Open Access
Original contribution
Issue
Parasite
Volume 18, Number 1, February 2011
Page(s) 71 - 78
DOI https://doi.org/10.1051/parasite/2011181071
Published online 15 February 2011

© PRINCEPS Editions, Paris, 2011, transferred to Société Française de Parasitologie

Licence Creative Commons
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Introduction

Community ecology of fish parasites has been the subject of numerous studies since the early works of Dogiel and colleagues in the 1940 s (see Dove, 1999, but also Koskivaara et al., 1992; Rohde et al., 1995; Sasal & Morand, 1998). These studies have mostly concerned temperate fresh water fish (Šimková et al., 2002a, Šimková, Kadlec 2002b) and temperate or tropical marine parasites (Benajiba et al., 1994; Rohde et al., 1995; Lo et al., 1998; Sasal & Morand, 1998; Gonzalez & Poulin, 2005). However, studies concerning freshwater fish in intertropical zone and particularly in Africa are rare (Obiekezie, 1991; Obiekezie & Taege, 1991; Bilong Bilong & Njiné, 1998; Olurin & Somorin, 2006). As far as the parasite community interactions are concerned, some theoretical principles are proposed. The structure of parasite communities has been explained in different and sometimes contradictory ways. For Holmes (1973), the structure of parasite communities is the result of competitive interspecific interactions that act on the population’s spatial distribution and density (interactive communities). In contrast, for Price (1980) the structure of parasite communities may result from the random assembly of species that evolve independently (isolationist communities). Studying fish ectoparasites, Rohde (1991) concluded that the microhabitats of a given parasite species did not seem to be affected by the presence of potential competitors. However, except for a few isolated reports that showed positive interactions (Adams, 1986; Silan & Maillard, 1990; Koskivaara, 1992), most interspecific studies showed the lack of interactions in parasite communities (El Hafidi et al., 1998; Morand & Šimková, 2005). Generally, interactive communities are species rich, have many core species (often specialist), a large degree of niche overlap between parasite species, and a dominance of interspecific interactions over individualistic responses, resulting in predictable infracommunities (Holmes & Price, 1986). Isolationist communities generally have few species, a higher proportion of rare (satellite) generalist species, large amounts of available niche space, and dominance of individualistic responses over interspecific interactions. This results in communities which structure is difficult to predict and largely stochastically determined (Dove, 1999). Finally, greater parasite diversity represents more stable communities.

Barbus martorelli Roman, 1971 (Cyprinidae) is one of the common fish species in Southern Cameroon (Vivien, 1991). Highly consumed by rural human populations in this part of the nation, it thus constitutes one of main animal proteins source. The gills of this fish are parasitized by two species of Myxosporidia: Myxobolus barbi Fomena, Bouix and Birgi, 1985 and M. njinei Fomena, Bouix and Birgi, 1989 (Fomena et al., 1989) and eight species of Monogenea: Dactylogyrus bopeleti, D. insolitus, D. simplex, D. maillardi, Dogielius martorellii (Birgi & Lambert, 1987), Dogielius sp., Gyrodactylus sp. and Polystomatid larva (Tombi & Bilong Bilong, 2004). Aspects of the distribution of all the above gill parasites and the temporal structure of their communities were studied by Tombi & Bilong Bilong (2004) and Bilong Bilong & Tombi (2005) respectively. Taking in consideration this high parasite diversity, the present work aims to study the composition of different gill communities and determine whether or not the different populations are isolationist or interactive.

