Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-19T07:58:47.545Z Has data issue: false hasContentIssue false

Distribution of Pomphorhynchus laevis s.l. (Acanthocephala) among fish species at a local scale: importance of fish biomass density

Published online by Cambridge University Press:  05 November 2019

M.-J. Perrot-Minnot*
Affiliation:
Biogéosciences, UMR 6282 CNRS, Université Bourgogne Franche-Comté, 6 Boulevard Gabriel, 21000 Dijon, France
L. Bollache
Affiliation:
Laboratoire Chrono-environnement, UMR 6249 CNRS, Université Bourgogne Franche-Comté, 16 Route de Gray, 25000 Besançon, France
C. Lagrue
Affiliation:
Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada
*
Author for correspondence: M.-J. Perrot-Minnot, E-mail: [email protected]

Abstract

Parasite distribution among hosts is a fundamental aspect of host–parasite interactions. Aggregated parasite distributions within and across host species are commonly reported and potentially influenced by many factors, whether host or parasite specific, or related to host–parasite encounter and compatibility. Yet, the respective role of each in observed parasite distributions are often unclear. Here, we documented the distribution of the acanthocephalan parasite Pomphorhynchus laevis sensu lato (s.l.) in two replicate fish host populations. Aggregated distributions were observed in both populations, within and across fish host species. We found a positive abundance–prevalence relationship across fish species, suggesting that resource availability (fish host biomass density) was the main driver of P. laevis s.l. distribution. This was supported by further positive associations between mean parasite load and fish biomass density. We found little evidence for intensity-dependent regulation within host (i.e. intra-host competition among co-infecting parasites). Furthermore, P. laevis s.l. infection had no detectable effect on fish condition indices, except on the body condition of female barbel (Barbus barbus). Therefore, P. laevis s.l. tended to accumulate with size/age within fish species, and with fish biomass density among fish species, with apparently negligible limitations due to intra-host intensity-dependent regulation of parasite, or to parasite-induced morbidity in fish. The relative availability of final hosts for trophic transmission thus appears to be the main driver of P. laevis s.l. distribution among fish.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2019 

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

Both authors contributed equally to this work.

