Article

Recognizing the Causes of Parasite Morphological Variation to Resolve the Status of a Cryptogenic Pentastome

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Abstract

Exotic species can threaten biodiversity by introducing parasites to native hosts. Thus, it is critical to identify if the same parasite species infects both native and exotic hosts. However, developmental- or environmental-induced morphological variation may render species identification ambiguous. Our study reports a range expansion in the southern United States of the pentastome Raillietiella indica from the Mediterranean gecko, Hemidactylus turcicus, as well as a host expansion into the green anole, Anolis carolinensis, in the anole's native range. Species identification was based on sequence data and male spicule shape. In agreement with a study from Australia, we found that much of the morphological variation in hook measurements, the primary diagnostic traits of raillietiellid pentastomes, was due to development. Here, we explicitly link this developmental variation to instar stage by incorporating experimental infection data obtained from the literature. We also show that the various hook traits are themselves highly correlated and, thus, likely not independent. Taking instar stage and correlated hook variables into account, we directly controlled for development on a composite hook size measurement. Using a large sample size from H. turcicus, we did not find any consistent effects of potential factors (host sex, host snout-vent-length, or parasite intensity) that may result in environmental-induced variation in relative hook size (corrected for body length). However, relative male spicule size tended to be negatively correlated with parasite intensity. In contrast, both pentastome body length and relative hook size significantly varied among host species whereas relative male spicule size was not significantly different among host species. Our study independently supports the conclusions that developmental- and host-induced morphological variations need to be accounted for to accurately identify pentastome species.

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... In the gecko species Hemidactylus frenatus, the species Raillietiella indica (syn R. frenatus, R. hebitihamata) develops hooks that are significantly different from those that R. indica develops in the marine toad (Rhinella marina), to the extent that they would morphologically identified as different species (11). Similarly, R. indica hook measurements vary significantly depending on whether the host is a Mediterranean gecko or a green anole (Anolis carolinensis) (12). Feral populations of another member of the gecko genus Hemidactylus, H. turcicus (Mediterranean gecko) populations are well established in Alachua County (13). ...
... Raillietiella indica was reported in the Mediterranean gecko, Hemidactylus turcicus in Texas in the early 1980s (15). Sakla et al. (12) later reported R. indica was not only infecting H. turcicus, but that it had also made its way into the native Anolis carolinensis in Louisiana, and noted an unpublished report of R. indica in H. frenatus in New Orleans, Louisiana as early as 2008. The authors speculated the introduction of R. indica into Louisiana could be from the Mediterranean gecko, known to New Orleans since 1949, or introduced from the Cuban brown anole, Anolis sagrei, another known host of R. indica (12). ...
... Sakla et al. (12) later reported R. indica was not only infecting H. turcicus, but that it had also made its way into the native Anolis carolinensis in Louisiana, and noted an unpublished report of R. indica in H. frenatus in New Orleans, Louisiana as early as 2008. The authors speculated the introduction of R. indica into Louisiana could be from the Mediterranean gecko, known to New Orleans since 1949, or introduced from the Cuban brown anole, Anolis sagrei, another known host of R. indica (12). The exact origin of free-ranging Florida Burmese pythons, the natural host(s) for R. orientalis, in southern Florida is unknown; however, a prevailing theory is due to the release of animals destined for the pet trade in the 1990s. ...
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Raillietiella orientalis is an obligate, crustacean parasite that resides in the respiratory tract of definitive snake hosts. Common throughout southeastern Asia and Australia, R. orientalis is believed to have been introduced into southern Florida, United States along with Burmese pythons (Python bivittatus) in the 1990s. While the invasive range of Burmese pythons is restricted to southern Florida, R. orientalis has advanced north in the state in native snake species. R. orientalis were recovered from the lungs, trachea, oral cavity, and esophagus of an emaciated adult female free-ranging banded water snake (Nerodia fasciata) in north central (Alachua County), Florida, USA. Concurrent findings included the recovery of Ochetosoma sp. trematodes from the oral cavity, and multifocal dermal lesions consistent with snake fungal disease (Ophidiomyces ophiodiicola). This is the first report of R. orientalis in north central Florida, well outside the invasive range of the Burmese python, documenting the substantial northward expansion of the known geographical range of this invasive pentastome in Florida.
... The genus Raillietiella is the most specious including 45 described species and also many unclassified species (Christoffersen & de Assis, 2013). Raillietiella species are found nearly indica can vary in two different definitive hosts (Mediterranean geckos (Hemidactylus turcicus) and green anoles (Anolis carolinensis)) and Raillietiella orientalis morphology varies considerably between different snake species (Kelehear et al., 2014;Sakla et al., 2019;Westfall et al., 2019). This morphological variation within a parasite species between different hosts makes identification of these parasites particularly challenging at the species level, especially in a newly described host. ...