Material and Methods

Host specimens were caught from May 1998 to August 1999, in the Foulou watercourse at Nkolfoulou 3°53’N, 11°34’E i.e. in the outskirts of Yaoundé, Capital of the Republic of Cameroon (Central Africa). Fish standard lengths (SL) were measured from the extremity of the muzzle to the last vertebra. Methods of catching, transport, dissection, parasite collection have been described by Tombi & Bilong Bilong (2004). Three levels of analyses, from the large to the most reduced, were retained in the present study of parasite associations, i.e. the infracommunity, the gill filament and the filament fraction levels respectively. The latter was obtained by subdividing a filament in three equidistant parts (proximal, median, and distal fractions), using an ocular micrometer of the stereoscopic microscope. The terms infrapopulation and infracommunity on the one hand, compound and component community on the other hand, are defined according to Sousa (1994) and Combes (1995). The prevalence and intensity of parasites were defined according to Margolis et al. (1982). On the prevalence basis and according to Valtonen et al. (1997), parasite species were termed common (occurrence > 50%), intermediate (10% ≤ occurrence ≤ 50%) and rare (occurrence < 10%). These categories correspond to what Hansky in Koskivaara & Valtonen (1991) designated as core, secondary or satellite. It should be noted that rare species were hereafter excluded from the inter-action analysis due to their rare occurrence and very low intensities: less than two. Furthermore and according to Rohde (1979), Holmes, (1987), and Combes, (1995), rare species are not structuring.

Quantifying community structure using null models

Dice’s coefficient (D) and that of Whittaker & Fairbanks (WF) were used to measure the degree of association. Dice coefficient is a similarity measure related to the Jaccard index. The percentage similarity index of Whittaker & Fairbanks incorporates information about all of the species that are counted and, theoretically, values for this index will range from 0.0 (totally different communities) to 100 (identical communities). Forbes’ index measured the amount of association deviation from expectation (Abdallah & Saporta, 2003). The Chi-square (χ2) test was used to evaluate the degree of departure from random association and P values less than 5% were considered significant. The abbreviation “d.f.” was used for degree of freedom. We tested whether co-occurrence of different monogenean species in the same fish host were more or less frequent than expected by chance, we followed Janovy et al. (1995) by generating a null model of expected frequencies based on the actual prevalence of the different parasite species. The null model corresponds to the probability that any two or more parasite species co-occurring in a fish is equal to the product of their prevalence in the sample. Observed and expected frequencies were compared with a Chi-square (χ2) test (Janovy et al., 1995).

Results

A total of 558 Barbus martorelli were caught and dissected from May 1998 to August 1999. Their standard length (SL) varied from 30 to 119 mm. The prevalences of helminth species were 80.6%, 84.4%, 70.8%, 33.2%, 9.3%, 0.4%, 5.9%, and 5.6% for D. bopeleti, D. insolitus, D. simplex, D. maillardi, Dogielius sp., Do. martorelli, Polystomatid larva and Gyrodactylus sp. respectively; the occurrence of myxosporidian cysts was 79% and 27.7% for M. barbi and M. njinei respectively. Thus, D. bopeleti, D. insolitus and D. simplex represented the helminth core species, while D. maillardi was a secondary one and Dogielius sp., Do. martorelli, Polystomatid larva and Gyrodactylus sp. revealed rare. Diffuse spores being uncountable, based on the occurrence of cysts, M. barbi and M. njinei were considered core and secondary metazoan species respectively.

Infracommunity

Four (0.7%) of 558 B. martorelli were not parasitized while 554 (99.3%) were infected by at least one parasite species. A total of 8,773 helmiths and 44,824 cysts were collected with an average of 16.56 ± 15.02 and 98.79 ± 203.58 parasites/fish respectively. 24 host individuals (4.3%) showed a single species infection and 42 (7.6%), 119 (21.5%), 179 (32.3%), 131 (23.7%), 50 (9.0%) and 9 (1.6%) had multiple infections with 2, 3, 4, 5, 6 and 7 parasite species respectively (Table I). Myxobolus njinei and none of the rare species were found solely. A total of 95 of the 1,023 expected combinations were observed (Table I). Myxobolus barbi, alone, parasitized 18 host individuals. The following combinations “D. insolitus – M. barbi”, “D. bopeleti – D. insolitus – M. barbi”, “D. bopeleti – D. insolitus – D. simplex – M. barbi”, “D. bopeleti – D. insolitus – D. maillardi – D. simplex – M. barbi”, “D. bopeleti – D. insolitus – D. maillardi – D. simplex – M. barbi – M. njinei” and “D. bopeleti – D. insolitus – D. maillardi – D. simplex – Do. martorelli – M. barbi – M. njinei” were the most frequent for multiple infections by 2, 3, 4, 5, 6 and 7 different species respectively (Table I). In Nkolfoulou, two parasite combinations: “D. bopeleti – D. insolitus – D. simplex – M. barbi” and “D. bopeleti – D. insolitus – D. maillardi – D. simplex – M. barbi” amongst 95 observed had intermediate occurrence # 15.2% and # 10.3% respectively; the other remaining assemblages were rare. Also, none of the 544 B. martorelli harboured eight to ten parasite species.

