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Recognizing the Causes of Parasite Morphological Variation to Resolve the Status of a Cryptogenic Pentastome
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.
... 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. ...
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. ...
Pentastomes are crustacean endoparasites in the lungs of herpetofauna and rarely mammals and birds. To date, the only pentastomes reported in chelonians, all aquatic turtles, are Diesingia megastomum from Brazil and Pelonia africana from South Africa. In March 2021, 185 juvenile tortoises (Chelonoidis niger) were confiscated after an attempted illegal exportation from the Galápagos. It is believed the tortoises were removed from nests on Santa Cruz Island. The young tortoises were individually wrapped in plastic and at seizure ten were dead and another 25 tortoises subsequently died. One of the tortoises, estimated to be 3 months old, had 11 pentastomes in the lungs. The pentastomes were identified as a Raillietiella sp. based on morphology. The specimens had a claviform body that tapers into a bifid tail, a 165.3 μm × 92.1 μm buccal cadre, and sharp tipped anterior and posterior hooks with the posterior hooks being larger than the anterior. The males have smooth copulatory spicules with a rounded, smooth base. All females were gravid. Molecular analysis confirmed that the parasites were a Raillietiella sp. Based on the COI gene, it was most similar (82.7% identical) to an undescribed Raillietiella species from a Caribbean anole (Anolis cristatellus) found in Florida followed by R. hebitihamata (81%), R. indica (80.7%), and R. orientalis (78.8–80.7%). Based on the 18S rRNA gene sequence (1799 bp), it was most similar (99.3% identical) to two undescribed Raillietiella species followed by R. aegypti from a berber skink (Eumeces schneideri) from Saudia Arabia. Phylogenetically, with both molecular targets, the Raillietiella sp. from the Galápagos tortoise grouped with other Raillietiella spp. and was basal within the group. Currently, the origin of this parasite (native to Galápagos or introduced) and the life cycle are unknown. Because some pentastome species, especially when in aberrant hosts, can be pathogenic, additional studies of parasites in native and introduced reptile and amphibian species in the Galápagos are needed to better understand the risk this parasite poses to Galápagos tortoises.
... 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. ...
Ultrastructural and molecular data are provided from a single adult female pentastomid opportunistically collected from a road-killed rattlesnake in Russell, KS. Ultrastructural data consisted of light and SEM microscopy of the pentastomid and its eggs, while molecular data consisted of partial 18S and 28S ribosomal sequences and a partial cytochrome c oxidase subunit 1 sequence from the same specimen used for SEM. Ultrastructural and molecular data support generic identification of the pentastomid as Porocephalus sp. These molecular data were also used with previously published pentastomid sequence data for a concatenated phylogenetic analysis, which support the current, morphology-based taxonomic placement of the genus.
Identification of the origin of parasites of nonindigenous species (NIS) can be complex. NIS may introduce parasites from their native range and acquire parasites from within their invaded range. Determination of whether parasites are non-native or native can be complicated when parasite genera occur within both the NIS’ native range and its introduced range. We explored potential for spillover and spillback of lung parasites infecting Burmese pythons (Python bivittatus) in their invasive range (Florida). We collected 498 indigenous snakes of 26 species and 805 Burmese pythons during 2004–2016 and examined them for lung parasites. We used morphology to identify three genera of pentastome parasites, Raillietiella, a cosmopolitan form, and Porocephalus and Kiricephalus, both New World forms. We sequenced these parasites at one mitochondrial and one nuclear locus and showed that each genus is represented by a single species, R. orientalis, P. crotali, and K. coarctatus. Pythons are host to R. orientalis and P. crotali, but not K. coarctatus; native snakes are host to all three species. Sequence data show that pythons introduced R. orientalis to North America, where this parasite now infects native snakes. Additionally, our data suggest that pythons are competent hosts to P. crotali, a widespread parasite native to North and South America that was previously hypothesized to infect only viperid snakes. Our results indicate invasive Burmese pythons have affected parasite-host dynamics of native snakes in ways that are consistent with parasite spillover and demonstrate the potential for indirect effects during invasions. Additionally, we show that pythons have acquired a parasite native to their introduced range, which is the initial condition necessary for parasite spillback.
