Anindo Choudhury

Parasite inventories and DNA-based taxonomy: lessons from helminths of freshwater fishes in a megadiverse country.

Abstract Freshwater fish helminth parasites are undoubtedly the most well-known group among vertebrate parasites in Mexico; these parasites include 37 adult and 43 larval (metacercariae) species of trematodes, 62 monogeneans, 15 adult and 18 larval (metacestode) cestodes, 6 adult and 4 larval (cystacanth) acanthocephalans, and 54 adult and 15 larval nematodes (L3). Here, we evaluate the extent of the freshwater fish helminth inventory of Mexico using species accumulation curves and discuss the implications of DNA-based taxonomic methods in our understanding of the helminth biodiversity in freshwater fishes. Future directions for the study of the helminth parasites of freshwater fishes are proposed, particularly the role of DNA-based species delimitation criteria in recognizing parasite species, but also in discovering cryptic species. Species accumulation curves indicate that even though the asymptote has not been reached, a tendency toward stabilization is observed in all taxonomic groups except monogeneans. We suggest, therefore, that the inventory, as conventionally understood, is nearing completion for most groups. We suggest that future survey work aimed at enhancing the biodiversity inventory should be strategic, i.e., it should combine the need to target missing components of the host spectrum with the choice of appropriate drainages based on biogeographic, faunistic, and hydrologic data. We also posit that the future belongs to DNA-based taxonomic approaches that aim to uncover previously unrecognized biodiversity.

Parasites of native and nonnative fishes of the Little Colorado River, Grand Canyon, Arizona.

A 2-yr, seasonal, parasitological study of 1,435 fish, belonging to 4 species of native fishes and 7 species of nonnative fishes from the lower Little Colorado River (LCR) and tributary creeks, Grand Canyon, Arizona, yielded 17 species of parasites. These comprised 1 myxozoan (Henneguya exilis), 2 copepods (Ergasilus arthrosis and Lernaea cyprinacea), 1 acarine (Oribatida gen. sp.), 1 piscicolid leech (Myzobdella lugubris), 4 monogeneans (Gyrodactylus hoffmani, Gyrodactylus sp., Dactylogyrus extensus, and Ligictaluridus floridanus), 4 nematodes (Contracaecum sp., Eustrongylides sp., Rhabdochona sp., and Truttaedacnitis truttae), 3 cestodes (Bothriocephalus acheilognathi, Corallobothrium fimbriatum, and Megathylacoides giganteum), and 2 trematodes (Ornithodiplostomum sp. and Posthodiplostomum sp.). Rhabdochona sp. was the only adult parasite native to the LCR. Infection intensities of Ornithodiplostomum sp. and B. acheilognathi were positively correlated with length of the humpback chub Gila cypha. Adult helminths showed a high degree of host specificity, except B. acheilognathi, which was recovered from all fish species examined but was most abundant in cyprinids. Abundance of B. acheilognathi in the humpback chub was highest in the fall and lowest in the summer in both reaches of the LCR. There was no major taxonomic difference in parasite assemblages between the 2 different reaches of the river (LC1 and LC2). Parasite community diversity was very similar in humpback chub, regardless of sampling site or time. The parasite fauna of the LCR is numerically dominated by B. acheilognathi and metacercariae of Ornithodiplostomum sp. The richest and most diverse component community occurred in a nonnative species, the channel catfish Ictalurus punctatus, but infracommunity species richness was highest in a native host, humpback chub.

Adult Endohelminth Parasites of Ictalurid Fishes (Osteichthyes: Ictaluridae) in Mexico: Empirical Evidence for Biogeographical Patterns

Abstract The helminth fauna of Mexican ictalurids was investigated through original surveys and published literature in order to evaluate the biogeography of host-parasite associations of a primarily nearctic host group in a major faunal transition area. In total, 84 specimens of 4 species of ictalurids (Ictalurus balsanus, Ictalurus dugesi, Ictalurus furcatus, and Ictalurus punctatus) were sampled from 7 localities in 5 hydrological drainages. Ten species of adult endohelminths were recovered from this survey, including 4 species of digeneans (Phyllodistomum lacustri, Genarchella tropica, Alloglossidium corti, and Campechetrema sp.), 3 cestodes (Corallobothrium fimbriatum, Megathylacoides giganteum, and Choanoscolex lamothei), and 3 nematodes (Dichelyne mexicanus, Goezia sp., and Rhabdochona sp.). The adult helminth fauna of ictalurids reported in this study is composed of taxa that are typical of ictalurids in other parts of North America, north of Mexico. This core fauna (in a historical biogeographic sense) includes the corallobothriines C. fimbriatum and M. giganteum and the digeneans P. lacustri and A. corti. Two other helminths, C. lamothei and D. mexicanus, may be added to this group in the future. Other helminths occurred sporadically and provide evidence for host-sharing (ecological host extensions), but we were unable to identify any valid cases of host-switching from more distantly related hosts. The helminth fauna provides evidence that the ictalurids developed their characteristic helminth fauna without neotropical influences and that the phylogenetic affinities of the ictalurids do not appear to be with any neotropical siluriform.