Table I.

Types of combinations among gill parasites.

Interspecific interactions

At the infracommunity level, all parasite core species showed strong positive associations as D ≥ 0.60 (Fig. 1). The same result was obtained with WF index, except for the pair “D. simplex – M. barbi” for which the association was weak (WF = 0.25). Core species and secondary ones never developed strong associations. In all associations observed, the values of F index were almost equal to 1 and due at random, except for D. maillardi and M. njinei (Fig. 1). Conversely, at the level of a filament (Fig. 2), D varied from 0.9.10−4 to 73.10−4, supporting obviously that no interaction exist between the different taxa. Forbes’ index varied from 0.013 to 0.31 indicating that, these associations differ from the expected assemblages (P < 0.001), except for the pair “D. bopeleti – D. insolitus” (P = 0.88). At the filament fraction level and for the different parasite assemblages, D and WF varied from 0.0065 to 0.013 and -0.99 to -0.95 respectively, proving almost the whole absence of interaction between these parasites.

thumbnail Fig 1.

Association coefficients calculated for pairs of parasite species at the infracommunity level.

In each box, the first two numbers up to down represent the values of Dice and Whittaker & Fairbanks indexes respectively, and the third number the value of Forbes index.

thumbnail Fig 2.

Association coefficients calculated for pairs of parasites species at the filament level.

In each box, the first two numbers up to down represent the values of Dice and Whittaker & Fairbanks indexes respectively, while the two latter represent Forbes index and χ2 test respectively; * p < 0.05.

Community structure

We compared the observed species richness to that predicted by the null model for interactions of parasite species in an assemblage (Janovy et al., 1995). We found a significant difference (χ2 = 77.17, d.f. = 5, P < 0.0001). Fig. 3 shows this frequency distribution. A significantly greater number of fish carried 1, 5 or 6 (rare species are not considered) parasite species whereas fewer than expected carried 2, 3 or 4 parasite species.

thumbnail Fig 3.

Observed (grey bars) and expected (white bars) frequency distribution of gill parasite species richness at the infracommunity level.

Discussion

The gill parasite fauna of Barbus martorelli is very diversified and made up of two species of Myxosporidia and eight of Monogenea, i.e. seven Monopisthocotyleans and one Polyopisthocotylean, all core and secondaries species presenting aggregated distribution (Tombi & Bilong Bilong, 2004). Such observed rich parasitofauna, including many phyla, have been regularly reported in fishes (Koskivaara et al., 1991; Benajiba et al., 1994; Oliva & Luque, 1998; Tavares & Luque, 2004; Gonzales & Poulin, 2005). In Africa, the study of fish parasite diversity had mainly concerned organisms of the same phylum (Birgi & Lambert, 1987; Fomena et al., 1989; Bilong Bilong et al., 1999; Bilong Bilong et al., 2004; Nack et al., 2005; Nack & Bilong Bilong, 2007).