One of the frequent questions by users of the mixed model function lmer of the lme4 package has been: How can I get p values for the F and t tests for objects returned by lmer? The lmerTest package extends the 'lmerMod' class of the lme4 package, by overloading the anova and summary functions by providing p values for tests for fixed effects. We have implemented the Satterthwaite's method for approximating degrees of freedom for the t and F tests. We have also implemented the construction of Type I - III ANOVA tables. Furthermore, one may also obtain the summary as well as the anova table using the Kenward-Roger approximation for denominator degrees of freedom (based on the KRmodcomp function from the pbkrtest package). Some other convenient mixed model analysis tools such as a step method, that performs backward elimination of nonsignificant effects - both random and fixed, calculation of population means and multiple comparison tests together with plot facilities are provided by the package as well.
Negative effects of parasites on their hosts are well documented, but the proximate mechanisms
by which parasites reduce their host’s fitness are poorly understood. For example, it
has been suggested that parasites might be energetically demanding. However, a recent
meta-analysis suggests that they have statistically insignificant effects on host resting metabolic
rate (RMR). It is possible, though, that energetic costs associated with parasites are
only manifested during and/or following periods of activity. Here, we measured CO2 production
(a surrogate for metabolism) in Mediterranean geckos (Hemidactylus turcicus) infected
with a lung parasite, the pentastome Raillietiella indica, under two physiological conditions:
rested and recently active. In rested geckos, there was a negative, but non-significant association
between the number of pentastomes (i.e., infection intensity) and CO2 production. In
recently active geckos (chased for 3 minutes), we recorded CO2 production from its maximum
value until it declined to a stationary phase.We analyzed this decline as a 3 phase
function (initial decline, secondary decline, stationary). Geckos that were recently active
showed, in the secondary phase, a significant decrease in CO2 production as pentastome
intensity increased. Moreover, duration of the secondary phase showed a significant positive
association with the number of pentastomes. These results suggest that the intensity of
pentastome load exerts a weak effect on the metabolism of resting geckos, but a strong
physiological effect on geckos that have recently been active; we speculate this occurs via
mechanical constraints on breathing. Our results provide a potential mechanism by which
pentastomes can reduce gecko fitness.
The pentastomid parasite,
Raillietiella frenata
, is native to Asia where it infects the Asian House gecko,
Hemidactylus frenatus
. This gecko has been widely introduced and recently
R. frenata
was found in introduced populations of cane toads (
Rhinella marina
) in Australia, indicating a host-switch from introduced geckos to toads. Here we report non-native adult
R. frenata
infecting the lungs of native cane toads in Panama. Eight of 64 toads were infected (median = 2·5, range = 1–80 pentastomids/toad) and pentastomid prevalence was positively associated with the number of buildings at a site, though further sampling is needed to confirm this pattern. We postulate that this pattern is likely due to a host shift of this parasite from an urban-associated introduced gecko. This is the first record of this parasite infecting cane toads in their native range, and the first instance of this parasite occurring in Central America.
Maximum likelihood or restricted maximum likelihood (REML) estimates of the
parameters in linear mixed-effects models can be determined using the lmer
function in the lme4 package for R. As for most model-fitting functions in R,
the model is described in an lmer call by a formula, in this case including
both fixed- and random-effects terms. The formula and data together determine a
numerical representation of the model from which the profiled deviance or the
profiled REML criterion can be evaluated as a function of some of the model
parameters. The appropriate criterion is optimized, using one of the
constrained optimization functions in R, to provide the parameter estimates. We
describe the structure of the model, the steps in evaluating the profiled
deviance or REML criterion, and the structure of classes or types that
represents such a model. Sufficient detail is included to allow specialization
of these structures by users who wish to write functions to fit specialized
linear mixed models, such as models incorporating pedigrees or smoothing
splines, that are not easily expressible in the formula language used by lmer.
