Pomphorhynchus laevis

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Pomphorhynchus laevis
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Animalia
Phylum: Acanthocephala
Class: Palaeacanthocephala
Order: Echinorhynchida
Family: Pomphorhynchidae
Genus: Pomphorhynchus
Species:
P. laevis
Binomial name
Pomphorhynchus laevis
Müller, 1776

Pomphorhynchus laevis is an endo-parasitic acanthocephalan worm, with a complex life cycle, that can modify the behaviour of its intermediate host, the freshwater amphipod Gammarus pulex . [1] P. laevis does not contain a digestive tract and relies on the nutrients provided by its host species. In the fish host this can lead to the accumulation of lead in P. laevis by feeding on the bile of the host species. [2]

Contents

Life cycle and host species

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 its intermediate host, gammarids. From them it is trophically transmitted to fish. 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]

Host species

In the wild, P. laevis is known to infect a range of fish species from several families as definitive hosts. The preferred final hosts of P. laevis are the chub and barbel when in freshwater, and the minnow when in an isolated body of water. [5] Other definitive hosts include the gudgeon, roach, vairone, nase, rudd, common dace, loach, catfish, perch, bullhead, three-spined stickleback, [6] brown trout [7] and round goby. [8]

Location of infection

Infection in the fish host is in the posterior part of the middle intestine, more specifically behind the pyloric caeca. [7] 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]

Ecology

A positive association between fish biomass density and P. laevis abundance has been observed, suggesting the parasite populations increase in hosts with age, and that there is limited impact of intra-host density on parasite settlement. [6]

Environmental impacts on ecology

Heavy metals

P. laevis, like other acanthocephalan species, is able to reduce concentrations of metals (such as arsenic, cadmium, copper, lead, and zinc) in their definitive hosts by absorption through the host's bile. [1] [9] This reduces the metal concentrations in the bile of its host. [4] Consequently, P. laevis is a potential indicator of pollution. [9]

Temperature

The infection success of acanthors emerging from eggs to Gammarus pulex is not affected by temperature, but developmental rate is increased at warmer temperatures (14 versus 17 °C). [10] At the same temperatures parasite infection reduces survival of these hosts, but this is not compounded by temperature. [10]

Host manipulation

Intermediate host

Pomphorhynchus laevis facilitates its transmission from the intermediate to the definitive host by altering the behaviour and visual appearance of its gammarid intermediate hosts.

Manipulation of appearance

At the same time, the parasites itself develops a bright orange colour making it more visible and consequently more likely to be consumed by a fish host. [1] 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. [3]

Manipulation of behaviour

Infected gammarids are made to develop a preference for fish odours [11] and responses to light. [12]

Pomphorhynchus laevis can change the response of Gammarus pulex to light (phototaxis). Uninfected, healthy individuals of G. pulex show strong photophobic behaviour, meaning they avoid light. This helps to avoid predation. When infected with P. laevis, G. pulex become strongly photophilic and seek out light. The increases the chance of predation, in turn increasing the likelihood of parasite transmission. [12] [13] This alteration in behaviour in response 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 counterparts. [12]

It is also shown that G. pulex infected with the infective larval stage (cystacanths) of P. laevis, are less likely to show behaviours that would normally allow them to avoid predation. These behaviours include 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. [14] 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. [12]

Manipulation of feeding and metabolism

In the same host food presence does not appear to affect time and intensity of infection, while low food availability does negatively affect host growth. Possibly due to reduced metabolic rate of the host. [15]

Manipulation of immune response

After invading the host P. laevis needs to deal with their host's immune system. Levels of phenoloxidase and total immune activity were significantly reduced in infected G. pulex compared to controls. This led to a positive effect on bacterial growth in the host, which may a negative affect gammarid health and consequently infecting P. laevis. [13]

Definitive hosts

P. laevis excretes several neurochemical in the gut of the fish hosts, it thus appears likely that the parasites alters the physiological functioning of its host's alimentary tract . [7]

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. [16]

Related Research Articles

<span class="mw-page-title-main">Acanthocephala</span> Group of parasitic thorny-headed worms

Acanthocephala is a group of parasitic worms known as acanthocephalans, thorny-headed worms, or spiny-headed worms, characterized by the presence of an eversible proboscis, armed with spines, which it uses to pierce and hold the gut wall of its host. Acanthocephalans have complex life cycles, involving at least two hosts, which may include invertebrates, fish, amphibians, birds, and mammals. About 1,420 species have been described.