In B. martorelli, the fact that M. njinei and all rare species were not observed solely (monospecific infection) suggests that, these parasites may be able to infect their host only when the latter is infected by one or more other parasite taxa. In Cameroon, a similar observation was made for Cichlidogyrus falcifer and Onchobdella aframae, two monogenean gill parasites of Hemichromis fasciatus (Cichlidae) in the Ozum II and Melen pounds (Bilong Bilong, 1995). This could be related to the effects of some parasites on the fish immune responses, which may impact co-infections (Šimková et al., 2008; Poisot et al., 2009). This observation and the fact that all but one (98.9%) parasite combinations observed included the core species D. bopeleti, D. insolitus, D. simplex and M. barbi confirm that negative interactions did not seem to play an important role in these parasite infracommunities. The use of null model (Janovy et al., 1995) confirmed also that parasite species are positively associated rather than negatively. Tombi & Bilong Bilong (2004) showed that the average total number of helminth individuals increased with host size, and was associated with a progressive decrease in the number of cysts, suggesting the existence of negative interspecific interactions between parasite phyla. However, we found no negative association between Myxobolus barbi (which formed cysts most abundantly in the different infracommunities studied) and any monogenean species. Therefore, the reduction of this myxosporean cyst abundance as a function of the host length could be associated to some changes related to fish age, such as immune defence (West & Roubal, 1998; Morand et al., 2002).

Altogether, our results confirm Rohde’s (1994) opinion that positive interactions between fish ectoparasites are more frequent than negative. Contrary to the statements of Holmes & Price (1986) that negative interactions should be frequent, our results also suggest that infrapopulations of monogeneans in B. martorelli are isolationist, although infracommunities are speciesrich and have mainly core species. In isolationist parasite communities where interactions are negligible, the co-occurrence of species in hosts is not expected to deviate from that expected by chance if interspecific interactions are the main structuring processes in parasite infracommunities. Lerssutthichawal & Lim (2005) also stated that the diversity in a community is an indication of stability, i.e. the greater the diversity the more stable the community. In conclusion, the infracommunities structure of B. martorelli seems to be predictable stable, and isolationist. Therefore, it is worthwhile to determine the spatial niche width of these core species, because it remains unexplained that none of the hosts harboured eight to ten parasite species.

Acknowledgments

The authors hereby thank Dr. Anna Eno for editing this article. We also thank two referees for their helpful comments and suggestions.

