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Biomedical subjects

R C Tinsley

Publications and source records attributed to R C Tinsley.

At least 19 recordsLinked to original sources

Effects of environmental temperature on the susceptibility of Xenopus laevis and X. wittei (Anura) to Protopolystoma xenopodis(Monogenea).

Immune responses in ectothermic vertebrates and the life-processes of their parasites are profoundly linked to ambient temperature, but the functional effect of thermal environment on infectivity and host-specificity in helminths from ectotherms is poorly known. Primary infection establishment of Protopolystoma xenopodis (Monogenea) in compatible hosts ( Xenopus laevis: Anura) is strongly modulated by ambient temperature. Significantly fewer worms survived to the urinary bladder stage at 25 degrees C than at 15 degrees C (relatively high and low temperatures for this system in nature). Pre-infection exposure of X. laevis to cold (10 degrees C) did not significantly affect parasite establishment in the urinary bladder (at 15 or 25 degrees C p.i.), nor shorter-term postlarval survival in the kidneys (at 20 degrees C p.i.), suggesting that residual immunosuppressive effects on host susceptibility are not important. Low temperatures had no permissive effect on the establishment of P. xenopodis in incompatible hosts (Xenopus wittei). The link between thermal conditions and parasitic infection of ectotherms is discussed.

Animals↗

Host factors limiting monogenean infections: a case study.

Comprehensive field data on polystomatid monogeneans record low prevalence and intensity of infection and suggest that worm burdens in this group are strongly regulated: thus, in the majority of Polystoma species infecting anuran amphibians mean abundance is typically less than one parasite/host. There is circumstantial evidence that the dominant control is attributable to host factors which over-ride variations in transmission success. This review provides a brief summary of information on Pseudodiplorchis americanus, a parasite of the desert toad, Scaphiopus couchii, and then focuses in detail on the spectrum of factors regulating infrapopulations of Protopolystoma xenopodis, a parasite of the aquatic Xenopus laevis. Infection levels of adult worms and their contribution to transmission are regulated by external environmental factors (especially temperature), by host factors (including behaviour and population density), and by a range of parasite factors including intra- and inter-specific competitive interactions and variations in intrinsic characters, especially survivorship and reproductive output. In addition to these factors whose primary effect is to modulate transmission rates, there is a major attrition in parasite numbers between invasion and maturity (3 months post-infection). Long-term laboratory experiments on the Xenopus laevis/Protopolystoma xenopodis interaction demonstrate a powerful acquired immune response. Primary infection is characterised by a high prevalence of established adult worms but the success of subsequent challenge infection is greatly reduced, leading to low prevalence and extended pre-patent period. In the small proportion of hosts supporting a second infection of adult parasites, surviving burdens are small (one to two worms/host) and show reduced egg production. These results provide an explanation for the low burdens encountered in field studies: a majority of adult X. laevis in natural populations are likely to exhibit strong, relatively long-term, post-infection immunity after the loss of a previous infection.

Amphibians↗

Survival, feeding and embryo development of Gyrodactylus gasterostei (Monogenea: Gyrodactylidae).

Viviparous gyrodactylid monogeneans which are detached from their host may form an important source of infection in fish communities. This is particularly significant for these ectoparasites which have no specific free-living stage and where transmission usually occurs through transfer of adult parasites when fish come into close contact. In this study, in vitro survival of Gyrodactylus gasterostei was correlated with changes in tissue ultrastructure of parents and their embryos during detachment and following return to a host. At 10 degrees C, detached worms survived for up to 89 h (50%) survival = 20 h) with mortality influenced by both age-independent and age-dependent factors. The gastrodermis of attached, fed parasites is syncytial and contains a variety of vesicles and feeding vacuoles. However, following detachment and starvation, degenerative changes occur within the gastrodermis, eventually leading to marked damage to the embryo/s. When starved worms reattached to a fish, they began browsing on host epithelial cells within 1 min and ultrastructural evidence for phagocytic activity in the gastrodermis was detected after 5 min. Putative waste vacuoles increased in abundance after 5-30 min on the new host, coinciding with the reappearance of electron-dense vesicles and possibly indicating completion of the first intracellular cycle of digestion. Parental feeding directly influenced the normal cyclical maturation and regression of the uterine lining between births. In extreme cases, starvation led to detached parasites (6.1%) aborting their embryos. However, even short periods off the host influenced development and survival of embryos, suggesting that temporary interruption of nutrient flow to the embryo can significantly affect gyrodactylid reproductive rates.