We define co-introduced parasites as those which have been transported with an alien host to a new locality, outside of their natural range, and co-invading parasites as those which have been co-introduced and then spread to new, native hosts. Of 98 published studies of co-introductions, over 50% of hosts were freshwater fishes and 49% of parasites were helminths. Although we would expect parasites with simple, direct life cycles to be much more likely to be introduced and establish in a new locality, a substantial proportion (36%) of co-introductions were of parasites with an indirect life cycle. Seventy-eight per cent of co-introduced parasites were found in native host species and can therefore be classed as co-invaders. Host switching was equally common among parasites with direct and indirect life cycles. The magnitude of the threat posed to native species by co-invaders will depend, among other things, on parasite virulence. In 16 cases where co-introduced parasites have switched to native hosts and information was available on relative virulence, 14 (85%) were more virulent in native hosts than in the co-introduced alien host. We argue that this does not necessarily support the naïve host theory that co-invading parasites will have greater pathogenic effects in native hosts with which they have no coevolutionary history, but may instead be a consequence of the greater likelihood for parasites with lower virulence in their natural host to be co-introduced.
Pentastomids are endoparasites of the respiratory system of vertebrates, maturing primarily in carnivorous reptiles. Adult and larval pentastomids can cause severe pathology resulting in the death of their intermediate and definitive hosts. The study of pentastomids is a neglected field, impaired by risk of zoonoses, difficulties in species identification, and life cycle complexities. We surveyed wild snakes in the tropics of Australia to clarify which host species possess these parasites, and then sought to identify these pentastomids using a combination of morphological and molecular techniques. We detected pentastomid infections in 59% of the 81 snakes surveyed. The ubiquity of pentastomid infections in snakes of the Australian tropics sampled in this study is alarmingly high considering the often-adverse consequences of infection and the recognized zoonotic potential of these parasites. The pentastomids were of the genera Raillietiella and Waddycephalus and infected a range of host taxa, encompassing seven snake species from three snake families. All seven snake species represent new host records for pentastomids of the genera Raillietiella and/or Waddycephalus. The arboreal colubrid Dendrelaphis punctulatus and the terrestrial elapid Demansia vestigiata had particularly high infection prevalences (79% and 100% infected, respectively). Raillietiella orientalis infected 38% of the snakes surveyed, especially frog-eating species, implying a frog intermediate host for this parasite. R. orientalis was previously known only from Asian snakes and has invaded Australia via an unknown pathway. Our molecular data indicated that five species of Waddycephalus infect 28% of snakes in the surveyed area. Our morphological data indicate that features of pentastomid anatomy previously utilised to identify species of the genus Waddycephalus are unreliable for distinguishing species, highlighting the need for additional taxonomic work on this genus.
The success of a biological invasion can depend upon other invasions; and in some cases, an earlier invader may fail to spread until facilitated by a second invader. Our study documents a case whereby an invasive parasite has remained patchily distributed for decades due to the fragmented nature of available hosts; but the recent arrival of a broadly distributed alternative invasive host species provides an opportunity for the parasite to expand its range considerably. At least 20 years ago, endoparasitic pentastomids (Raillietiella frenata) were brought with their native host, the invasive Asian house gecko Hemidactylus frenatus, to the port city of Darwin in tropical Australia. These geckos rarely disperse away from human habitation, restricting the transmission of their parasites to urban environments – and thus, their pentastomids have remained patchily distributed and have only been recorded in scant localities, primarily surrounding Darwin. The recent range expansion of the invasive cane toad Rhinella marina into the Darwin area has provided an alternative host for this
pentastomid. Our results show that the cane toad is a competent host for Ra. frenata – toads shed fully embryonated pentastomid eggs in their faeces – and that pentastomids are now common in cane toads near Darwin. Likely reflecting the tendency for the parasite’s traditional definitive host (the Asian house gecko) and only known intermediate host (the cockroach) to reside around buildings, we found the prevalence of this parasite follows an urban distribution. Because cane toads are widely distributed through urban and rural habitat and can shed viable pentastomid eggs, the toad invasion is likely to facilitate the parasite’s spread across the tropics, into areas (and additional susceptible hosts) that were previously inaccessible to it.