References

  1. Abdalla H. & Saporta G. Mesures de distance entre modalités de variables qualitatives; application à la classification. Revue Statistique Appliquée, 2003, 51, 75–90. [Google Scholar]
  2. Adams A.M. The parasite community on the gills of Fundulus kansae (Garman) from the South Platte River, Nebraska (USA). Acta Parasitologica, 1986, 31, 47–54. [Google Scholar]
  3. Benajiba M.H., Silan P., Marques A. & Bouix G. Protozoaires et Métazoaires parasites de l’anguille Anguilla anguilla : L.,1758 : structures temporelles de leurs populations dans une lagune Méditerranéenne. Annales Sciences Naturelles, 1994, 15, 141–149. [Google Scholar]
  4. Bilong Bilong C.F. Les Monogènes parasites des poissons d’eau douces du Cameroun : biodiversité et spécificité; biologie des populations inféodées à Hemichromis fasciatus. Thèse de Doctorat d’État, Université de Yaoundé I, Cameroun, 1995, 341 pp. [Google Scholar]
  5. Bilong Bilong C.F., Atyame Ntem C.M. & Njine T. Structure de la guilde des Monogènes parasites branchiaux du poisson Hemichromis fasciatus au lac municipal de Yaoundé. Journal of the Cameroon Academy of Sciences, 2004, 4, 33–40. [Google Scholar]
  6. Bilong Bilong C.F., Le Pommelet E. & Silan P. The gills of Hemichromis fasciatus Peters, 1858 (Teleotei, Cichlidae), a biotope for ectoparasites: structure, heterogeneity and growth model. Écologie, 1999, 30, 125–130. [Google Scholar]
  7. Bilong Bilong C.F. & Njine T. Dynamique de populations de trois Monogènes parasites d’Hemichromis fasciatus Peters, 1858 dans le lac municipal de Yaoundé, et intérêt possible en pisciculture intensive. Annales Faculté Sciences Université Yaoundé I. Série Sciences Naturelles et Vie, 1998, 34, 295–303. [Google Scholar]
  8. Bilong Bilong C.F. & Tombi J. Temporal structure of a component community gill parasites of Barbus martorelli Roman, 1971 (Freshwater Cyprinidae) in the centre province, Cameroon. Cameroon Journal Biological Biochemical Sciences, 2005, 13, 9–18. [Google Scholar]
  9. Birgi E. & Lambert A. Les Dactylogyridae (Plathelminthes, Monogenea) des Cyprinidae du genre Barbus du Sud Cameroun. Revue Hydrobiologie Tropicale, 1987, 20, 37–48. [Google Scholar]
  10. Combes C. Interactions durables. Écologie et évolution du parasitisme. Collection d’écologie 26. Masson, Paris, 1995, 524 pp. [Google Scholar]
  11. Dove A.D.M. A new index of interactivity in parasite communities. International Journal for Parasitology, 1999, 29, 915–920. [CrossRef] [PubMed] [Google Scholar]
  12. El Hafidi F., Berrada-Rkhami O., Benazzou T. & Gabrion C. Microhabitat distribution and coexistence of Microcotylidae (Monogenea) on the gills of the striped mullet Mugil cephalus: chance or competition? Parasitology Research, 1998, 84, 315–320. [CrossRef] [PubMed] [Google Scholar]
  13. Fomena A., Bouix G. & Birgi E. Contribution à l’étude des myxosporidies des poissons d’eau douce du Cameroun II. Espèces nouvelles du genre Myxobolus Bütschli, 1882. Bulletin Institut Français d’Afrique Noire, 1989, 46, 167–192. [Google Scholar]
  14. Gonzàlez M.T. & Poulin R. Spatial and temporal predictability of the parasite community structure of a benthic marine fish along its distributional range. International Journal for Parasitology, 2005, 35, 1369–1377. [CrossRef] [PubMed] [Google Scholar]
  15. Holmes J.C. Site selection by parasitic helminths: interspecific interactions, site segregation, and their importance to the development helminth communities. Canadian Journal of Zoology, 1973, 51, 333–347. [CrossRef] [PubMed] [Google Scholar]
  16. Holmes J.C. The structure of Helminth communities. International Journal for Parasitology, 1987, 17, 203–208. [CrossRef] [PubMed] [Google Scholar]
  17. Holmes J.C. & Price P.W. Communities of parasites, in: Community Ecology: Pattern and Process Anderson D.J. & Kikkawa J. (eds), Blackwell Scientific Publications, Victoria, 1986, 187–213. [Google Scholar]