... Based on previous studies on variations of morphology based on host, male spicule size appeared to be conserved among host species, while body length and hook size varied greatly between hosts (Sakla et al., 2019). The morphology of the copulatory spicules in the specimens described in this study were distinct from other described species of Raillietiella. ...
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... Previously reported intraspecific variation for other pentastomid species at 18S has ranged from 0-0.07% while 28S has ranged from 0-0.9% (Barton and Morgan 2016, Woodyard et al. 2019b, Woodyard et al. 2019a. Similarly, cox 1 variation has been reported as by 0-1.03% within species (Kelehear et al. 2011, Barton and Morgan 2016, Sakla et al. 2019, Woodyard et al. 2019b, Woodyard et al. 2019a). While the 18S sequence from our analysis is a 100% match to previously published sequence data from Porocephalus crotali in GenBank (MG559607), there is limited data available to determine variability at this marker between species. ...
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For thirty years I have read publications about this spate of invasions; and many of them preserve the atmosphere of first-hand reporting by people who have actually seen them happening, and give a feeling of urgency and scale that is absent from the drier summaries of text-books. We must make no mistake: we are seeing one of the great historical convulsions in the world’s fauna and flora. We might say, with Professor Challenger, standing on Conan Doyle’s ‘Lost World’, with his black beard jutting out: ‘We have been privileged to be present at one of the typical decisive battles of history—the battles which have determined the fate of the world.’ But how will it be decisive? Will it be a Lost World? These are questions that ecologists ought to try to answer.
Article
Forty-three percent of adult Mediterranean geckos, Hemidactylus turcicus, from southern Texas were infected with a pulmonary pentastome, Raillietiella frenatus. Pentastome occurrence and biomass did not affect carcass, liver or testis mass of males or carcass mass of females through the year. However, liver mass in females during the nonreproductive period and fatbody mass in both sexes during the reproductive period was significantly lower in individuals with the highest biomass of pentastomes. Infected females had a higher frequency of medium sized yolked follicles than uninfected females, but the latter had a significantly higher frequency of oviductal eggs than infected female geckos. We estimated that oviductal egg production in this gecko population was reduced by 21% due to the pentastome infection. These data indicated that this macroparasitic infection should be considered as a possible factor in the population regulation of H. turcicus in southern Texas.
Article
Raillietiella teagueselfi n. sp. is described from the lungs of the Mediterranean gecko, Hemidactylus turcicus, in Houston, Texas, U.S.A. This new pentastomid is most closely related to R. affinis Bovien, 1927, of Asiatic Tokay geckos (Gekko gecko) in Indonesia, but mature males differ in possessing rounded posterior hooks with swollen, blunt-tipped barbs, instead of relatively sharp-tipped hooks. In addition, the annulus number of females can readily differentiate the new species from 6 of the 10 blunt-tipped species (R. gehyrae Bovien, 1927; R. hemidactyli Hett, 1934; R. maculatus Rao and Hiregauder, 1959; R. monarchus Ali et al., 1984; R. mabuiae (Heymons, 1922); and R. scincoides Ali et al., 1984). Two of the remaining 3 species of blunt-tipped raillietiellids (R. frenatus Ali et al., 1981, and R. maculibris Ali et al., 1984) are differentiated from female R. teagueselfi by having larger hook dimensions. The new species can be distinguished from R.freitasi (Motta and Gomes, 1968) by having a hooked spicule. Observations on the prevalence and intensity of infections are presented.
Article
Lack of knowledge of the extent of natural morphological variation can undermine proper taxonomic decisions. Confounding this problem is artifactual variation that arises from improper fixation techniques. For the morphologically based taxonomy of the cestode genus Oochoristica, little information exists on the plasticity of important taxonomic characters. In addition, paratypes of several species of Oochoristica are highly contracted and contorted. These paratypes were recovered from preserved hosts; thus, the tapeworms were killed and fixed inside the host (in situ fixation). Experiments demonstrated that in situ fixation of Oochoristica javaensis results in highly contracted specimens, and statistical comparisons between relaxed and in situ-fixed tapeworms revealed significant differences for proglottid measurements. Natural variation for the paratypes recovered from preserved hosts is likely misrepresented by the artificial variation induced by in situ fixation. Lastly, data from natural infections suggested that proglottid characters of O. javaensis are plastic and may be subject to crowding effects.