Animals↗

Pathological effects of Pseudodiplorchis americanus (Monogenea: Polystomatidae) on the lung epithelium of its host, Scaphiopus couchii.

Infection of the desert toad, Scaphiopus couchii, by the monogenean Pseudodiplorchis americanus involves 2 principal sites: post-invasion juveniles reside in the respiratory tract for 1 month before migrating to the urinary bladder where they reach sexual maturity and may live up to 4 years. While previous work has demonstrated the long-term impact on host condition of the blood-feeding adults, this study assesses pathological effects of the short-term pulmonary infection. Lung ultrastructure was compared in toads (i) maintained in captivity for 1 year without invasion, and (ii) experimentally infected with 50-300 juveniles/host, equivalent to burdens in the wild, and examined 23-44 days p.i. Typically, the alveolar lining of S. couchii is composed of a single cell type with characteristics of both Type I and Type II pneumocytes. However, infected lung tissue exhibited an inflammatory reaction with epithelial cell vacuolation, interstitial oedema, and an increase of alveolar exudate, leucocytes and fibrous tissue. Accompanying a post-infection increase in host immune cells in the lungs, there was evidence of reciprocal tegumental damage to the parasites. Lung epithelium of toads free of infection for 1 year exhibited scar tissue representing a residual effect of past infection. The pathological consequences of P. americanus infection therefore have 2 components. Acute lung infection coincides with the host's brief activity season: impaired respiratory function could compromise feeding and accumulation of reserves and hence ability to survive following a 10 month period of hibernation. Additionally, adult toads are normally exposed annually to re-infection and may accumulate chronic lung damage with extended effects on host survival.

Animals↗

Behavior favoring transmission in the viviparous monogenean Gyrodactylus turnbulli.

Transmission by Gyrodactylus turnbulli occurs most frequently when its hosts (Poecilia reticulata) come into close contact. This study is the first description of a specific migratory behavior that facilitates transmission of a gyrodactylid from dead hosts. Recently-dead guppies typically float at the water's surface; G. turnbulli moves off these fish into the water film, hanging motionless with the haptor held by surface tension. Because guppies are surface feeders, detached parasites in the water film are more likely to contact a new host.

Animals↗

Differentiation of two locally sympatric Protopolystoma (Monogenea: Polystomatidae) species by temperature-dependent larval development and survival.

The developmental response of egg stages to different environmental temperature regimes was studied in Protopolystoma xenopodis and Protopolystoma orientalis (Monogenea: Polystomatidae) isolates from southern Africa. Eggs failed to develop at 10 degrees C, whilst at 15 degrees C only P. xenopodis completed larval development, hatching 49--88 days post-collection. Respective hatching windows were 26--34 (P. xenopodis) and 37--49 (P. orientalis) days at 20 degrees C, and 18--26 and 27--37 days at 25 degrees C. Continuous maintenance at 30 degrees C was lethal for eggs of both species. There were no consistent interspecific differences in the response of egg stages to low and high temperature shocks during early embryonic development.

Africa, Southern↗

Protopolystoma xenopodis (Monogenea) primary and secondary infections in Xenopus laevis.

The reproductive kinetics of Protopolystoma xenopodis primary and secondary infections in Xenopus laevis were monitored in a 3-year study. Thirty-five naïve, lab-raised, full-sib X. laevis from 1 spawning were each exposed to 30 P. xenopodis eggs. The course of infections at 20 degrees C was monitored by screening isolated hosts for parasite egg production. Ninety-four percent of toads supported the development of gravid parasites. Infections became patent 9-19 weeks p.i., lasted 3-30 months and produced estimated totals of 1-7152 eggs/host. Variation in primary infection characters was discontinuous: a subgrouping of hosts (16%) was characterized by extended infection duration and low reproductive rate. In order to test the effect of long-term infection history on a subsequent challenge, each host was re-exposed to P. xenopodis infective stages (30 eggs/host) 6 months after the loss of its original infection. Establishment of patent infection was significantly lower (15%), and pre-patent period (12-28 weeks) longer, than in primary infections of the same hosts, and than in concurrently exposed naïve controls (contemporary full-sibs of the primary/secondary infection group, maintained in parallel; n = 28). There was no relationship between primary infection characteristics and secondary infection outcome. Overall reproductive output per initial infective stage for the primary exposure exceeded that for the secondary exposure by a ratio of 15:1. Results suggest that primary infection with P. xenopodis can elicit strong, long-term protective immunity against re-infection in X. laevis.