References

Amin, OM, Abdullah, SMA and Mhaisen, FT (2003) Description of Pomphorhynchus spindletruncatus n. sp (Acanthocephala : Pomphorhynchidae) from freshwater fishes in northern Iraq, with the erection of a new pomphorhynchid genus, Pyriproboscis n. g., and keys to genera of the Pomphorhynchidae and the species of Pomphorhynchus Monticelli, 1905. Systematic Parasitology 54, 229235.Google Scholar
Anderson, RM and Gordon, DM (1982) Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortalities. Parasitology 85, 373398.Google Scholar
Arneberg, P (2001) An ecological law and its macroecological consequences as revealed by studies of relationships between host densities and parasite prevalence. Ecography 24, 352358.Google Scholar
Arneberg, P, Skorping, A, Grenfell, B and Read, AF (1998) Host densities as determinants of abundance in parasite communities. Proceedings of the Royal Society B: Biological Sciences 265, 12831289.Google Scholar
Barton, K (2018) MuMIn: multi-model inference. R package version 1.42.1.Google Scholar
Bates, D, Maechler, M, Bolker, B and Walker, S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 148.Google Scholar
Buck, JC and Lutterschmidt, WI (2017) Parasite abundance decreases with host density: evidence of the encounter-dilution effect for a parasite with a complex life cycle. Hydrobiologia 784, 201210.Google Scholar
Bush, AO, Lootvoet, KD, Lotz, JM and Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575583.Google Scholar
Canty, A and Ripley, B (2019).boot: Bootstrap R (S-Plus) functions. R package version 1.3-23.Google Scholar
Chellappa, S, Huntingford, FA, Strang, RHC and Thomson, RY (1995) Condition factor and hepatosomatic index as estimates of energy status in male 3-spined stickleback. Journal of Fish Biology 47, 775787.Google Scholar
Crompton, DWT and Nickol, BB (1985) Biology of acanthocephala. 1st edn. 519 pp. Cambridge, Cambridge University Press.Google Scholar
Dinno, A (2015) Dunn.test: Dunn's test of multiple comparisons using rank sums. R package version 1.3.1.Google Scholar
Dobson, AP and Keymer, AE (1985) Life history models. pp. 347384 in Crompton, DWT and Nickol, BB (Eds) The Biology of the Acanthocephala. Cambridge, UK, Cambridge Universitv Press.Google Scholar
Dragun, Z, Filipović Marijić, V, Kapetanović, D, et al. (2013) Assessment of general condition of fish inhabiting a moderately contaminated aquatic environment. Environmental Science and Pollution Research 20, 49544968.Google Scholar
Dudiňák, V and Špakulová, M (2003) The life cycle and seasonal changes in the occurrence of Pomphorhynchus laevis (Palaeacanthocephala, Pomphorhynchidae) in a small isolated lake. Parasite 10, 257262.Google Scholar
Gaston, KJ, Blackburn, T, Greenwood, JJD, Gregory, RD, Quinn, RM and Lawton, JH (2000) Abundance-occupancy relationships. Journal of Applied Ecology 37, 3959.Google Scholar
Gourbière, S, Morand, S and Waxman, D (2015) Fundamental factors determining the nature of parasite aggregation in hosts. PLoS ONE 10(2), e0116893.Google Scholar
Hussey, NE, Cocks, DT, Dudley, SFJ, McCarthy, ID and Wintner, SP (2009) The condition conundrum: application of multiple condition indices to the dusky shark Carcharhinus obscurus. Marine Ecology Progress Series 380, 199212.Google Scholar
Jenkins, T and Owens, IP (2011) Biogeography of avian blood parasites (Leucocytozoon spp.) in two resident hosts across Europe: phylogeographic structuring or the abundance–occupancy relationship? Molecular Ecology 20, 39103920.Google Scholar
Johnson, PTJ and Hoverman, JT (2014) Heterogeneous hosts: how variation in host size, behaviour and immunity affects parasite aggregation. Journal of Animal Ecology 83, 11031112.Google Scholar
Johnson, PTJ and Wilber, MQ (2017) Biological and statistical processes jointly drive population aggregation: using host-parasite interactions to understand Taylor's power law. Proceedings of the Royal Society B: Biological Sciences 284, 20171388.Google Scholar
Kalogianni, E, Kmentová, N, Harris, E, Zimmerman, B, Giakoumi, S, Chatzinikolaou, Y and Vanhove, MPM (2017) Occurrence and effect of trematode metacercariae in two endangered killifishes from Greece. Parasitology Research 116, 30073018.Google Scholar
Kennedy, CR (2006) Ecology of the acanthocephala. 1st edn. 260 pp. Cambridge, Cambridge University Press.Google Scholar
Kilpatrick, AM and Ives, AR (2003) Species interactions can explain Taylor's power law for ecological time series. Nature 422, 6568.Google Scholar
Lester, RJG (1984) A review of methods for estimating mortality due to parasites in wild fish populations. Helgoländer Meeresunters 37, 5364.Google Scholar