Article
Because assumptions of strict host specificity and geographic isolation apparently have been used as criteria in determining species of Oochoristica, studies were conducted to address the effects that these assumptions could have on resolving the taxonomy of Oochoristica. Experimental infections of native fence lizards, Sceloporus undulatus undulatus, and Indo-Pacific geckos, Hemidactylus garnotii, demonstrated that the exotic tapeworm Oochoristica javaensis lacked host specificity. In addition, tapeworms with gravid proglottids, a stage of development that has not been previously reported for any species of Oochoristica, were obtained from both hosts. Evidence against the assumption of geographic isolation stems from the fact that lizard species known to harbor Oochoristica spp. have been introduced beyond their native ranges, and in some cases, these introductions predate the species descriptions. Lack of support for either assumption indicates a need for more rigorous analyses and experimentation to determine species of Oochoristica.
Article
Invasive species are spreading at high rates, yet fundamental processes allowing them to progress through the stages of invasion are unclear. The establishment stage is a critical point because this is when exotic species can survive, reproduce, and begin to spread. Unfortunately, inference of population dynamics during this stage may be impossible if historical and observational data are incomplete. Nonetheless, critical inferences on population dynamics during the establishment stage can be acquired indirectly by characterizing demographic history via the population genetics of recently introduced populations. Geckos have been introduced at a global scale and are one of the most successfully establishing families of alien reptile known. Here we conduct a series of population genetic analyses among five close subpopulations of the introduced Mediterranean gecko Hemidactylus turcicus. We tested for non-equilibrium genetic signatures, a pattern expected during early stages of invasion if there were few founders or repeated introductions led to population turnover. Genetic analyses showed no evidence of non-equilibrium dynamics such as genetic bottlenecks. Moreover, we found strong support for population genetic equilibrium dynamics. The observed results may have been generated via an introduction that involved high propagule pressure. However, given the life history of H. turcicus including generation time and dispersal potential, we favor the hypothesis that the invasive metapopulation has rapidly reached the establishment stage as indicated by relatively constant effective sizes and migration rates among introduced subpopulations. The ability to rapidly pass through the establishment stage may in part explain the invasion success of these geckos.
Article
The life-cycles of two closely related cephalobaenid pentastomids, Raillietiella gehyrae and Raillietiella frenatus, which utilize geckos as definitive hosts and cockroaches as intermediate hosts, have been investigated in detail. Early development in the fat-body of cockroaches involves 2 moults to an infective, 3rd-stage larva which appears from 42–44 days post-infection. Complete development in geckos involves a further 5 moults in the case of males and 6 for females. Males mature precociously and copulation is a once-in-a-lifetime event which occurs around day 80 post-infection when both sexes are the same size but the uterus of the female is undeveloped. Sperm, stored in the spermathecae, is used to fertilize oocytes which slowly accumulate in the developing saccate uterus. Patency commences when the uterus carries approximately 4000–5500 eggs but only 25–36 % of these contain fully developed primary larvae. Since only mature eggs are deposited, we postulate that the vagina (?) of the female must be equipped with a selective filter that allows through large eggs but retains smaller, immature eggs. Thus the only limit on fecundity is the total number of sperms in the spermathecae and this is precisely the same factor that constrains egg production in the advanced order Porocephalida.
Article
Three species of Raillietiella with blunt tips to the posterior hooks have been described from south-east Asia and Indonesia. However, we have established that two other species. R. hemidactyli from an Indian agamid lizard and R. mabuiae from an African skink, also possess blunt hooks but this fact is unaccountably not mentioned in early descriptions. The various species are distinguished by differences in body-length, or number of abdominal annuli and/or host and geographical distribution. Certain of the morphological characters overlap and some authors have considered the complex a single species. We have examined preserved material from a variety of sources, including type specimens, and by using comparative hook data and a standardized annulus counting procedure we show that at least three of the earlier described species are valid. A new species, R. frenatus, is described. An attempt is made to correct the various errors in identification that have crept into the more recent literature. ac]19801204
Article
It would be an exaggeration to argue that most invasions produce ecosystem impacts, and the term should be reserved for cases in which many species in an ecosystem are affected. However, certain facts suggest that true ecosystem impacts are more common than is normally assumed. First, the term “ecosystem impact” has often been reserved for cases in which the nutrient regime or nutrient cycling is affected, whereas physical structural and other changes in ecosystems ought to be included. Second, as with all ecology, very few systems and species have been studied relative to all those that exist, so it is likely that many ecosystem impacts remain to be detected. Third, there are many types of impacts, many are idiosyncratic, many are subtle, and many are indirect, so it is likely that many impacts have simply not been recognized even in studied systems. Finally, the frequency of the lag phenomenon in invasions implies that at least some existing non-native species that are currently having little or no impact will eventually have much greater ones. These facts suggest that, even if it would be an overstatement to say that most invasions cause ecosystem impacts, it would not be more of an overstatement than the common assertion that very few introduced species have any significant impact. KeywordsFire regime–Habitat structure–Invasional meltdown–Lag time–Nutrient cycling