Animals↗

A redescription of Chabaudus leberrei (Bain & Philippon, 1969) (Nematoda: Seuratoidea) from Xenopus spp. in Swaziland.

Chabaudus leberrei (Bain & Philippon, 1969) is redescribed from the pipid anurans Xenopus muelleri (Peters) and X. laevis laevis (Daudin) (new host records) in northern Swaziland, based on light and scanning electron microscope studies. The six anterior protuberances characteristic of the genus Chabaudus Inglis & Ogden, 1965, are, in C. leberrei, formed by bipartite lamellae associated with the internal margins of the three lips. Intraspecific variation in the number and disposition of male caudal papillae and in the development of the cephalic vesicle is documented.

Animals↗

Ultrastructure of spermiogenesis and spermatozoa of Discocotyle sagittata (Monogenea: Polyopisthocotylea: Discocotylinea).

Ultrastructural analysis revealed that the spermatozoon of Discocotyle sagittata (Leuckart, 1842) is composed of two parallel axonemes, mitochondrion, nucleus and cortical microtubules. The nucleus, which occupies a central/distal position and has an unusual crescent-shaped profile, is slightly shorter than the mitochondrial rod. The two axonemes, which are of unequal length, and the cortical microtubules (up to 68 forming a continuous ring in the principal region) extend almost the entire length of the spermatozoon. A fold of the plasma membrane creates a unilateral flange or undulating membrane. Epifluorescence microscopy indicated that spermatogenesis gives rise to clusters of 64 spermatids connected to a common cytophore. Spermiogenesis and the structure of the filiform sperm of D. sagittata conform to the typical polyopisthocotylean pattern.

Animals↗

Combined ribosomal DNA and morphological analysis of individual gyrodactylid monogeneans.

A method is presented for the isolation and analysis of hamuli, marginal hooks, and bars from individual gyrodactylid monogeneans using scanning electron microscopy (SEM), while simultaneously processing parasites for rDNA analysis using the polymerase chain reaction (PCR). The haptors of ethanol-fixed gyrodactylids were protease digested to liberate hooks for SEM, whereas DNA extracted from the bodies was used for PCR. The method resulted in hooks and hamuli being prepared from more than 90% of Gyrodactylus turnbulli individuals, a significant improvement on previously published digestion-based SEM techniques. PCR on the same parasites was less successful, but sequence data were obtained from 50% of individuals. Amplification of rDNA internal-transcribed spacer regions from individual worms used for SEM gave PCR products consistent with those predicted from our previous sequence analysis. This method allows the correlation of morphology and DNA sequence from the same individual and can be applied to ethanol-fixed material, such as field collected and museum specimens.

Animals↗

Parasite adaptation to extreme conditions in a desert environment.

Deserts represent universally recognized extreme environments for animal life. This paper documents the highly specialized adaptations of Pseudodiplorchis americanus, a monogenean parasite of the desert toad, Scaphiopus couchii. Building on a long-term record of parasite population ecology (continuing since the early 1980s), field studies focus on the effects of severe drought in the Sonoran Desert, Arizona, in the mid 1990s. This provides a test of the ability of the host-parasite system to tolerate exceptional perturbation. The analysis provides new insight into parasite infection dynamics in a natural wildlife system through integration of host and parasite population age structure. The environmental check interrupted host recruitment in 1993-95 and parasite recruitment in 1995-97. This produced an imprint in age structure and infection levels recognizable over several years: parasite recruitment failure reduced transmission 2-3 years later. The host (maximum life span 17 years) tolerated the disruption but the impact was more serious for the parasite (life span 3 years) leading to extinction of some previously stable populations. Despite this demonstration of a rare event exacerbating external environmental constraints, experimental studies suggest that the internal (host) environment normally creates the most severe conditions affecting P. americanus. Only about 3% of parasites survive from invasion until first reproduction. Post-invasion factors including host immunity, characteristic of most parasite life cycles, constitute a greater constraint upon survival than external conditions, even in a desert environment.

Adaptation, Physiological↗

Life history specializations of monogenean flatworms: a review of experimental and microscopical studies.