The pentastome Raillietiella indica was collected from the introduced toad Bufo marinus in Oahu, Hawaii, U.S.A. The parasite was identified as R. indica from similarities in morphology of the hooks, buccal cadre, and male copulatory spicule. This represents a new host record for this parasite, previously only recorded from Bufo melanostictus. This also represents a new locality record because this parasite has only been reported previously in India, Burma, and Taiwan. This is the third record of B. marinus as a host for parasites in Hawaii.
For the past 25 years NIH Image and ImageJ software have been pioneers as open tools for the
analysis of scientific images. We discuss the origins, challenges and solutions of these two programs,
and how their history can serve to advise and inform other software projects.
The taxonomy of the Recent members of the crustacean subclass Pentastomida is based on nine accepted family names derived from 12 available names, 24 generic names derived from 37 available names (plus two incorrect subsequent spellings and one nomen nudum) and 124 accepted species names derived from 183 available names of which six remain incertae sedis as to their generic assignment. Compilation of this list has revealed that existing catalogues have included misspellings, wrong attributions and dates of the authors of taxa, and incorrectly nominated type-species. These are corrected here with reference to the original descriptions and diagnoses. Notably, all families except one were erected much earlier and by authors other than Fain (1961), who was credited by Martin & Davis (2001) and other authors before and afterwards with seven of the nine families they recognised. Other significant taxonomic anomalies are revealed. Raillietiellidae Sambon, 1922 is a senior synonym of Cephalobaenidae Heymons, 1922, the name in popular usage for the family including Cephalobaena Heymons, 1922 and Raillietiella Sambon, in Vaney & Sambon, 1910; here the two genera are placed in separate families following Almeida & Christoffersen (1999). Heymonsia Hett, 1934, considered a junior synonym of Raillietiella, is a nomen nudum. Raillietiella geckonis (Diesing, 1850) is a potential senior synonym of several SE Asian species of this genus. Raillietiella frenata Ali, Riley & Self, 1981 is a widely used species name but is a subjective junior synonym of R. hebitihamata Self & Kuntz, 1960 according to its own authors. Morphological and molecular evidence suggest that R. indica Gedoelst, 1921 is a subjective senior synonym of both species. The priority of Linguatulidae Haldeman, 1851 over Linguatulida Vogt, 1851, erected as a family in the same year, is established by applying the First Reviser rule. Linguatula serrata Frölich, 1789 is herein selected as the type-species of Prionoderma, making it an objective synonym of Linguatula Frölich, 1789. The priority of L.
serrata over Taenia rhinaris Meyer, 1789 and T.capraea Abildgaard, 1789, all published in the same year, is established by applying the First Reviser rule. The purported synonymy of Netrorhynchus Zenker, 1827, also misspelled Nettorhynchus, with Armillifer Sambon, 1922 would seem to be ill-founded and without popular support. Armillifer australis Heymons, 1935, published as a subspecies of A.
moniliformis (Diesing, 1836), is both a senior synonym and a homonym of A. australis Riley & Self, 1981. Humboldt (1812) is confirmed as the author of Porocephalus Humboldt, 1812 and P. crotali Humboldt, 1812. Pentastomidae Shipley, 1909 is an older family name than its subjective synonym Porocephalinae Sambon, 1922, but prevailing usage allows the latter to be retained as a family name. Cayerina mirabilis Kishida, 1927 is a genus and species from a Japanese frog that has not appeared in the more recent pentastome literature. Sebekia minor (Wedl, 1861) is an objective senior synonym of the more widely used S. wedli Gigioli, in Sambon, 1922. The importance of the many junior synonyms will become evident should refined morphological and molecular evidence reveal cryptic species or greater host-specificity than presently recognised.
Unlabelled:
Unipro UGENE is a multiplatform open-source software with the main goal of assisting molecular biologists without much expertise in bioinformatics to manage, analyze and visualize their data. UGENE integrates widely used bioinformatics tools within a common user interface. The toolkit supports multiple biological data formats and allows the retrieval of data from remote data sources. It provides visualization modules for biological objects such as annotated genome sequences, Next Generation Sequencing (NGS) assembly data, multiple sequence alignments, phylogenetic trees and 3D structures. Most of the integrated algorithms are tuned for maximum performance by the usage of multithreading and special processor instructions. UGENE includes a visual environment for creating reusable workflows that can be launched on local resources or in a High Performance Computing (HPC) environment. UGENE is written in C++ using the Qt framework. The built-in plugin system and structured UGENE API make it possible to extend the toolkit with new functionality.
