Cryptic speciation and patterns of phenotypic variation of a highly variable acanthocephalan parasite.

An investigation of a parasite species that is broadly host- and habitat-specific and exhibits alternative transmission strategies was undertaken to examine intraspecific variability and if it can be attributed to cryptic speciation or environmentally induced plasticity. Specimens of an acanthocephalan parasite, Leptorhynchoides thecatus, collected throughout North America were analysed phylogenetically using sequences of the cytochrome oxidase I gene and the internal transcribed spacer region. Variation in host use, habitat use, and transmission were examined in a phylogenetic context to determine if they were more likely phylogenetically based or due to environmental influences. Results indicated that most of the variation detected can be explained by the presence of cryptic species. The majority of these species have narrow host and microhabitat specificities although one species, which also may comprise a complex of species, exhibits broad host and habitat specificity. Alternate transmission pathways only occurred in two of the cryptic species and correlate with host use patterns. Taxa that mature in piscivorous piscine hosts use a paratenic fish host to bridge the trophic gap between their amphipod intermediate host and piscivorous definitive host. One potential example of environmentally induced variation was identified in three populations of these parasites, which differ on their abilities to infect different host species.

A comparison of biological performances among a laboratory-isolated population and two wild populations of Moniliformis moniliformis.

Divergence of biological performance of a laboratory-reared population of Moniliformis moniliformis (Acanthocephala) was investigated after 31 yr, or approximately 60 generations, of genetic isolation. An isolate of the laboratory-reared population and isolates of 2 wild populations were used to begin 3 independent life cycles that were maintained for 1 generation for interbreeding and life history trait comparison. Both wild population isolates represented populations with open gene flow. One wild population isolate represented a present-day sample of descendants of the parent population of the laboratory isolate. All 3 populations hybridized, and egg production occurred in all mixed-sex pairs of different populations. The 3 populations did not differ significantly in prepatent period, mean daily egg production, or establishment within the definitive host Rattus norvegicus. The 3 populations varied in patent period, but the laboratory-isolated worms differed from the 2 wild population isolates no more than they did from each other. A positive correlation between mean daily egg production and duration of patent period resulted in different cumulative egg productions. A 31-yr period of isolation did not produce greater divergence in a laboratory population of M. moniliformis than occurs between wild populations with respect to the biological parameters measured.

Experimental investigation of physiological factors that may influence microhabitat specificity exhibited by Leptorhynchoides thecatus (Acanthocephala) in green sunfish (Lepomis cyanellus).

Representatives of Leptorhynchoides thecatus (Acanthocephala) inhabit ceca of green sunfish but cannot survive in the anterior intestine. The influence of elevated cecal protein concentrations, pH, and amounts of lumenal materials on the microhabitat specificity of L. thecatus was investigated. An attempt was made to alter the distribution of worms in starved fish, in fish of which cecal pH was reduced, and in fish of which intestinal protein concentration was elevated. Protein concentration and pH showed no effect on worm distribution. Starving hosts had no effect on worm number or distribution but resulted in retardation of worm growth and development, providing a mechanism by which worms may overwinter and by which peak egg production may coincide with abundance of the amphipod intermediate host. None of the factors investigated is solely responsible for the microhabitat specificity of L. thecatus. It is suggested that helminth site specificity is characterized by long histories of adaptation to specific habitats with many physiological adaptations being facilitated synergistically. Maximization of sexual congress may exert an important selective pressure favoring this establishment of microhabitat specificity.

Reintroduction of Profilicollis Meyer, 1931, as a genus in acenthocephala: significance of the intermediate host.

Polymorphid acanthocephalans with long necks, spheroid proboscides, and eggs without polar swellings of the fertilization membrane constitute a morphologically distinct group of species. In the past, this taxon was considered a separate genus, Profilicollis. More recently, workers have been unwilling to accept these features as generic-level characters, and presently the group is considered a subgenus of Polymorphus. An analysis prompted by our studies of various polymorphid cystacanths in crabs along the coasts of Scotland and the U.S.A. reveals that all records of Polymorphus in decapods refer to species with 6 cement glands frequently assigned to Hexaglandula, to incidental occurrences of species purported to be Polymorphus minutus, or to species of the subgenus Profilicollis. Occurrence in decapod crustaceans implies substantial life history differences from the other species of the genus occurring in amphipod crustaceans. We conclude this, together with morphological distinctiveness, justifies return of Profilicollis to full generic status within Polymorphidae.