Molecular prospecting for cryptic species in Phyllodistomum lacustri (Platyhelminthes, Gorgoderidae)

Rosas‐Valdez, R., Choudhury, A. & Pérez‐Ponce de León, G. (2011). Molecular prospecting for cryptic species in Phyllodistomum lacustri (Platyhelminthes, Gorgoderidae). —Zoologica Scripta, 40, 296–305.

Experimental infection of the endangered bonytail chub (Gila elegans) with the Asian fish tapeworm (Bothriocephalus acheilognathi): impacts on survival, growth, and condition

Bothriocephalus acheilognathiYamaguti, 1934, a tapeworm known to be pathogenic to some fish species, has become established in the endangered humpback chub (Gila cypha Miller, 1964) in Grand Canyon, USA, following the tapeworms introduction into the Colorado River system. The potential impact of this tapeworm on humpback chub was studied by exposing the closely related bonytail chub (Gila elegans Baird and Girard, 1853) to the parasite under a range of conditions that included potential stressors of humpback chub in their natal waters, such as abrupt temperature change and a limited food base. Survival of infected fish under low food rations was considerably lower than that of control fish, and mortality of infected fish began 20 days earlier. Growth of infected fish was signifi- cantly reduced, and negative changes in health condition indices were found. No significant negative impacts were re- vealed from the synergistic effects between temperature shock and infection. Bothriocephalus acheilognathi does present a potential threat to humpback chub in Grand Canyon and should be considered, along with conventional con- cerns involving altered flow regimes and predation, when management decisions are made concerning conservation of this endangered species. Resume ´ : Bothriocephalus acheilognathiYamaguti, 1934, un ver plat connu comme pathogene pour certaines especes de

The Phylogenetic Position of Allocreadiidae (Trematoda: Digenea) From Partial Sequences of the 18S and 28S Ribosomal RNA Genes

Species of Allocreadiidae are an important component of the parasite fauna of freshwater vertebrates, particularly fishes, and yet their systematic relationships with other trematodes have not been clarified. Partial sequences of the 18S and 28S ribosomal RNA genes from 3 representative species of Allocreadiidae, i.e., Crepidostomum cooperi, Bunodera mediovitellata, and Polylekithum ictaluri, and from 79 other taxa representing 78 families of trematodes obtained from GenBank, were used in a phylogenetic analysis to address the relationships of Allocreadiidae with other plagiorchiiforms/plagiorchiidans. Maximum parsimony and Bayesian analyses of combined 18S and 28S rRNA gene sequence data place 2 of the allocreadiids, Crepidostomum cooperi and Bunodera mediovitellata, in a clade with species of Callodistomidae and Gorgoderidae, which, in turn is sister to a clade containing Polylekithum ictaluri and representatives of Encyclometridae, Dicrocoelidae, and Orchipedidae, a grouping supported by high bootstrap values. These results suggest that Polylekithum ictaluri is not an allocreadiid, a conclusion that is supported by reported differences between its cercaria and that of other allocreadiids. Although details of the life cycle of callodistomids, the sister taxon to Allocreadiidae, remain unknown, the relationship of Allocreadiidae and Gorgoderidae is consistent with their larval development in bivalve, rather than gastropod, molluscs, and with their host relationships (predominantly freshwater vertebrates). The results also indicate that, whereas Allocreadiidae is not a basal taxon, it is not included within the suborder Plagiorchiata. No support was found for a direct relationship between allocreadiids and opecoelids either.