Availability and implementation:
UGENE binaries are freely available for MS Windows, Linux and Mac OS X at http://ugene.unipro.ru/download.html. UGENE code is licensed under the GPLv2; the information about the code licensing and copyright of integrated tools can be found in the LICENSE.3rd_party file provided with the source bundle.
Taxonomic studies of parasites can be severely compromised if the host species affects parasite morphology; an uncritical analysis might recognize multiple taxa simply because of phenotypically plastic responses of parasite morphology to host physiology. Pentastomids of the genus Raillietiella are endoparasitic crustaceans primarily infecting the respiratory system of carnivorous reptiles, but also recorded from bufonid anurans. The delineation of pentastomids at the generic level is clear, but the taxonomic status of many species is not. We collected raillietiellids from lungs of the invasive cane toad (Rhinella marina), the invasive Asian house gecko (Hemidactylus frenatus), and a native tree frog (Litoria caerulea) in tropical Australia, and employed a combination of genetic analyses, and traditional and novel morphological methods to clarify their identity. Conventional analyses of parasite morphology (which focus on raw values of morphological traits) revealed two discrete clusters in terms of pentastome hook size, implying two different species of pentastomes: one from toads and a tree frog (Raillietiella indica) and another from lizards (Raillietiella frenatus). However, these clusters disappeared in allometric analyses that took pentastome body size into account, suggesting that only a single pentastome taxon may be involved. Our molecular data revealed no genetic differences between parasites in toads versus lizards, confirming that there was only one species: R. frenatus. This pentastome (previously known only from lizards) clearly is also capable of maturing in anurans. Our analyses show that the morphological features used in pentastomid taxonomy change as the parasite transitions through developmental stages in the definitive host. To facilitate valid descriptions of new species of pentastomes, future taxonomic work should include both morphological measurements (incorporating quantitative measures of body size and hook bluntness) and molecular data.
Systematics involves resolving both the taxonomy and phylogenetic placement of organisms. We review the advantages and disadvantages of the two kinds of information commonly used for such inferences--morphological and molecular data--as applied to the systematics of metazoan parasites generally, with special attention to the malaria parasites. The problems that potentially confound the use of morphology in parasites include challenges to consistent specimen preservation, plasticity of features depending on hosts or other environmental factors, and morphological convergence. Molecular characters such as DNA sequences present an alternative data source and are particularly useful when not all the parasite's life stages are present or when parasitaemia is low. Nonetheless, molecular data can bring challenges that include troublesome DNA isolation, paralogous gene copies, difficulty in developing molecular markers, and preferential amplification in mixed species infections. Given the differential benefits and shortcomings of both molecular and morphological characters, both should be implemented in parasite taxonomy and phylogenetics.
From January to April 2006, 37 specimens of Hemidactylus mabouia were collected in houses, in the municipality of Barbalha (7 degrees 20' S and 39 degrees 18' W), Ceará State, Northeast Brazil. Among the individuals captured, 17 were infected with pentastomids, totalling a prevalence of 45.9%, which did not differ between sexes. Host size did not influence the infection intensity. Two species of pentastomids were found: Raillietiella frenatus and R. mottae. The prevalence of R. frenatus (43.2%) was higher than R. mottae (2.7%), whereas the infection intensity of R. frenatus was comparatively lower (1.8 +/- 1.4) than R. mottae (36 parasites in a single host). Overall mean intensity of infection was 3.8 +/- 8.4 pentastomids. We found no pentastomid infecting juvenile geckos. The parameters of infection in this host population are in accordance to the findings of other studies, in which the high parasitism rate was associated to the feeding habits of geckos living in houses and buildings. Hemidactylus mabouia is a new host to R. mottae and the infection by R. frenatus is the first record of the occurrence this pentastomid species in Brazil.