<i>Gammarus pulex</i> Species of crustacean

Gammarus pulex is a species of amphipod crustacean found in fresh water across much of Europe. It is a greyish animal, growing to 21 mm (0.83 in) long.

<i>Profilicollis</i> Genus of thorny-headed worms

Profilicollis is a genus of acanthocephalan parasites of crustaceans. The status of the genus Profilicollis has been debated, and species placed in this genus were formerly included in the genus Polymorphus. However, research on the morphology of the group and their use of hosts has concluded that Profilicollis and Polymorphus should be regarded as distinct genera, and species previously described as Polymorphus altmani are now referred to as Profilicollis altmani in taxonomic and biological literature. Profilicollis parasites infect decapod crustaceans, usually shore crabs, as intermediate hosts, and use many species of shorebirds as definitive (final) hosts.

Promoniliformis is a monotypic genus of acanthocephalans containing a single species, Promoniliformis ovocristatus, that infests tenrecs in Madagascar. The genus PromoniliformisDollfus and Golvan, 1963 is characterized by possessing two distinct kinds of proboscis hooks. There is only one species in this genus.

<span class="mw-page-title-main">Pomphorhynchidae</span> Family of thorny-headed worms

Pomphorhynchidae is a family of parasitic worms from the order Echinorhynchida.

<i>Moniliformis moniliformis</i> Species of thorny-headed worm

Moniliformis moniliformis is a parasite of the Acanthocephala phylum in the family Moniliformidae. The adult worms are usually found in intestines of rodents or carnivores such as cats and dogs. The species can also infest humans, though this is rare.

<i>Gammarus lacustris</i> Species of crustacean

Gammarus lacustris is an aquatic amphipod.

Acanthocephaloides is a genus of parasitic worms belonging to the family Arhythmacanthidae.

Euzetacanthus is a genus in Acanthocephala.

Spiracanthus is a monotypic genus of acanthocephalans containing a single species, Spiracanthus bovichthys, that infests animals.

Eocollis is a genus in Acanthocephala.

Cavisoma is a monotypic genus of acanthocephalans containing a single species, Cavisoma magnum, that infests animals.

Filisoma is a genus in Acanthocephala.

Neorhadinorhynchus is a genus in Acanthocephala.

Brentisentis is a genus in Acanthocephala.

Nephridiacanthus is a genus of parasitic worms belonging to the family Oligacanthorhynchidae.

Microsentis is a monotypic genus of worms belonging to the family Neoechinorhynchidae.

Hexaspiron is a genus in Acanthocephala belonging to the family Neoechinorhynchidae.

Gorytocephalus is a genus in Acanthocephala belonging to the family Neoechinorhynchidae.

Octospiniferoides is a genus in Acanthocephala belonging to the family Neoechinorhynchidae.

