Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-25T18:22:18.016Z Has data issue: false hasContentIssue false
  • English
  • Français

Crowding in the first intermediate host does not affect infection probability in the second host in two helminths

Published online by Cambridge University Press:  14 February 2018

D.P. Benesh
D.P. Benesh*
Affiliation:
Department of Evolutionary Ecology, Max-Planck-Institute for Evolutionary Biology, August-Thienemann-Strasse 2, DE-24306 Plön, Germany
*
Author for correspondence: D.P. Benesh, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

When many worms co-infect the same host, their average size is often reduced. This negative density-dependent growth is called the crowding effect. Crowding has been reported many times for worms in their intermediate hosts, but rarely have the fitness consequences of crowding been examined. This study tested whether larval crowding reduces establishment success in the next host for two parasites with complex life cycles, the nematode Camallanus lacustris and the cestode Schistocephalus solidus. Infected copepods, the first host, were fed to sticklebacks, the second host. Fish received a constant dose, but the infection intensity in copepods was varied (e.g. giving two singly infected copepods or one doubly infected copepod). Worms from higher-intensity infections did not have significantly reduced infection success in fish. However, crowded treatments had a disproportionate number of low and high infection rates, and although this trend was not significant, it hints at the possibility that multiple worms within a copepod are more likely to either all infect or all die when transmitted to the next host. These results indicate that a smaller larval size due to crowding need not reduce the establishment probability of a worm in the next host.

Type
Research Paper
Information
Journal of Helminthology , Volume 93 , Issue 2 , March 2019 , pp. 172 - 176
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

Current address: Humboldt University, Molecular Parasitology, Philippstr. 13, Haus 14, 10115 Berlin, Germany.

