Pomphorhynchus laevis (Zoega in Muller, 1776)

Perrot-Minnot, Marie-Jeanne, Guyonnet, Emilie, Bollache, Loïc & Lagrue, Clément, 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, pp. 135-144 : 138-139

3.1. Host range and specificity of P. laevis and P. tereticollis

All parasites sampled in the Ouche locality and almost all parasites from the Vingeanne locality were successfully assigned to one of the two Pomphorhynchus species (with only one individual fish out of 10 having less than 80% of its parasites assigned to either species in the Vingeanne locality). Identification effort per individual fish was representative of parasite intensity, as confirmed by a significant correlation between the number of parasites identified and Pomphorhynchus intensity (spearman rank correlation test, S=67546, P <0.0001, Rho=0.89). We also genotyped 95 extra-intestinal Pomphorhynchus from 33 individual fish from 4 species in the River Ouche, and from 3 catfish individuals in the River Vingeanne, out of the 475 extra-intestinal parasites recorded (20%).

Across all fish species, P. laevis represented 71.3% and 37.8% of all intestinal acanthocephalan parasites genotyped from the Ouche (N=342) and Vingeanne River (N=473), respectively. A higher proportion of P. laevis than P. tereticollis was found as extra-intestinal parasites, reaching 97% and 48% of extra-intestinal individuals in fish from Ouche and Vingeanne localities, respectively. Extra-intestinal parasites from gudgeon, minnow and stickleback were nearly all P. laevis , while catfish harboured both P. laevis and P. tereticollis as extra-intestinal cystacanths ( Fig. 1 ).

To test whether the relative proportion of each parasite species in fish hosts differs from the proportion found in intermediate hosts, we first estimated the proportion of P. laevis and P. tereticollis in pooled samples of gammarids collected in October 2004, February 2005 and May 2005. Overall, 195 out of 7290 gammarids from the river Vingeanne (2.67%) and 145 out of 5737 from the river Ouche (2.5%) were infected with Pomphorhynchus cystacanths. The relative number of gammarids infected with P. tereticollis and P. laevis was different between the two localities (Fisher exact test, Chi 2 =105.85, df=1, P <0.0001). Prevalence of P. laevis in gammarid hosts was higher than that of P. tereticollis in the Ouche locality (1.67% and 0.85%, respectively), while the reverse was found in the Vingeanne locality (0.32%, df=1, Chi 2 =85, P <0.0001, ecological type nested within population, df=2, Chi 2 =398.5, P <0.0001). More specifically, P. laevis was relatively more abundant in bentho-pelagic fish, in particular chub in both localities, and vairone and minnow in the river Ouche..Conversely, P. tereticollis was relatively more abundant in benthic fish (bottom-feeders) in both localities, in particular barbel in both localities (and loach in the river Ouche; Fig. 1 ). The mean abundance of P. laevis in each host species increased significantly with local fish biomass (Rsq.adj.=0.41, F 1,11 =9.1, P = 0.012; Fig. 2 ). This trend was not significant for P. tereticollis (Rsq.adj.=0.07, F 1,9 =1.36, P = 0.21), with bentho-pelagic fish from the Ouche River harbouring low abundance of P. tereticollis relative to their local biomass (particularly chub and minnow; Fig. 2 ).

Host range structural diversity (Shannon-Wiener index H’) was higher, and taxonomic diversity (phylo-structural index STD*) and specialization (link strength on resource: PDI) lower, for P. laevis compared to P. tereticollis in the Ouche locality, while the reverse was found in the Vingeanne locality ( Table 1). The higher strength of link on resource (PDI) in Vingeanne locality compared to Ouche locality was associated with a lower structural diversity (Shannon index), independently of parasite species. Interestingly, the prevalence in intermediate hosts increased with increasing taxonomic specificity towards fish hosts (lower phylo-structural index STD*), irrespective of locality and Pomphorhynchus species ( Table 1; Fig. 4 ). Weak negative or positive associations between prevalence in intermediate host and resource specialization or structural diversity, respectively, were also observed ( Table 1). The level of niche overlap between P. laevis and P. tereticollis was low to intermediate in both localities ( Table 1), and lower in the Vingeanne than Ouche locality.

Combining parasite abundance to the local density of each fish species revealed that 80% (Ouche locality) to 90% (Vingeanne locality) of intestinal P. laevis and P. tereticollis were cycling through only one to three host species ( Fig. 3a and b ). As illustrated by their respective flow rate, the two Pomphorhynchus species exhibited a contrasting use of two of the most abundant fish species, with P. laevis mainly using European chub and P. tereticollis mainly using common barbel. This pattern was particularly clear in the Vingeanne locality, where fewer fish species were used overall ( Fig. 3b ).

and 2.34%, respectively; Fig. 1 ). In most fish species from which at least 20 Pomphorhynchus were genotyped, one of the two species was significantly more abundant than expected from its relative abundance in intermediate hosts (Fisher exact test, probabilities corrected for multiple testing: P <0.05 to 0.001; Fig. 1 ). In addition, the relative proportion of P. laevis and P. tereticollis differed significantly according to fish ecology (nested GLM with binomial distribution: Population effect,

Figures

Fig. 1. Percentage of P. laevis (plain bars) and P. tereticollis (striped bars) among Pomphorhynchus parasites collected from amphipod intermediate hosts in the benthos, and from the fish definitive hosts, either in the intestine or collected as extraintestinal cystacanths, in (a) the Ouche and (b) Vingeanne localities. The proportion of P. laevis and P. tereticollis in each fish species was compared to their proportion in intermediate gammarid hosts using Fisher exact test (P-values given after correction for multiple test: ***: P <0.001; **: P <0.01; *: P <0.05; ns: not significant). Letters above bars refer to post-hoc comparison between fish species (Tukey HSD). Numbers below bars are sample sizes (number of parasites). Bentho-pelagic fish species are abbreviated in italics, benthic species in standard font. Species abbreviations: Barbus barbus, Bbs; Gobio gobio, Gg; Squalius cephalus, Sc; Telestes souffia, Ts; Chondrostoma nasus, Cn; Rutilus rutilus, Rr; Scardinius erythrophthalmus, Se; Leuciscus leuciscus, Ll; Phoxinus phoxinus, Pp; Barbatula barbatula, Bba; Ameiurus melas, Am; Perca fluviatilis, Pf; Cottus gobio, Cg; Gasterosteus aculeatus, Ga.

Fig. 2. Relationship between fish biomass (g.100m-2) and P. laevis (a) or P. tereticollis (b) mean abundance per fish species, across fish species and localities (Ouche and Vingeanne localities). Both variables were log10-transformed.

Fig. 4. Relationship between the phylo-structural index of specificity towards definitive hosts and observed prevalence in gammarid intermediate hosts (%) in P. laevis and P. tereticollis. The phylo-structural index of specificity increases with the taxonomic diversity of fish species used.

Fig. 3. Relative flow rates of P. tereticollis and P. laevis in their hosts in the Ouche (a) and Vingeanne (b) localities, taking into account the abundance of adult intestinal parasites and the relative abundance of each fish host species in the local community. The thickness of arrows and percentages indicate the estimated relative value of each fish species as a resource for each Pomphorhynchus species.