  18. Janovy JR J., Clopton R.E., Clopton D.A., Synder S.D., Efting A. & Krebs L. Species density distributions as null models for ecological significant interactions of parasite species in an assemblage. Ecological Modelling, 1995, 77, 189–196. [CrossRef] [Google Scholar]
  19. Koskivaara M. Environmental factors affecting monogeneans parasitic on freshwater fishes. Parasitology Today, 1992, 8, 339–342. [CrossRef] [Google Scholar]
  20. Koskivaara M. & Valtonen E.T. Paradiplozoon homoion (Monogenea) and some other gill parasites on roach Rutilus rutilus in Finland. Aqua Fennica, 1991, 21, 137–143. [Google Scholar]
  21. Koskivaara M., Valtonen E.T. & Prost M. Dactylogyrids on the gills of roach in Central Finland: features of infection and species composition. International Journal for Parasitology, 1991, 21, 565–572. [CrossRef] [PubMed] [Google Scholar]
  22. Koskivaara M., Valtonen E.T. & Vuori K.M. Microhabitat distribution and coexistence of Dactylogyrus species (Monogenea) on the gills of roach. Parasitology, 1992, 104, 273–281. [CrossRef] [Google Scholar]
  23. Lerssutthichawal T. & Lim S.H.L. Diversity of freshwater Monogeneans from Siluriform fishes of Thailand, in: Diseases in Asian Aquaculture V. Walker P., Lester R. & Bondad-Reantaso M.G. (eds.), Fish Health Section, Asian Fisheries Society, Manila, 2005, 217–225. [Google Scholar]
  24. Lo C.M., Morand S. & Galzin R. Parasite diversity/host age and size relationship in three coral reef fishes from French Polynesia. International Journal for Parasitology, 1998, 28, 1695–1708. [CrossRef] [PubMed] [Google Scholar]
  25. Margolis L., Esh G.W., Holmes J.C., Kuris A.M. & Schad G.A. The use of the ecological terms in parasitology (Report of an ad hoc committee of the American Society of Parasitogists). Journal for Parasitology, 1982, 68, 131–133. [CrossRef] [Google Scholar]
  26. Morand S. & Šimkovà A. Metapopulation biology of marine fish parasites, in: Marine Parasite Rohde K., (ed.), CSIRO Publishing, Collingwood, Australia, 2005, 302–309. [Google Scholar]
  27. Morand S., Šimkovà A., Matejusovà I., Plaisance L., Verneau O. & Desdevises Y. Investigating patterns may reveal processes: evolutionary ecology of ectoparasitic monogeneans. International Journal for Parasitology, 2002, 32, 111–119. [CrossRef] [PubMed] [Google Scholar]
  28. Nack J. & Bilong Bilong C.F. Biotope des ectoparasites branchiaux de Clarias camerunensis Lönnberg, 1895 (Pisces: Clariidae) : modèle de croissance de l’aire colonisable. Journal of the Cameroon Academy of Sciences, 2007, 7, 11–16. [Google Scholar]
  29. Nack J. Bilong Bilong C.F. & Euzet L. Monogènes parasites de Clariidae (Teleostei, Siluriforms) au Cameroun: I. Description de deux nouvelles espèces du genre Gyrodactylus dans le bassin du Nyong, parasite, 2005, 12, 213–220. [CrossRef] [EDP Sciences] [PubMed] [Google Scholar]
  30. Obiekezie A.I. The principal pathogens and diseases of cultured fishes in Nigeria, in: Aquaculture in Africa. Koop K. (ed.), 1991, 197–207. [Google Scholar]
  31. Obiekezie A.I. & Taege M. Mortalities in hatchery reared fry of the African catfish, Clarias gariepinus (Burchell) caused by Gyrodactylus groschafti Ergens, 1973. Bulletin European Associaton Fish Patholology, 1991, 11, 82–85. [Google Scholar]
  32. Oliva M.E. & Luque J.L. Metazoan parasite infracommunities in five Sciaenids from the Central Peruvian Coast. Memorias Institudo Oswaldo Cruz, 1998, 93, 175–180. [CrossRef] [Google Scholar]
  33. Olurin K.B. & Somorin C.A. Intestinal helminths of the fishes of Owa Stream, South-West Nigeria. Research Journal of Fish and Hydrobiology, 2006, 1, 6–9. [Google Scholar]
  34. Poisot T., Šimková A., Hyršl P. & Morand S. Interactions between immunocompetence, somatic condition, and parasitism in the chub in early spring. Journal of Fish Biology, 2009, 75, 1667–1682. [CrossRef] [PubMed] [Google Scholar]
  35. Price P.W. Evolutionary biology of parasites. Princeton University Press, 1980, 237 pp. [Google Scholar]
  36. Rohde K. A critical evaluation of intrinsic and extrinsic factors responsible for niche restriction in parasites. American Naturalist, 1979, 144, 648–671. [Google Scholar]