Effects of coinfection with Pomphorhynchus bulbocolli on development of leptorhynchoides thecatus (Acanthocephala) in amphipods (Hyalella azteca).

The effect of the presence of Pomphorhynchus bulbocolli on the development of Leptorhynchoides thecatus (Acanthocephala) in amphipod intermediate hosts (Hyalella azteca) was examined. Two groups of amphipods were exposed either to eggs of both species (experimental) or only to L. thecatus eggs (control). Amphipods of both groups were dissected 39 days postexposure. The percentage of L. thecatus at the cystacanth stage and mean abundance of cystacanths and precystacanths per amphipod were determined. Contingency table analysis and Fisher's exact tests demonstrated that a significantly smaller proportion of L. thecatus reached the cystacanth stage in coinfected amphipods of the experimental group than either worms in the control group or worms in L. thecatus-only infections of the experimental group. Interspecific interaction between acanthocephalans in intermediate hosts has not been reported previously. Coinfection reduces the number of L. thecatus in amphipods available for transmission to definitive hosts. Habitat separation by eggs of L. thecatus and P. bulbocolli might reduce this effect if amphipods are less likely to become coinfected when eggs are in different microhabitats than when they are not.

Structure of Leptorhynchoides thecatus and Pomphorhynchus bulbocolli (Acanthocephala) eggs in habitat partitioning and transmission.

The role of egg structure in transmission and habitat use of Leptorhynchoides thecatus and Pomphorhynchus bulbocolli (Acanthocephala) was investigated. During storage in tap water at 4 C, the outer membrane of L. thecatus eggs was lost, releasing ribbonlike filaments of the fibrillar coat. After similar storage, the outer membrane and fibrillar coat of P. bulbocolli eggs remained intact. Eggs of L. thecatus entangled in algae, whereas those of P. bulbocolli settled to the substratum. Leptorhynchoides thecatus infections in amphipod intermediate hosts were significantly more prevalent and dense when eggs were allowed to entangle than when they were not. Prevalence and relative density of P. bulbocolli infections in amphipods were not significantly different between trials in which entanglement was possible and those in which it was not. These results indicate that although the same species of amphipod, Hyalella azteca, is the intermediate host for both acanthocephalan species, mechanisms of transmission differ. Differences in fibrillar coats result in segregation of the environment in a manner that affects transmission and occurrence in intermediate hosts.

Copulation and sexual congress of Leptorhynchoides thecatus (Acanthocephala).

Pairs of the acanthocephalan Leptorhynchoides thecatus from laboratory infections were observed copulating at 21 days, 5 wk, and 12 wk postinfection (PI) in green sunfish, Lepomis cyanellus. Additionally, copulating pairs of worms from natural infections were observed. In each instance of paired males and females, the male was in 1 pyloric cecum of the fish and the female in another. Each had its posterior end protruding into the intestinal lumen at the point from which the ceca arise. The completely extruded bursa of the male fully enclosed the posterior end of the female in a firm attachment. In 1 instance at 5 wk PI, 2 males were observed in copula. One male had its copulatory bursa completely retracted, and the copulatory bursa of the other male was positioned just as though the mate were a female. Based on these and previous findings, it is concluded that male acanthocephalans mate indiscriminately and often throughout their lives. Habitation of ceca maximizes sexual congress because individuals often are positioned with their posterior ends extending into the intestinal lumen within the small area from which ceca originate. Emigration to find a mate is unnecessary.

Comparison of Leptorhynchoides thecatus (Acanthocephala) recruitment into green sunfish and largemouth bass populations.

The degree to which host suitability is a reflection of host community structure in generalist parasites was studied experimentally in the common fish acanthocephalan Leptorhynchoides thecatus. Previous study has shown that green sunfish (Lepomis cyanellus) are required, and largemouth bass (Micropterus salmoides) are suitable (but not required) hosts, where they occur sympatrically in natural communities. The present study examined populations of L. cyanellus and M. salmoides held separately in mesocosms and exposed to L. thecatus cystacanths via laboratory-infected Hyalella azteca (Amphipoda). Recruitment, maturation, and transmission of worms were examined over a 17-wk period and compared between fish species. Infections with L. thecatus were found as early as 2 wk after the introduction of cystacanth-infected amphipods, and by week 11 fishes of both species harbored gravid worms. Immature worms were observed in both host species by week 17 and were presumed to be a result of natural egg production and release resulting in infections of amphipods and the subsequent reinfection of fish. No significant difference in the prevalence, abundance, percentage of worms gravid, or time of parasite maturation was found between host populations. Results indicate that the different roles played by these host species in the maintenance of L. thecatus supra-populations in natural systems are not due to intrinsic factors but rather to differences in host autecology and community structure.