References

Benesh, DP (2011) Intensity-dependent host mortality: what can it tell us about larval growth strategies in complex life cycle helminths? Parasitology 138, 913–925.Google Scholar
Benesh, DP (2016) Autonomy and integration in complex parasite life cycles. Parasitology 143, 1824–1846.Google Scholar
Benesh, DP, Weinreich, F and Kalbe, M (2012) The relationship between larval size and fitness in the tapeworm Schistocephalus solidus: bigger is better? Oikos 121, 1391–1399.Google Scholar
Brown, SP, De Lorgeril, J, Joly, C and Thomas, F (2003) Field evidence for density-dependent effects in the trematode Microphallus papillorobustus in its manipulated host, Gammarus insensibilis. Journal of Parasitology 89, 668–672.Google Scholar
Caddigan, SC, Pfenning, AC and Sparkes, TC (2017) Competitive growth, energy allocation, and host modification in the acanthocephalan Acanthocephalus dirus: field data. Parasitology Research 116, 199–206.Google Scholar
Clarke, AS (1954) Studies on the life cycle of the pseudophyllidean cestode Schistocephalus solidus. Proceedings of the Zoological Society of London 124, 257–302.Google Scholar
Cornet, S (2011) Density-dependent effects on parasite growth and parasite-induced host immunodepression in the larval helminth Pomphorhynchus laevis. Parasitology 138, 257–265.Google Scholar
De Block, M and Stoks, R (2005) Fitness effects from egg to reproduction: bridging the life history transition. Ecology 86, 185–197.Google Scholar
Dörücü, M, Wilson, D and Barber, I (2007) Differences in adult egg output of Schistocephalus solidus from singly- and multiply-infected sticklebacks. Journal of Parasitology 93, 1518–1520.Google Scholar
Dubinina, MN (1980) Tapeworms (Cestoda, Ligulidae) of the fauna of the USSR. New Dehli, Amerind Publishing Company.Google Scholar
Dupont, F and Gabrion, C (1987) The concept of specificity in the procercoid–copepod system: Bothriocephalus claviceps (Cestoda) a parasite of the eel (Anguilla anguilla). Parasitology Research 73, 151–158.Google Scholar
Eizaguirre, C, Lenz, TL, Kalbe, M and Milinski, M (2012) Rapid and adaptive evolution of MHC genes under parasite selection in experimental vertebrate populations. Nature Communications 3, 621.Google Scholar
Fredensborg, BL and Poulin, R (2005) Larval helminths in intermediate hosts: does competition early in life determine the fitness of adult parasites? International Journal for Parasitology 35, 1061–1070.Google Scholar
Hafer, N and Benesh, DP (2015) Does resource availability affect host manipulation? – an experimental test with Schistocephalus solidus. Parasitology Open 1, e3.Google Scholar
Hafer, N and Milinski, M (2015) When parasites disagree: evidence for parasite-induced sabotage of host manipulation. Evolution 69, 611–620.Google Scholar
Hanzelova, V, Scholz, T, Gerdeaux, D and Kuchta, R (2002) A comparative study of Eubothrium salvelini and E. crassum (Cestoda: Pseudophyllidea) parasites of Arctic charr and brown trout in alpine lakes. Environmental Biology of Fishes 64, 245–256.Google Scholar
Heins, D, Baker, J and Martin, H (2002) The ‘crowding effect’ in the cestode Schistocephalus solidus: density-dependent effects on plerocercoid size and infectivity. Journal of Parasitology 88, 302–307.Google Scholar
Holmes, J (1961) Effects of concurrent infections on Hymenolepis diminuta (Cestoda) and Moniliformis dubius (Acanthocephala). I. General effects and comparison with crowding. Journal of Parasitology 47, 209–216.Google Scholar
Janovy, J and Kutish, G (1988) A model of encounters between host and parasite populations. Journal of Theoretical Biology 134, 391–401.Google Scholar
Janwan, P, Intapan, PM, Sanpool, O, Sadaow, L, Thanchomnang, T and Maleewong, W (2011) Growth and development of Gnathostoma spinigerum (Nematoda: Gnathostomatidae) larvae in Mesocyclops aspericornis (Cyclopoida: Cyclopidae). Parasites & Vectors 4, 93.Google Scholar
Keymer, A (1981) Population dynamics of Hymenolepis diminuta in the intermediate host. Journal of Animal Ecology 50, 941–950.Google Scholar
Kurtz, J, Kalbe, M, Aeschlimann, PB, Häberli, MA, Wegner, KM, Reusch, TBH and Milinski, M (2004) Major histocompatibility complex diversity influences parasite resistance and innate immunity in sticklebacks. Proceedings. Biological Sciences 271, 197–204.Google Scholar
Lotz, J, Bush, A and Font, W (1995) Recruitment-driven, spatially discontinuous communities: a null model for transferred patterns in target communities of intestinal helminths. Journal of Parasitology 81, 12–24.Google Scholar
Michaud, M, Milinski, M, Parker, GA and Chubb, JC (2006) Competitive growth strategies in intermediate hosts: experimental tests of a parasite life-history model using the cestode, Schistocephalus solidus. Evolutionary Ecology 20, 39–57.Google Scholar
Moravec, FS (1969) Observations on the development of Camallanus lacustris (Zoega, 1776). Věstník Československé Společnosti Zoologické 33, 15–33.Google Scholar
Parker, GA, Chubb, JC, Roberts, GN, Michaud, M and Milinski, M (2003) Optimal growth strategies of larval helminths in their intermediate hosts. Journal of Evolutionary Biology 16, 47–54.Google Scholar
Poulin, R (1994) The evolution of parasite manipulation of host behaviour: a theoretical analysis. Parasitology 109, S109–S118.Google Scholar
Poulin, R, Nichol, K and Latham, ADA (2003) Host sharing and host manipulation by larval helminths in shore crabs: cooperation or conflict? International Journal for Parasitology 33, 425–433.Google Scholar
Read, C (1951) The ‘crowding effect’ in tapeworm infections. Journal of Parasitology 37, 174–178.Google Scholar
Roberts, LS (1966). Developmental physiology of cestodes. I. Host dietary carbohydrate and the ‘crowding effect’ in Hymenolepis diminuta. Experimental Parasitology 18, 305–310.Google Scholar
Roberts, LS (2000). The crowding effect revisited. Journal of Parasitology 86, 209–211.Google Scholar
Rosen, R and Dick, TA (1983) Development and infectivity of the procercoid of Triaenophorus crassus Forel and mortality of the first intermediate host. Canadian Journal of Zoology 61, 2120–2128.Google Scholar
Rusinek, OT, Bakina, MP and Nikolskii, AV (1996) Natural infection of the calanoid crustacean Epischura baicalensis by procercoids of Proteocephalus sp. in Listvenichnyi Bay, Lake Baikal. Journal of Helminthology 70, 237–247.Google Scholar
Scharsack, JP, Koch, K and Hammerschmidt, K (2007) Who is in control of the stickleback immune system: interactions between Schistocephalus solidus and its specific vertebrate host. Proceedings of the Royal Society B 274, 3151–3158.Google Scholar
Shostak, AW, Walsh, JG and Wong, YC (2008) Manipulation of host food availability and use of multiple exposures to assess the crowding effect on Hymenolepis diminuta in Tribolium confusum. Parasitology 135, 1019–1033.Google Scholar
Smyth, J (1946) Studies on tapeworm physiology I. The cultivation of Schistocephalus solidus in vitro. Journal of Experimental Biology 23, 47–70.Google Scholar
Steinauer, ML and Nickol, BB (2003) Effect of cystacanth body size on adult success. Journal of Parasitology 89, 251–254.Google Scholar
Valkounova, J (1980) The most important factors affecting the larval development of cestodes of the family Hymenolepididae in crustaceans (Copepoda). Věstník Československé Spolecčnosti Zoologické 44, 230–240.Google Scholar
Vickery, WL and Poulin, R (2010) The evolution of host manipulation by parasites: a game theory analysis. Evolutionary Ecology 24, 773–788.Google Scholar
Wedekind, C (1997) The infectivity, growth, and virulence of the cestode Schistocephalus solidus in its first intermediate host, the copepod Macrocyclops albidus. Parasitology 115, 317–324.Google Scholar
Weinersmith, KL, Warinner, CB, Tan, V, Harris, DJ, Mora, AB, Kuris, AM, Lafferty, KD and Hechinger, RF (2014) A lack of crowding? Body size does not decrease with density for two behavior-manipulating parasites. Integrative and Comparative Biology 54, 184–192.Google Scholar
Weinreich, F, Benesh, DP and Milinski, M (2013) Suppression of predation on the intermediate host by two trophically-transmitted parasites when uninfective. Parasitology 140, 129–135.Google Scholar
Zander, CD, Groenewold, S and Strohbach, U (1994) Parasite transfer from crustacean to fish hosts in the Lübeck Bight, SW Baltic Sea. Helgoländer Meeresuntersuchungen 48, 89–105.Google Scholar