This review illustrates the use of experimental approaches combined with microscopy to study the biology of monogenean parasites. Studies of feeding, development, reproduction, and systematics have been based on gyrodactylids, flatworms infecting teleost fishes. In a contrasting system involving an amphibian host in a desert environment, analysis of adaptations to extreme conditions has focused on Pseudodiplorchis americanus. The unusual reproductive strategies, particularly the interactions between mother and offspring, are highlighted for both monogeneans. Species of Gyrodactylus are viviparous, maintaining up to three generations of embryos simultaneously in utero, and many of their reproductive specializations are related to progenesis. Embryo nutrition takes place via a metabolically-active syncytial uterine lining that has close association with the parental gut. Microscopy has also proved an essential adjunct to molecular studies of speciation and host specificity. P. americanus is ovoviviparous and the adaptations for embryo maintenance are unique. The primary keratin-type eggshell is replaced by a flexible secondary elastin capsule produced by the uterus; parental nutrients are transferred through cytoplasmic connections to the developing embryo. TEM has demonstrated unique adaptations of P. americanus to its micro-environments, including secretion of tegumental vesicles that provide protection from digestive enzymes during migration through the host gut. This paper highlights the potential of monogeneans for studies of fundamental biological principles.

Animals↗

Effects of temperature on oviposition rate in Protopolystoma xenopodis (Monogenea: Polystomatidae).

Protopolystoma xenopodis is an oviparous monogenean occurring as an adult in the urinary bladder of the African clawed toad, Xenopus laevis. Egg production was monitored in two groups of infected hosts exposed to decreasing environmental temperatures. Despite possible upward trends in reproductive capacity with parasite age, oviposition rate was severely depressed at lower temperatures. In one experiment, egg production was monitored in a sample of seven hosts at 2 degrees C intervals between 20 and 8 degrees C. Overall mean egg production rate showed a consistent decline from 11.9 eggs/worm/day (e/w/d) at 20 degrees C (days 1-10) to 0.9 e/w/d at 8 degrees C (days 115-124). In a second experiment (n = 11 hosts) oviposition rate was recorded at the same intervals between 20 and 6 degrees C and then hosts were returned to 20 degrees C. Overall mean egg production rate decreased consistently from 4.1 e/w/d at 20 degrees C (days 1-10) to 0.2 e/w/d at 6 degrees C (days 124-131), at which temperature all infections continued to produce eggs. When parasites were then returned to 20 degrees C (141-150 days), mean oviposition rate at this temperature (12.7 e/w/d) was found to have increased by 310% from the start of the experiment (130 days earlier) and by 6350% from production at 6 degrees C (9 days earlier). P. xenopodis has been introduced to South Wales, U.K. and present results show that it could produce eggs here through almost all of the year. However, a massive annual reduction in the reproductive output of this parasite in the U.K., compared with that in natural sites, is predicted.

Age Factors↗

Incompatibility of Protopolystoma xenopodis (Monogenea: Polystomatidae) with an octoploid Xenopus species from southern Rwanda.

Protopolystoma xenopodis is an oviparous monogenean occurring as an adult in the urinary bladder of the clawed toad Xenopus laevis. Oncomiracidia invade the host's kidneys where juveniles develop, subsequently migrating to the definitive site. In central Africa, the tetraploid X. laevis occurs in sympatry with octoploid congeners, including Xenopus wittei, believed to be the hybrid derivatives of X. laevis- and Xenopus fraseri-like parental lineages. Twenty laboratory-raised, naive specimens of an X. wittei-like species from southern Rwanda were each exposed to 30 embryonated P. xenopodis eggs (at 20 degrees C) and screened for parasite egg production until 9 months post-exposure. These toads failed to support the development of gravid parasites (comparable experimental procedures produce at least 35% prevalence of patent infection in the natural host X. laevis). Further X. wittei aff. (n = 26) and X. laevis (n = 17) were exposed to P. xenopodis oncomiracidia and dissected at variable times post-exposure: larvae were able to invade the kidneys of X. wittei aff. and began feeding and morphological development. Severe mortality of juveniles occurred in both natural and unnatural hosts between invasion and 39 days post-exposure. However, while small numbers of parasites persisted in X. laevis, no stages were found in X. wittei aff. beyond 39 days. Present data demonstrate the incompatibility of P. xenopodis with X. wittei aff. and are consistent with a hypothesis that specificity in Protopolystoma-Xenopus systems is determined primarily by the ability of juveniles to complete development in the host's kidneys.

Animals↗

Reproductive interference in concurrent infections of two Protopolystoma species (Monogenea: Polystomatidae).