The systematic position of Wallinia spp. and Margotrema spp. (Digenea), parasites of Middle-American and Neotropical freshwater fishes, based on the 28S ribosomal RNA gene

The systematic relationships of aspinose allocreadiid-like digeneans from Middle-American and Neotropical freshwater fishes, such as Wallinia Pearse, 1920, Margotrema Lamothe-Argumedo, 1970, Magnivitellinum Kloss, 1966 and other related genera, remain enigmatic. Wallinia (2 spp.) and Margotrema (2 spp.) have been placed in the subfamily Walliniinae, within the Macroderoididae. Recent descriptions of species in these genera have followed this classification but have raised questions about their affinities with macroderoidids. Partial sequences of the 28S rRNA gene of Walliniachavarriae Choudhury, Hartvigsen & Brooks, 2002 and Margotremabravoae Lamothe Argumedo, 1970, as representatives of their genera, were used in a phylogenetic analysis along with the available sequences of macroderoidids and allocreadiids. Results from Maximum Parsimony, Maximum Likelihood and Bayesian Analyses were identical in placing both genera into one clade along with allocreadiids rather than the macroderoidids. Margotrema was the sister group of Crepidostomum Braun, 1900, and Wallinia was the sister group of both Margotrema and Crepidostomum combined. Bootstrap and Bremer values, as well as posterior probabilities derived from Bayesian analysis strongly supported these relationships in three analyses.

PHYLOGENETIC ANALYSIS ON GENERA OF CORALLOBOTHRIINAE (CESTODA: PROTEOCEPHALIDEA) FROM NORTH AMERICAN ICTALURID FISHES, USING PARTIAL SEQUENCES OF THE 28S RIBOSOMAL GENE

Partial sequences of the 28S rDNA (ribosomal gene) were obtained from a total of 11 populations of 5 species (in 3 genera) of North American corallobothriine proteocephalideans. These included Corallobothrium fimbriatum (3 populations), Corallobothrium parafimbriatum (1 population), Corallotaenia minutia (1 population), Megathylacoides giganteum (2 populations), and Megathylacoides lamothei (4 populations). These sequences were used in a phylogenetic analysis to test the monophyly of Corallobothriinae and to investigate the interrelationships of the North American species. The results indicate that Corallobothriinae, as conventionally understood, is not monophyletic and that only the North American corallobothriines, parasites of ictalurid catfishes, form a monophyletic group. Corallobothrium parafimbriatum is sister taxon to a clade that includes Corallotaenia intermedia and C. minutia and not to its congener C. fimbriatum. Also, M. giganteum from Mexico appears to be more closely related to M. lamothei than to its conspecific in Canada. This and the amount of sequence divergence indicate possible cryptic speciation in its endemic host, the Lerma catfish, Ictalurus dugesi.

Phylogeny and biogeography of Rhabdochona Railliet, 1916 (Nematoda: Rhabdochonidae) species from the Americas

A phylogenetic analysis of 40 species of Rhabdochona Railliet, 1916, including all 21 valid species in the Americas, resulted in 1733 equally most parsimonious trees and indicates that Rhabdochona is arguably monophyletic. Species from the Americas do not form a monophyletic group, since each of the six clades of Rhabdochona includes species from the Americas and species from other continents. The synapomorphies defining each clade stem from the morphology of the left spicule. Teeth number was consistent in one clade only, suggesting that this␣character, while useful for taxonomic purposes, is not indicative of phylogeny. Species of Rhabdochona associated with certain host groups, such as salmonids, catostomids and goodeids, do not always form monophyletic assemblages, nor do species associated with smaller discrete areas, such as the Mesa Central of Mexico. This indicates widespread host-switching rather than co-speciation as the main phenomenon in the evolution of this group, at least in the species from the Americas. Phylogenetic patterns reveal an ancient origin for the group that probably pre-dates current continental configurations.

Parasitism and body condition in humpback chub from the Colorado and little Colorado Rivers, Grand Canyon, Arizona

Abstract Glen Canyon Dam has greatly altered the Colorado River in Grand Canyon. The Little Colorado River (LCR) provides a small refuge of seasonally warm and turbid water that is thought to be more suitable than the Colorado River for endangered humpback chub Gila cypha. However, the LCR has low productivity and contains nonnative fishes and parasites, which pose a threat to humpback chub. The Colorado River hosts a different suite of nonnative fishes and is cold and clear but more productive. We compared condition factor (K), abdominal fat index (AFI), and presence and number of two introduced pathogenic parasites (Lernaea cyprinacea and Bothriocephalus acheilognathi) between juvenile (<150 mm total length) humpback chub from the LCR and those from the Colorado River during 1996–1999. Both K and AFI were lower and L. cyprinacea prevalence and B. acheilognathi prevalence were higher in LCR fish than in Colorado River fish for all years. Mean K and AFI were 0.622 and 0.48, respectively, in the LCR and 0....