously examined for C. formosanus, waste not!), and we examined them using what we had learned from the exposure experiments.

The results of our survey showed that not only was the largemouth bass (Micropterus salmoides) hosting H. pumilio metacercariae, but so were several species of conservation concern:

The Devils River minnow (Dionda diaboli) - IUCN red list status: endangered

The fountain darter (Etheostoma fonticola) - IUCN red list status: endangered

The Rio Grande darter (Etheostoma grahami) - IUCN red list status: vulnerable

The Pecos gambusia (Gambusia nobilis) - IUCN red list status: endangered

Devils River, Texas, USA. 2014. I'm still amazed that the invasive snail Melanoides tuberculata managed to get introduced somewhere as remote as the Devils River.  Some of us speculate that contaminated scientific equipment was the cause!

Now none of these fish were hosting metacercariae in densities anywhere near what I had seen in the artificial infections with Cyprinella venusta, as was expected.  So its pretty hard to make the argument that these trematodes are having serious deleterious effects on these fish.  However, I had previously worked on a project examining fish gills for Centrocestus formosanus metacercariae (McDermott et al. 2014) in the same spring systems.  I found that about 50% of all the fish from the Haplorchis pumilio study were also infected with Centrocestus formosanus.  So it seems that many Texas spring fish species are hosting two species of exotic trematodes, increasing the parasite pressure on these already threatened populations.

Our paper was the first report of H. pumilio infecting fishes in North America north of Mexico.  Centrocestus formosanus has been reported in several other states of the USA, and I reckon that where C. formosanus is found, H. pumilio will surely follow (if it isn't already there).  Furthermore, as time goes on, additional species of exotic trematode will make their way to Texas and the rest of North America.  Melanoides tuberculata is a known host for over 100 species of parasite (Pinto and Melo, 2011).  I found a fourth species of exotic exploiting M. tuberculata shortly before I left the USA for Australia.  As more and more species of exotic parasite arrive, they will put more and more pressure on the native fauna.  As drought occurs more often and becomes more severe, and as anthropogenic effects intensify, stressors experienced by these threatened and endangered fishes will begin to compound.

I'm afraid I don't have a solution to the problems we identified.  There are currently no viable control measures for M. tuberculata in the spring systems in which it has invaded, and those measures that have been suggested (and even attempted) border on the absurd.  However, the overwhelming problem facing all Texas spring species is reduced spring flow.  One of the major causes of this is excessive extraction of groundwater.  We need a paradigm shift in our mindsets.  We need to realize the value of wild places, especially our spring fed oases in the arid southwest.  We need to use less, think more, and to realize that having a green lawn in the middle of summer in the southwest is ridiculous and irresponsible.  Be proud of your dead grass.

REFERENCES

McDermott, K.S., T.L. Arsuffi, T.M. Brandt, D.C. Huston and K.G. Ostrand. 2014. Exotic digenetic trematode (Centrocestus formosanus) distribution and occurrence, its exotic snail intermediate host (Melanoides tuberculatus), and fish infection rates in West Texas Springs Systems. The Southwestern Naturalist, 59: 212-220.

Sommerville C (1982a) The life history of Haplorchis pumilio(Looss, 1896) from cultured tilapias. Journal of Fish Diseases 5: 233–241.

Sommerville C (1982b) The pathology of Haplorchis pumilio (Looss, 1896) infections in cultured tilapias. Journal of Fish Diseases 5: 243–250.

Pinto, H.A., and A.L. Melo. 2011. A checklist of trematodes (Platyhelminthes) transmitted by Melanoides tuberculata (Mollusca: Thiaridae). Zootaxa 2799: 15-28.

Tolley-Jordan, L.R., and J.M. Owen. 2008. Habitat influences snail community structure and trematode infection levels in a spring-fed river, Texas, USA. Hydrobiologia 600: 29-40.