The prevention of interspecific reproductive interference is one possible explanation for spatial niche divergence between congeneric monogeneans. However, there is little direct evidence that reproductive interactions with other species are potentially deleterious to the majority of parasitic platyhelminths. Xenopus fraseri-like clawed toads from lowland rainforest in eastern Democratic Republic of Congo are infected by two species of polystomatid monogenean, Protopolystoma fissilis and Protopolystoma ramulosus. Both occur as adults in the host urinary bladder, and exhibit identical copulatory structures and similar body sizes. The small area of the habitat in relation to parasite body size makes close proximity inevitable in concurrent infections. Eggs were collected from five naturally infected hosts: two of these harboured concurrent infections, and three were infected with P. fissilis only. Eggs from concurrent infections showed reduced viability (57.6% embryonation, n = 413) compared with those from P. fissilis-only infections (85.2%, n = 439). This effect may be due to some form of reproductive interference, possibly failure to develop following interspecific cross-fertilisation.

Animals↗

Correlation of parasite speciation and specificity with host evolutionary relationships.

Protopolystoma (Monogenea, Polystomatidae) is strictly specific to the anuran amphibian genus Xenopus. The host group is characterised by a polyploid series in which chromosome numbers reflect diploid, tetraploid, octoploid and dodecaploid constitutions; the series is considered to have evolved through interspecies hybridisation and genome duplication. This study correlates information on host evolutionary relationships with patterns of parasite speciation and host specificity. Protopolystoma is restricted to one subgenus (Xenopus) with multiples of 36 chromosomes, and is absent from the subgenus Silurana (with multiples of 20 chromosomes). Molecular, biochemical and karyotype evidence distinguishes three subgroups within Xenopus. Representative species from each subgroup, Xenopus muelleri, Xenopus fraseri and Xenopus laevis, have been examined for polystomatid infection. Two species of Protopolystoma occur in each of these host species. In X. muelleri, the two Protopolystoma species reflect parasite co-speciation corresponding with the divergence of two sibling host species. Xenopus fraseri and X. laevis (both with 2n = 36 chromosomes) are implicated in the hybrid origin of two octoploid species, Xenopus wittei and Xenopus vestitus (both 2n = 72). The relationships of the Protopolystoma species in these Xenopus taxa reflect this presumed ancestry. Xenopus wittei carries two species of Protopolystoma, one shared with X. fraseri and the other shared with X. laevis. Xenopus vestitus carries a single species of Protopolystoma which is shared with X. laevis but there is no "heirloom" which reflects its hybrid origin involving X. fraseri. In addition to these shared parasite species which may reflect shared host genes, X. fraseri and X. laevis each carry separate species-specific Protopolystoma which do not occur in other Xenopus species even where there is evidence of common genetic information (as in the allopolyploid wittei and vestitus). This case study may be interpreted as indicating a powerful influence of host genetic factors on susceptibility to infection, host-specificity, and parasite speciation.

Animals↗

Environmental effects on transmission of Discocotyle sagittata (Monogenea): egg production and development.

Egg production by the freshwater gill monogenean Discocotyle sagittata infecting rainbow trout (Oncorhynchus mykiss) was monitored at 5, 13 and 18 degrees C; eggs were incubated at 6, 10, 13, 15, 16, 18, 22 and 26 degrees C and the hatching times determined. Mean per capita output at 13 degrees C ranged from 0.8 eggs/worm/day (e/w/d) to 18.3 e/w/d for 25 hosts (burdens 1-17 worms/host). Average egg production rates for worms in single burdens varied from 3 e/d to 14.6 e/d at 13 degrees C, mean 7.6 e/d (+/- 0.63) (n = 8). Egg production was temperature dependent, increasing from a mean of 1.5 e/w/d at 5 degrees C to 12.0 e/w/d at 18 degrees C. Developmental rate was also temperature dependent: larvae began hatching after 84 days at 6 degrees C, 28 days at 13 degrees C, and 20 days at 18 degrees C. Eggs laid within the same 24 h period hatched over 3-7 days at 13-18 degrees C; this range was extended at decreasing temperatures. Egg viability was generally high: between 13 and 18 degrees C a mean of 92% of larvae successfully emerged. However, viability declined at the highest and lowest temperatures (23% hatching at 6 degrees C, 55% at 8 degrees C and 47% at 26 degrees C). The implications for seasonal parasite transmission are discussed.

Animals↗