Pomphorhynchus laevis
Pomphorhynchus laevis is an endo-parasitic acanthocephalan worm, with a very complex life cycle, that can modify the behavior of its intermediate host, the freshwater amphipod Gammarus pulex.[1] This species does not contain a digestive tract and relies on the nutrients provided by its host species leading to the accumulation of lead in P. laevis from the bile of the host species.[2]
Pomphorhynchus laevis | |
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Scientific classification | |
Kingdom: | Animalia |
Phylum: | Acanthocephala |
Class: | Palaeacanthocephala |
Order: | Echinorhynchida |
Family: | Pomphorhynchidae |
Genus: | Pomphorhynchus |
Species: | P. laevis |
Binomial name | |
Pomphorhynchus laevis Müller, 1776 | |
Life cycle
Pomphorhynchus laevis is a parasite with a complex life cycle, meaning that it needs multiple host species to complete it. The female releases eggs containing acanthor that are then ingested by an arthropod. The acanthor is then released from the egg and becomes acanthella which penetrate the host's gut wall and transforms into the infective cystacanth stage which presents as a cyst. The larval stages (cystacanths) reside in the hemocoel of, Gammarids, its intermediate host. Several fish species can serve as the definitive host, where P. laevis infect the intestine.[3] In the fish host, bile is an important resource for the growth of P. laevis.[4] The preferred final hosts of Pomphorhynchus laevis include the chub, Leuciscus cephalus and barbel, Barbus barbus when in freshwater and the minnow, Phoxinus phoxinus when in an isolated body of water.[5] Immature P. laevis are mainly found in the proximal part of the digestive tract while mature and developing P. laevis are found near the first intestinal loop with the posterior third loop of the digestive tract being uninhabitable.[5]
Lead accumulation
When chub (Leuciscus cephalus) infected with Pomphorhynchus laevis are exposed to different concentrations of lead, the parasite is able to reduce lead concentrations in the host. The normal mechanism of filtering lead for a freshwater fish includes the binding of the lead to steroids contained in the bile of the liver. The bile then travels down the bile duct into the small intestine where the lead is either absorbed or excreted. The parasite reduces the lead concentration in the bile of the chub once it has traveled to the small intestine by absorbing the metals contained in the bile. The lead being absorbed by P. laevis leaves less lead in the bile to be reabsorbed by the chub. This results in decreased levels of lead in the bile of the fish as well as in the fish organs.[6] P. laevis itself builds up high concentrations of lead (1000 times water concentration).[7]
Host manipulation
Pomphorhynchus laevis facilitates its movement between their hosts by altering the behavior and visual appearance of its gammarid hosts. Infected gammarids are manipulated to develop a preference for fish odours.[8] At the same time, the parasites itself develops a bright orange color making it more visible and consequently more likely to be consumed by a subsequent fish host.[9] This visual manipulation is effective specifically on host species that can serve as suitable hosts as fish species that are not suitable hosts are less attracted.[10]
Pomphorhynchus laevis also causes changes in the behavior of Gammarus pulex when responding to light. Normally, the species G. pulex show strong photophobic behavior, meaning they avoid light, which is advantageous to evade predation. When infected with P. laevis, G. pulex become strongly photophilic and seek out light which increases their chance of predation in turn increasing the likelihood of parasite transmission.[11] This alteration in behavior pertaining to light was found to involve an alteration in serotonergic activity of the brain. The immunoreactivity of the brain to serotonin was found to be increased by around 40 percent for infected G. pulex when compared to uninfected G. pulex.[11] It is also shown that G. pulex infected with the cystacanths, the infective larval stage of P. laevis, are less likely to show behaviors that would normally allow them to avoid predation such as using refuge less frequently, being less likely to cluster together when in the presence of danger, and frequently clinging to things floating in the water.[12] When G. pulex are infected by the non-infective life stage of P. laevis, there is an increased use of refuge which in turn decreases the risk of predation which is advantageous to the parasite due to them not being able to infect the next host when in this life stage.[11]
Biomimetics
This worm swells its proboscis to press microneedles into the intestinal wall, with a very strong adhesive force. This has inspired a structural skin graft adhesive that sticks strongly but has minimal tissue damage while in place and upon removal.[13]
References
- Bakker, Theo C.M.; Dominique Mazzi; Sarah Zala (June 1997). "Parasite Induced Changes in Behavior and Color Make Gammarus pulex More Prone to Fish Predation". Ecology. University of Bern, CH-3032 Hinterkappelen, Switzerland: Ecological Society of America. 78 (5): 1098–1104. doi:10.1890/0012-9658(1997)078[1098:PICIBA]2.0.CO;2. S2CID 85643670.CS1 maint: location (link)
- Sures, B.; Thielen, F.; Baska, F.; Messerschmidt, J.; von Bohlen, A. (2005). "The intestinal parasite Pomphorhynchus laevis as a sensitive accumulation indicator for the platinum group metals Pt, Pd, and Rh". Environmental Research. 98 (1): 83–88. doi:10.1016/j.envres.2004.05.010. ISSN 0013-9351. PMID 15721887.