Lester, RJG and McVinish, R (2016) Does moving up a food chain increase aggregation in parasites? Journal of The Royal Society Interface 13, 20160102.Google Scholar
Masson, G, Vanacker, M, Fox, MG and Beisel, JN (2015) Impact of the cestode Triaenophorus nodulosus on the exotic Lepomis gibbosus and the autochthonous Perca fluviatilis. Parasitology 142, 745755.Google Scholar
Médoc, V, Rigaud, T, Motreuil, S, Perrot-Minnot, M-J and Bollache, L (2011) Paratenic hosts as regular transmission route in the acanthocephalan Pomphorhynchus laevis: potential implications for food webs. Naturwissenschaften 98, 825835.Google Scholar
Morand, S and Krasnov, B (2008) Why apply ecological laws to epidemiology? Trends in Parasitology 24, 304309.Google Scholar
Nagrodski, A, Suski, CD and Cooke, SJ (2013), Health, condition, and survival of creek chub (Semotilus atromaculatus) across a gradient of stream habitat quality following an experimental cortisol challenge. Hydrobiologia 702, 283–296.Google Scholar
Pérez-del-Olmo, A, Morand, S, Raga, JA and Kostadinova, A (2011) Abundance–variance and abundance–occupancy relationships in a marine host–parasite system: the importance of taxonomy and ecology of transmission. International Journal for Parasitology 41, 13611370.Google Scholar
Perrot-Minnot, M-J, Špakulová, M, Wattier, R, Kotlík, P, Düşen, S, Aydoğdu, A and Tougard, C (2018) Contrasting phylogeography of two Western Palaearctic fish parasites despite similar life cycles. Journal of Biogeography 45, 101115.Google Scholar
Perrot-Minnot, MJ, Guyonnet, E, Bollache, L and Lagrue, C (2019) Differential patterns of definitive host use by two fish acanthocephalans occurring in sympatry: Pomphorhynchus laevis and Pomphorhynchus tereticollis. International Journal for Parasitology: Parasites and Wildlife 8, 135144.Google Scholar
Poulin, R (2007a) Evolutionary ecology of parasites. 2nd edn. 332 pp. Princeton, Princeton University Press.Google Scholar
Poulin, R (2007b) Are there general laws in parasite ecology? Parasitology 134, 763776.Google Scholar
Poulin, R (2013) Explaining variability in parasite aggregation levels among host samples. Parasitology 140, 541546.Google Scholar
Poulin, R, Krasnov, BR and Mouillot, D (2011) Host specificity in phylogenetic and geographic space. Trends in Parasitology 27, 355361.Google Scholar
R Core Team (2018) R: A language and environment for statistical computing. 2.15.0 edn. Vienna, Austria, R Foundation for Statistical Computing. Available at https://www.R-project.org/.computing.Google Scholar
Rodríguez, SM and Valdivia, N (2017) Mesoscale spatiotemporal variability in a complex host-parasite system influenced by intermediate host body size. Peer Journal 5, e3675.Google Scholar
Scherer, R (2018) PropCIs: various confidence interval methods for proportions. R package version 0.3-0.Google Scholar
Shaw, DJ and Dobson, AP (1995) Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111, S111S133.Google Scholar
Špakulová, M, Perrot-Minnot, M-J and Neuhaus, B (2011) Resurrection of Pomphorhynchus tereticollis (Rudolphi, 1809) (Acanthocephala: Pomphorhynchidae) based on new morphological and molecular data. Helminthologia 48, 268277.Google Scholar
Tierney, JF, Huntingford, FA and Crompton, DWT (1996) Body condition and reproductive status in sticklebacks exposed to a single wave of Schistocephalus solidus infection. Journal of Fish Biology 49, 483493.Google Scholar
Vardić Smrzlić, I, Valić, D, Kapetanović, D, Filipović Marijić, V, Gjurčević, E and Teskeredžić, E (2015) Pomphorhynchus laevis (Acanthocephala) from the Sava River basin: new insights into strain formation, mtDNA-like sequences and dynamics of infection. Parasitology Intrnational 64, 243250.Google Scholar
Venables, WN and Ripley, BD (2002) Modern applied statistics with S. 4th edn. New York, Springer.Google Scholar
Wilson, K, Bjørnstad, ON, Dobson, AP, Merler, S, Poglayen, G, Randolph, S, Read, AF and Skorping, A (2002) Heterogeneities in macroparasite infections: patterns and processes. pp. 644 in Hudson, PJ, Rizzoli, A, Grenfell, BT, Heesterbeek, H and Dobson, AP (Eds) The ecology of wildlife diseases. Oxford, UK, Oxford University Press.Google Scholar
Zeileis, A and Hothorn, T (2002) Diagnostic checking in regression relationships. R News 2, 712.Google Scholar
Supplementary material: File

Perrot-Minnot et al. supplementary material

Perrot-Minnot et al. supplementary material

Download Perrot-Minnot et al. supplementary material(File)
File 302.4 KB