The genus Centrorhynchus (Acanthocephala) in North America with description of Centrorhynchus robustus n. sp., redescription of Centrorhynchus conspectus, and a key to species.

Reexamination of the type series of Centrorhynchus wardae Holloway, 1958, and Centrorhynchus conspectus Van Cleave and Pratt, 1940, revealed no consistent difference between the 2 purported species; therefore, C. wardae is considered a junior synonym of C. conspectus. Specimens from additional collections are consistent with this view and provided adequate material for redescription of the species. Centrorhynchus robustus n. sp. resembles C. conspectus in the number of hooks per Salient differences between the 2 species are size and body shape, with C. robustus having a robust trunk with the widest diameter anteriad and C. conspectus being elongate with no region of the trunk consistently widest. Additionally, a conspicuous posteriad swelling exhibited by females of C. conspectus is lacking in C. robustus. Centrorhynchus kuntzi is reported for the first time from Montana and Nebraska, and C. conspectus is reported for the first time from an eastern screech owl, Otus asio.

Establishment, survival, site selection and development of Leptorhynchoides thecatus in largemouth bass, Micropterus salmoides.

Establishment, survival and distribution of Leptorhynchoides thecatus (Acanthocephala) were investigated in largemouth bass, Micropterus salmoides, fed 10, 25, or 40 cystacanths and examined at 1, 3 or 5 weeks post-infection. Worms established widely in the alimentary tracts of bass but by 5 weeks post-infection had localized in the pyloric caeca and intercaecal region. Other individuals moved to parenteral sites where they remained immature, though viable. In the 10- and 25-level exposures, establishment and survivorship in the alimentary tract were roughly proportional to the dose of cystacanths. After 1 week post-infection in the 40-level exposure class, numbers of worms in the alimentary tract decreased significantly and parenteral occurrence increased significantly. Total survival of L. thecatus appeared to be density-independent. Maturation of worms was retarded temporarily as intensity of infection increased, but by 5 weeks post-infection worms from all doses were at roughly the same stage of development within sex. The caeca and intercaecal area apparently did not differ in their suitability for maturation.

Effects of Plagiorhynchus cylindraceus (Acanthocephala) on the energy metabolism of adult starlings, Sturnus vulgaris.

Although the relationship between intestinal parasitism, the ingestion and use of energy, and host survival is expected, little work has been done to outline the effect of such organisms upon their host's nutritional requirements in an ecological context. This study is the first to demonstrate that an intestinal helminth previously reported to be of little or no histopathological consequence, Plagiorhynchus cylindraceus, has a significant detrimental impact upon the flow of food energy through a definitive host, the European starling, Sturnus vulgaris. Within both male and female adult European starlings reductions in standard metabolic rates occurred as the result of initial infection, indicating that the host's basal metabolism/thermal regulatory abilities were altered. Moreover, initially infected male starlings, but not females, had an increased consumption and excretion of energy and maintained lower average daily body weights versus controls when temperature stressed. These results appear to be due to either a parasite-mediated alteration in host activity and/or to the disruption of host-digestive abilities. Additionally, these data indicate that, overall, male and female S. vulgaris respond differently to infection and that intestinal helminths normally thought to be of little or no pathological consequence to the host are factors that should be addressed in future studies regarding animal energetics, ecology, and behaviour.

Effect of Moniliformis moniliformis density on distribution within the definitive host population (Rattus norvegicus).

The population dynamics of Moniliformis moniliformis was studied in 'free-ranging' laboratory rats, Rattus norvegicus, presented with different relative density levels of M. moniliformis in cockroaches, Periplaneta americana. Changes in selected population parameters of the negative binomial distribution were evaluated as indicators of changes in aggregation. A significant increase in the degree of aggregation of parasites occurred as a result of the increase in relative density of infective stages available to the rats. This increase in aggregation was due to the increase in over-dispersion that occurred in female rats only. The degree of aggregation in females was found to be significantly higher than that in males at both treatment levels. The best indicators of the degree of aggregation were found to be the ratio of the variance to the relative density and the ratio of the log-variance to log-relative density. Changes in k were not correlated with changes in over-dispersion or the relative density.

Availability of caecal habitat as a density-dependent limit on survivorship of Leptorhynchoides thecatus in green sunfish, Lepomis cyanellus.