- Thünken, Timo; Baldauf, Sebastian A.; Bersau, Nicole; Frommen, Joachim G.; Bakker, Theo C.M. (2019). "Parasite-induced colour alteration of intermediate hosts increases ingestion by suitable final host species". Behaviour. 156 (13–14): 1329–1348. doi:10.1163/1568539X-00003568.
- Sures, Bernd; Siddall, Roy (October 1999). "Pomphorhynchus laevis: The Intestinal Acanthocephalan as a Lead Sink for its Fish Host, Chub (Leuciscus cephalus)". Experimental Parasitology. 93 (2): 66–72. doi:10.1006/expr.1999.4437. PMID 10502468.
- Dudiňák, V.; Špakulová, M. (2003). "The life cycle and seasonal changes in the occurrence ofPomphorhynchus laevis(Palaeacanthocephala, Pomphorhynchidae) in a small isolated lake". Parasite. 10 (3): 257–262. doi:10.1051/parasite/2003103257. ISSN 1252-607X. PMID 14535165.
- Sures, B.; Thielen, F.; Baska, F.; Messerschmidt, J.; von Bohlen, A. (2005). "The intestinal parasite Pomphorhynchus laevis as a sensitive accumulation indicator for the platinum group metals Pt, Pd, and Rh". Environmental Research. 98 (1): 83–88. doi:10.1016/j.envres.2004.05.010. ISSN 0013-9351. PMID 15721887.
- Sures, Bernd; Siddall, Roy (October 1999). "Pomphorhynchus laevis: The Intestinal Acanthocephalan as a Lead Sink for its Fish Host, Chub (Leuciscus cephalus)". Experimental Parasitology. 93 (2): 66–72. doi:10.1006/expr.1999.4437. PMID 10502468.
- Baldauf, Sebastian A.; Timo Thünken; Joachim G Frommen; Theo C M Bakker; Oliver Heupel; Harald Kullmann (2007). "Infection with an acanthocephalan manipulates an amphipod's reaction to a fish predator's odours". International Journal for Parasitology. An der Immenburg 1, D-53121 Bonn, Germany: University of Bonn, Institute for Evolutionary Biology and Ecology. 37 (1): 61–5. doi:10.1016/j.ijpara.2006.09.003. PMID 17049528.CS1 maint: location (link)
- Bakker, Theo C.M.; Dominique Mazzi; Sarah Zala (June 1997). "Parasite Induced Changes in Behavior and Color Make Gammarus pulex More Prone to Fish Predation". Ecology. University of Bern, CH-3032 Hinterkappelen, Switzerland: Ecological Society of America. 78 (5): 1098–1104. doi:10.1890/0012-9658(1997)078[1098:PICIBA]2.0.CO;2. S2CID 85643670.CS1 maint: location (link)
- Thünken, Timo; Baldauf, Sebastian A.; Bersau, Nicole; Frommen, Joachim G.; Bakker, Theo C.M. (2019). "Parasite-induced colour alteration of intermediate hosts increases ingestion by suitable final host species". Behaviour. 156 (13–14): 1329–1348. doi:10.1163/1568539X-00003568.
- Tain, Luke; Perrot-Minnot, Marie-Jeanne; Cézilly, Frank (2006-12-19). "Differential influence of Pomphorhynchus laevis (Acanthocephala) on brain serotonergic activity in two congeneric host species". Biology Letters. 3 (1): 69–72. doi:10.1098/rsbl.2006.0583. ISSN 1744-9561. PMC 2373828. PMID 17443968.
- Dianne, Lucile; Perrot-Minnot, Marie-Jeanne; Bauer, Alexandre; Guvenatam, Arnaud; Rigaud, Thierry (2014). "Parasite-induced alteration of plastic response to predation threat: increased refuge use but lower food intake in Gammarus pulex infected with the acanothocephalan Pomphorhynchus laevis". International Journal for Parasitology. 44 (3–4): 211–216. doi:10.1016/j.ijpara.2013.11.001. ISSN 0020-7519. PMID 24291320.
- Seung Yun Yang; et al. (April 2013). "A bio-inspired swellable microneedle adhesive for mechanical interlocking with tissue". Nature Communications. Massachusetts (mixed): Macmillan. 4 (1702): 1702. Bibcode:2013NatCo...4.1702Y. doi:10.1038/ncomms2715. PMC 3660066. PMID 23591869.