We describe "universal" DNA primers for polymerase chain reaction (PCR) amplification of a 710-bp fragment of the mitochondrial cytochrome c oxidase subunit I gene (COI) from 11 invertebrate phyla: Echinodermata, Mollusca, Annelida, Pogonophora, Arthropoda, Nemertinea, Echiura, Sipuncula, Platyhelminthes, Tardigrada, and Coelenterata, as well as the putative phylum Vestimentifera. Preliminary comparisons revealed that these COI primers generate informative sequences for phylogenetic analyses at the species and higher taxonomic levels.
Rates of nucleotide substitution for nuclear genes are thought to be governed primarily by the number of germ line replication events (the so-called "generation time" hypothesis). In contrast, rates of mitochondrial DNA evolution appear to be set primarily by DNA damage pathways of mutation mediated by mutagenic by-products of oxidative phosphorylation (the so-called "metabolic-rate" hypothesis). Comparison of synonymous substitution rates estimated for the mitochondrial cytochrome b gene and nuclear-encoded dlx, hsp70, and RAG-1 genes in mammals and sharks shows that rates of molecular evolution for sharks are approximately an order of magnitude slower than those for mammals for both nuclear and mitochondrial genes. In addition, there is significant positive covariation of substitution rate for mitochondrial and nuclear genes within sharks. These results, interpreted in light of the pervasiveness of DNA damage by mutagenic by-products of oxygen metabolism to both nuclear and mitochondrial genes and coupled with increasing evidence for cross-genome activity of DNA repair enzymes, suggest that molecular clocks for mitochondrial and nuclear genes may be set primarily by common mutational mechanisms.
Emerging infectious diseases (EIDs) of free-living wild animals can be classified into three major groups on the basis of
key epizootiological criteria: (i) EIDs associated with “spill-over” from domestic animals to wildlife populations living
in proximity; (ii) EIDs related directly to human intervention, via host or parasite translocations; and (iii) EIDs with no
overt human or domestic animal involvement. These phenomena have two major biological implications: first, many wildlife species
are reservoirs of pathogens that threaten domestic animal and human health; second, wildlife EIDs pose a substantial threat
to the conservation of global biodiversity.
Sixty-two brown anoles, Anolis sagrei, from Oahu, Hawaii were examined for helminths. Anolis sagrei was introduced to Hawaii, presumably from the Caribbean. Two species of trematodes, Mesocoelium monas and Platynosomum fastosum, 3 species of nematodes, Atractis scelopori, Physaloptera squamatae, and Physocephalus sp., 1 acanthocephalan, Acanthocephalus bufonis, and 1 pentastome, Raillietiella frenatus, were found. Atractis scelopori and P. squamatae, previously unknown in Hawaii, are widely distributed in the Caribbean and were most likely transported to Hawaii with the introduced anoles. Mesocoelium monas, P. fastosum, Physocephalus sp., A. bufonis, and R. frenatus have been previously reported from Hawaiian herptiles; A. sagrei most likely acquired infections of these parasites from Hawaiian populations. This study indicates that helminths can be transported with their introduced hosts and become established in the colonized areas and that introduced lizards may quickly acquire species of previously established helminthes.
The pentastome Raillietiella indica was collected from the introduced toad Bufo marinus in Oahu, Hawaii, U.S.A. The parasite was identified as R. indica from similarities in morphology of the hooks, buccal cadre, and male copulatory spicule. This represents a new host record for this parasite, previously only recorded from Bufo melanostictus. This also represents a new locality record because this parasite has only been reported previously in India, Burma, and Taiwan. This is the third record of B. marinus as a host for parasites in Hawaii.
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.
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.
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.
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.
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.
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.
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.
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
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
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
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.
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.
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.
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- J W O Ballard
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Un linguatulide nouveau parasite d'un batracien
- L Gedoelst
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Analyses of the effects of an exotic lizard (Anolis sagrei) on a native lizard (Anolis carolinensis) in Florida, using islands as experimental units
- T S Campbell
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(Anolis sagrei) on a native lizard (Anolis carolinensis) in
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
- C D Criscione
CRISCIONE, C. D. 2000. 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. M.S. Thesis, Southeastern Louisiana
University, Hammond, Louisiana, 146 p.
Naturalized reptiles and amphibians of the world
- C Lever
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Oxford University Press, Oxford, U.K., 318 p.