Distribution of Leptorhynchoides thecatus (Acanthocephala: Rhadinorhynchidae) among the pyloric caeca and the relationship between site and rate of maturation were studied in laboratory infections of 10, 25 and 40 cystacanths fed to green sunfish, Lepomis cyanellus. After 1 week fish fed at each intensity had significantly different numbers of worms. By the 3rd week post-infection, parasites disappeared from the anterior portion of the intestine. At this time the mean numbers of worms recovered from 25 and 40-cystacanth infections were not significantly different. At the end of the 1st week, the area where caeca join the alimentary tract (between caecal area) and caeca numbered 6 and 7 contained significantly more worms than the other sites. By the 3rd week post-infection only caecum 7 contained significantly more worms, and at 5 weeks there was no significant difference between the number of worms present in any caecum or the between caecal area. Initially worms in the more intense infections matured more slowly, but by the 3rd week post-infection there was no significant difference in the states of maturity. The rate of maturation was not related to the site occupied.

Survival of Macracanthorhynchus ingens in swine and histopathology of infection in swine and raccoons.

Animal husbandry aimed at preventing Macracanthorhynchus hirudinaceus infections in swine is not successful in preventing exposure to Macracanthorhynchus ingens, and it is probable that pigs occasionally acquire acanthocephalans of that species. In some pigs, M. ingens survived 2 weeks and grew several millimeters. In such cases, destruction of villi, erosion of epithelium, leukocytic infiltration, and altered cytological structure at attachment sites accompanied the infection. Penetration was limited to the submucosa, and the effects were not as severe as those occurring in the presence of M. hirudinaceus, which enters the muscularis.

Geographic and host-related variation among species of Fessisentis (Acanthocephala) and confirmation of the Fessisentis fessus life cycle.

Specimens of the 4 known species of Fessisentis, acquired through new collections in 6 states and laboratory infections, were compared with existing descriptions and collections. It was concluded that the number od longitudinal rows of proboscis hooks and lengths of proboscis receptacles, largest proboscis hooks, and reproductive systems are not useful in distinguishing the species. Egg size is of limited usefulness. Regardless of host or geographical locality, proboscis shape and length, the number of proboscis hooks in each longitudinal row, hook shape and size distribution, number of testes, number of cement glands, and female genital pore position are consistent differences. Cystacanths of Fessisentis fessus occurred in aquatic isopods, Asellus forbesi and Lirceus lineatus, in Jackson County, Illinois, where Siren intermedia is the usual definitive host. Laboratory infections confirmed the life cycle of this species.

Life history and host specificity of Mediorhynchus centurorum Nickol 1969 (Acanthocephala: Gigantorhynchidae).

Examination of 1905 arthropods from a swamp and surrounding pasture in sothern Louisiana revealed larval specimens of Mediorhynchus centurorum in 8 of 228 woodroaches, Parcoblatta pensylvanica, but in no other species. The life cycle was confirmed by feeding eggs of M. centurorum to laboratory-reared woodroaches. Cystacanths later recovered from the woodroaches developed into mature worms when pipetted into esophaguses of red-bellied woodpeckers, Centurus carolinius: red-headed woodpeckers, Melanerpes erythrocephalus; yellow-shafted flickers, Colaptes auratus; and a hairy woodpecker, Dendrocopos villosus. Infection was achieved in all woodpeckers fed cystacanths at least 47 days old and the mean prepatent period was 35 days. Cystacanths fed starlings, Sturnus vaulgaris, and red-winged blackbirds, Agelaius phoeniceus, did not produce infections although cystacanths from the same pool were infective to control woodpeckers. Larval development of Mediorhynchus centurorum in woodroaches did not differ significantly from that of M. grandis in grasshoppers. M. centurorum is the only species of the Gigantorhynchidae for which the life cycle has been confirmed by laboratory infections using an intermediate host species known infected nature.

Structure and function of the fibrillar coat of Leptorhynchoides thecatus eggs.

Leptorhynchoides thecatus eggs in fish feces were discovered to lack a thin, outer membrane present on eggs removed from body cavities of freashly collected worms; and to possess external structures which, with a light microscope, appeared as numerous fibrils. Scanning electron microscopy revealed to fibrils to be portions of a broad band of unwound fibrillar coat exposed after loss of the outer membrane. Fibrillar bands can entabgle in filamentous algae, anchoring eggs at the feeding sites of amphipod intermediate hosts. Amphipods fed in containers of algae over which eggs with exposed fibrillar bands had been added developed a significantly greater prevalence and intensity of acanthocephalan infection than did those fed in containers to which eggs had been added before the algae.