References

  1. 1 2 3 Bakker, Theo C. M.; Mazzi, Dominique; Zala, Sarah (1997). "Parasite-induced changes in behavior and color make Gammarus pulex more prone to fish predation". Ecology. 78 (4): 1098–1104. Bibcode:1997Ecol...78.1098B. doi:10.2307/2265861. JSTOR   2265861.
  2. ↑ 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. Bibcode:2005ER.....98...83S. doi:10.1016/j.envres.2004.05.010. PMID   15721887.
  3. 1 2 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 .
  4. 1 2 Sures, Bernd; Siddall, Roy (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.
  5. 1 2 Dudiňák, V.; Špakulová, M. (2003). "The life cycle and seasonal changes in the occurrence of Pomphorhynchus laevis (Palaeacanthocephala, Pomphorhynchidae) in a small isolated lake". Parasite. 10 (3): 257–262. doi: 10.1051/parasite/2003103257 . PMID   14535165.
  6. 1 2 Perrot-Minnot, M.-J.; Bollache, L.; Lagrue, C. (2020). "Distribution of Pomphorhynchus laevis s.l. (Acanthocephala) among fish species at a local scale: importance of fish biomass density". Journal of Helminthology. 94: e99. doi:10.1017/S0022149X1900097X. PMID   31685047. S2CID   207897566.
  7. 1 2 3 Dezfuli, B S; Pironi, F; Giari, L; Domeneghini, C; Bosi, G (2002). "Effect of Pomphorhynchus laevis (Acanthocephala) on putative neuromodulators in the intestine of naturally infected Salmo trutta". Diseases of Aquatic Organisms. 51 (1): 27–35. doi: 10.3354/dao051027 . PMID   12240968.
  8. ↑ Zaharieva, R. G.; Zaharieva, P. G.; Kirin, D. A. (2023). "Ecological study on helminths of three species of Gobiidae from the Danube River, Bulgaria". Helminthologia . 60 (1): 63–72. doi:10.2478/helm-2023-0008. PMC   10251753 . PMID   37305671.
  9. 1 2 Nachev, Milen; Sures, Bernd (2016). "Seasonal profile of metal accumulation in the acanthocephalan Pomphorhynchus laevis: a valuable tool to study infection dynamics and implications for metal monitoring". Parasites & Vectors. 9 (1): 300. doi: 10.1186/s13071-016-1576-4 . PMC   4878057 . PMID   27216617.
  10. 1 2 Labaude, Sophie; Cézilly, Frank; De Marco, Lila; Rigaud, Thierry (2020). "Increased temperature has no consequence for behavioral manipulation despite effects on both partners in the interaction between a crustacean host and a manipulative parasite". Scientific Reports. 10 (1): 11670. doi: 10.1038/s41598-020-68577-z . PMC   7363812 . PMID   32669670.
  11. ↑ Baldauf, Sebastian A.; Thünken, Timo; Frommen, Joachim G.; Bakker, Theo C.M.; Heupel, Oliver; Kullmann, Harald (2007). "Infection with an acanthocephalan manipulates an amphipod's reaction to a fish predator's odours". International Journal for Parasitology. 37 (1): 61–65. doi:10.1016/j.ijpara.2006.09.003. PMID   17049528.
  12. 1 2 3 4 Tain, Luke; Perrot-Minnot, Marie-Jeanne; Cézilly, Frank (2007). "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. PMC   2373828 . PMID   17443968.
  13. 1 2 Cornet, Stéphane; Franceschi, Nathalie; Bauer, Alexandre; Rigaud, Thierry; Moret, Yannick (2009). "Immune depression induced by acanthocephalan parasites in their intermediate crustacean host: Consequences for the risk of super-infection and links with host behavioural manipulation". International Journal for Parasitology. 39 (2): 221–229. doi:10.1016/j.ijpara.2008.06.007. PMID   18708062.
  14. ↑ 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" (PDF). International Journal for Parasitology. 44 (3–4): 211–216. doi:10.1016/j.ijpara.2013.11.001. PMID   24291320.
  15. ↑ Labaude, Sophie; Cézilly, Frank; Tercier, Xavier; Rigaud, Thierry (2015). "Influence of host nutritional condition on post-infection traits in the association between the manipulative acanthocephalan Pomphorhynchus laevis and the amphipod Gammarus pulex". Parasites & Vectors. 8 (1): 403. doi: 10.1186/s13071-015-1017-9 . PMC   4520090 . PMID   26223476.
  16. ↑ Yang, Seung Yun; O'Cearbhaill, Eoin D.; Sisk, Geoffroy C; Park, Kyeng Min; Cho, Woo Kyung; Villiger, Martin; Bouma, Brett E.; Pomahac, Bohdan; Karp, Jeffrey M. (2013). "A bio-inspired swellable microneedle adhesive for mechanical interlocking with tissue". Nature Communications. 4 (1): 1702. Bibcode:2013NatCo...4.1702Y. doi: 10.1038/ncomms2715 . PMC   3660066 . PMID   23591869.
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