Article
Four previously established Raillietiella spp. are redescribed. Two of these, R. kochi and R. shipleyi from African monitor lizards, cannot be reliably separated, R. shipleyi is regarded therefore as a synonym of R. kochi. A new species R. cartagenensis from South American geckos and a skink is differentiated from other sharp-hooked species on the unique form of the male copulatory spicule. The entire genus is assessed in the light of recent evidence and a new set of taxonomic groupings is proposed which is based primarily on host differences. However, 14 species, infecting small insectivorous lizards, are subdivided into two groups because of marked differences in the morphology of the posterior hook, an idea originally outlined by Self (1969). Appropriate combinations of body length, annulus number, posterior hook dimensions and the form of the male copulatory spicule provide adequate diagnostic criteria. Certain species infect a large number of hosts which have a wide range of diet. Since vertebrate intermediate hosts may be involved in the life-cycle it may subsequently transpire, when more sophisticated diagnostic techniques appear, that several species have been grouped together. The genus embraces 24 well characterized species and at least seven others await confirmation. ac]19840112
Article
While there is good evidence linking animal introductions to impacts on native communities via disease emergence, our understanding of how such impacts occur is incomplete. Invasion ecologists have focused on the disease risks to native communities through "spillover" of infectious agents introduced with nonindigenous hosts, while overlooking a potentially more common mechanism of impact, that of "parasite spillback." We hypothesize that parasite spillback could occur when a nonindigenous species is a competent host for a native parasite, with the presence of the additional host increasing disease impacts in native species. Despite its lack of formalization in all recent reviews of the role of parasites in species introductions, aspects of the invasion process actually favor parasite spillback over spillover. We specifically review the animal-parasite literature and show that native species (arthropods, parasitoids, protozoa, and helminths) account for 67% of the parasite fauna of nonindigenous animals from a range of taxonomic groups. We show that nonindigenous species can be highly competent hosts for such parasites and provide evidence that infection by native parasites does spillback from nonindigenous species to native host species, with effects at both the host individual and population scale. We conclude by calling for greater recognition of parasite spillback as a potential threat to native species, discuss possible reasons for its neglect by invasion ecologists, and identify future research directions.
Article
This chapter describes the biology of pentastomids and several of the most important deficiencies are outlined. Pentastomids, otherwise known as linguatulids or tongueworms, are a relatively neglected and poorly understood class of endoparasites, which occupy a unique position among invertebrates in that, as adults, they are entirely restricted to the respiratory tract of vertebrates: the majority of species grow to maturity in the lungs. About 90% of species infect reptiles, and it is probable that they have been associated with these hosts since the Mesozoic. Despite this long period for potential adaptive radiation, the basic body design is remarkably conservative, and pentastomids comprise a homogeneous and distinctive systematic assemblage of about 100 species. All possess a vermiform, often conspicuously annulated abdomen, usually strongly united with a rounded cephalothorax, which bears, on its ventral surface, a small sucking mouth flanked by two pairs of hooks. Pentastomids, in common with other parasites, are regulators of host populations and many of the species recovered from zoo autopsies. In some cases, host death is directly or indirectly attributable to a pentastomid infection.
Article
Parasite surveys of exotic hosts offer the opportunity to examine parasite colonization on different scales (i.e., host individual, host population, host species, and new geographic locality). Ten helminths (Macracanthorhynchus ingens, Mesocestoides lineatus, Oochoristica javaensis, Haematoloechus varioplexus, Mesocoelium monas, Telorchis corti, Cosmocercoides variabilis, Oswaldocruzia leidyi, Skrjabinoptera sp., and a larval acuariid nematode) were recovered from the exotic Mediterranean gecko Hemidactylus turcicus, in southeastern Louisiana. Only 1 exotic parasite, O. javaensis, colonized a new geographic locality, but 7 local helminths colonized a new host species. Helminth communities of H. turcicus were similar in structure to what has been hypothesized or observed for lizards. Thus, communities were composed of generalists and were depauperate (i.e., colonization of individual geckos or host populations was rare for most of the helminths); however, there was significant variation in community structure among local habitats. Although the gecko's behavioral and physiological attributes predict colonization by monoxenous helminths, only 2, C. variabilis and O. leidyi, were recovered. Eight heteroxenous helminths, 2 of which (the acuariid and O. javaensis) were the most widely distributed and abundant, were the better colonizers. The gecko's generalist diet may have exposed it to a diverse parasite fauna and thus been important in determining the helminths that could colonize.
The incomplete natural history of mitochondria
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Ecological and conservation implications regarding the helminth parasites of the introduced Mediterranean gecko, Hemidactylus turcicus, in southeastern Louisiana with notes on the life cycle and specificity of the cestode Oochorstica javaensis
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