  37. Rohde K. Intra- and interspecific interactions in low density populations in resource-rich habitats. Oikos, 1991, 60, 91–104. [CrossRef] [Google Scholar]
  38. Rohde K. Niche restriction in parasites: proximate and ultimate causes. Parasitology, 1994, 109, 69–84. [CrossRef] [Google Scholar]
  39. Rohde K., Hayward C. & Heap M. Aspects of the ecology of metazoan ectoparasites of marine fishes. International Journal for Parasitology, 1995, 25, 945–970. [CrossRef] [PubMed] [Google Scholar]
  40. Sasal P. & Morand S. Comparative analysis: a tool for studying monogenean ecology and evolution. International Journal for Parasitology, 1998, 28, 1637–1644. [CrossRef] [PubMed] [Google Scholar]
  41. Silan P. & Maillard C. Comparative structures and dynamics of some populations of helminths parasites of fishes: the sea bass – Diplectanum model. Acta Oecology, 1990, 11, 857–874. [Google Scholar]
  42. Šimková A., Kadlec D., Gelnar M. & Morand S. Abundanceprevalence relationship of gill congeneric ectoparasites: testing for core-satellite hypothesis and ecological specialisation. Parasitology Research, 2002a, 88, 682–686. [CrossRef] [Google Scholar]
  43. Šimková A., Lafond T., Ondrackova M., Jurajda P., Ottová E. & Morand S. Parasitism, life history traits and immune defence in cyprinid fish. BMC Evolutionary Biology, 2008, 8, 29–39. [CrossRef] [PubMed] [Google Scholar]
  44. Šimková A., Ondrackova M., Gelnar M. & Morand S. Morphology and coexistence of congeneric ectoparasite species: reinforcement of reproductive isolation? Biological Journal of the Linnean Society, 2002b, 76, 125–135. [Google Scholar]
  45. Sousa W.P. Patterns and processes in communities of helminth parasites. Trends Ecology and Evolution, 1994, 9, 52–57. [CrossRef] [Google Scholar]
  46. Tavares L.E.R. & Luque J.L. Community ecology of the metazoan parasites of White Sea catfish, Netuma barba (Osteichthyes: Ariidae), from the coastal zone of the state of Rio de Janeiro, Brazil. Brazil Journal of Biology, 2004, 64, 169–176. [CrossRef] [Google Scholar]
  47. Tombi J. & Bilong Bilong C.F. Distribution of gill parasites of the freshwater fish Barbus martorelli Roman, 1971 (Teleostei: Cyprinidae) and tendency to inverse intensity evolution between myxosporidia and monogenea as a function of the host age. Revue d’Élevage et Médecine. Vétérinaire des Pays Tropicaux, 2004, 57, 71–76. [Google Scholar]
  48. Valtonen E.T., Holmes J.C. & Koskivaara M. Eutrophication, pollution and fragmentation: effects on parasite communities in roach (Rutilus rutilus) and perch (Perca fluviatilis) in four lakes in Central Finland. Canadian Aquatic Fisheries Science, 1997, 54, 572–585. [CrossRef] [Google Scholar]
  49. Vivien J. Faune du Cameroun. Guide des Mammifères et Poissons. Gicam, Paris, 1991, 271 pp. [Google Scholar]
  50. West A.P. & Roubal F.R. Population dynamics of the monogenean Anoplodiscus cirrusspiralis on the snapper, Pagrus auratus. International Journal for Parasitology, 1998, 28, 571–577. [CrossRef] [Google Scholar]

All Tables

Table I.

Types of combinations among gill parasites.

All Figures

thumbnail Fig 1.

Association coefficients calculated for pairs of parasite species at the infracommunity level.

In each box, the first two numbers up to down represent the values of Dice and Whittaker & Fairbanks indexes respectively, and the third number the value of Forbes index.

In the text
thumbnail Fig 2.

Association coefficients calculated for pairs of parasites species at the filament level.

In each box, the first two numbers up to down represent the values of Dice and Whittaker & Fairbanks indexes respectively, while the two latter represent Forbes index and χ2 test respectively; * p < 0.05.

In the text
thumbnail Fig 3.

Observed (grey bars) and expected (white bars) frequency distribution of gill parasite species richness at the infracommunity level.

In the text

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