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Rebecca A. Cole

Publications and source records attributed to Rebecca A. Cole.

At least 19 recordsLinked to original sources

Physiological impacts of sublethal Cyathocotyle bushiensis and Sphaeridiotrema pseudoglobulus infections in captive Lesser Scaup (Aythya affinis)

Thousands of Lesser Scaup ( Aythya affinis ) die annually in the Upper Mississippi River System, USA, from intestinal infections after birds consume exotic faucet snails, Bithynia tentaculata , infected with introduced parasites, Cyathocotyle bushiensis and Sphaeridiotrema pseudoglobulus . To date, the low frequency (biannual) and magnitude of mortality events from intestinal infections likely prevents trematode mortalities from being a major contributor to Lesser Scaup population declines. However, questions remain regarding the role sublethal infections may have on Lesser Scaup fitness along with the potential for carryover effects in the following breeding season. We examined the impact of a single sublethal C. bushiensis and S. pseudoglobulus infection on select physiological parameters in Lesser Scaup over a 10-day period post inoculation through three trials, each involving three experimental groups: baseline control, trial control, and treatment ( n = 96 scaup). We found that male Lesser Scaup that were in better body condition before the trial had fewer C. bushiensis and Sphaeridiotrema pseudoglobulus recovered from their intestines at necropsy. Individuals with the highest numbers of C. bushiensis and S. pseudoglobulus in their intestines lost the largest amounts of body mass during the trial. We found that blood urea nitrogen and triglycerides were lower when C. bushiensis and S. pseudoglobulus were present. Triglycerides and glucose declined from Day 0 to Day 5 but stabilized on Day 10 of the trial. Our results highlight changes in physiological metrics in Lesser Scaup from a sublethal infection with C. bushiensis and S. pseudoglobulus under experimental conditions. Changes in Lesser Scaup health parameters indicated that scaup surviving a single sublethal trematode infection may have reduced body condition, which could lead to negative health implications in the following breeding season.

Wilson Journal of Ornithology

Lessons learned from using wild-caught and captive-reared lesser scaup (Aythya affinis) in captive experiments

Waterfowl are housed in captivity for research studies that are infeasible in the wild. Accommodating the unique requirements of semi-aquatic species in captivity while meeting experimental design criteria for research questions can be challenging and may have unknown effects on animal health. Thus, testing and standardizing best husbandry and care practices for waterfowl is necessary to facilitate proper husbandry and humane care while ensuring reliable and repeatable research results. To inform husbandry practices for captive-reared and wild-caught lesser scaup ( Aythya affinis ; hereafter, scaup), we assessed body mass and fat composition across two different aspects of husbandry, source population (captive-reared or wild caught), and housing densities (birds/m 2 ). Our results suggest that housing scaup at low densities (≤0.6 m 2 /bird, P = 0.049) relative to other species can minimize negative health effects. Captive-reared scaup were heavier ( P = 0.027) with greater body fat ( P < 0.001) and exhibited fewer signs of stress during handling than wild-caught scaup. In our experience, scaup which are captive-reared from eggs collected in the wild were better for long-term captivity studies as they maintained body mass between and recovered lost body mass following trials. Researchers would benefit from carefully evaluating the tradeoffs of using short- and long-term captive methods on their research question before designing projects, husbandry practices, and housing facilities for waterfowl.

Translational Animal Science

Morbidity in California giant salamander (Dicamptodon ensatus Eschscholtz, 1833) caused by Euryhelmis sp. Poche, 1926 (Trematoda: Heterophyiidae)

In the fall of 2021, California Department of Fish and Wildlife reported larval and adult California giant salamanders ( Dicamptodon ensatus Eschscholtz, 1833) with skin lesions at multiple creeks in Santa Clara and Santa Cruz Counties, California, USA. Field signs in both stages included rough, lumpy textured skin, and larvae with tails that were disproportionately long, flat, wavy, and flaccid. Presence of large-bodied larvae suggested delayed metamorphosis, with some larvae having cloudy eyes and suspected blindness. To determine the cause of the disease, three first-of-the-year salamanders from one location were collected, euthanized with 20% benzocaine, and submitted for necropsy to the U.S. Geological Survey, National Wildlife Health Center. Upon gross examination, all salamanders were emaciated with no internal fat stores, and had multiple pinpoint to 1.5-mm diameter raised nodules in the skin over the body, including the head, gills, dorsum, ventrum, all four limbs, and the tail; one also had nodules in the oral cavity and tongue. Histologically all salamanders had multiple encysted metacercariae in the dermis, subcutis, and skeletal muscles of the head, body, and tail that were often associated with granulomatous and granulocytic inflammation and edema. A small number of encysted meta cercariae or empty cysts were present in the gills with minimal inflammation, and rarely in the kidney with no associated inflammation. Morphology of live metacercariae (Trematoda: Heterophyiidae), and sequencing of the 28S rRNA gene identified a species of Euryhelmis (Poche, 1926). Artificial digestion of a 1.65 g, decapitated, eviscerated carcass yielded 773 metacercariae, all of similar size and morphology as the live specimens. Based on these findings, the poor body condition of these salamanders was concluded to be due to heavy parasite burden. Environmental factors such as drought, increased temperature, and overcrowded conditions may be exacerbating parasite infections in these populations of salamander.

California

Considerations for colorblind individuals on selecting colorimetric or fluorescent dye assay outcomes

A disadvantage of colorimetric detection in nucleic acid amplification assays is the possibility that a colorblind individual may interpret colors differently than observers with full-color vision. Using an isothermal amplification assay, the ability of colorblind individuals to distinguish between positive and negative results for four dyes was tested. Five individuals with self-reported colorblindness and four with full-color vision reported their observations of the color of the solution. Although colorblind individuals may accurately interpret assay results, they were often not accurate in reporting the color. Hydroxynaphthol blue was the most problematic dye, and both phenol red and SYBR™ green were less troublesome. Consideration for colorblind individuals is warranted when developing an assay and training staff in its performance.

BioTechniques

Epistylis spp. infestation in two species of mud turtles (Kinosternon spp.) in the American Southwest

The protistan genus Epistylis contains freshwater colonial species that attach to aquatic organisms in an epibiotic or parasitic relationship. They are known to attach to the epidermis and shells of aquatic turtles, but have not been reported to cause heavy infestations or morbidity in turtles. We documented heavy infestations of Epistylis spp. in several populations of Sonoran mud turtles ( Kinosternon sonoriense ) inhabiting livestock ponds in Arizona, USA, and rough-footed mud turtles ( Kinosternon hirtipes ) from livestock ponds in Texas, USA, over the course of several years. Severe Epistylis spp. infestations on mud turtles appeared to alter diving and swimming behavior when compared to uninfested conspecifics. Infestations were cleared in captivity using tap water or a 10% salt solution, and the turtles had no permanent damage to their shell or epidermis upon clearing. While several of the mud turtles we observed had poor body condition, it is possible that the severe infestations we observed were caused by a comorbidity associated with a pathogen, parasite, or poor habitat quality that made the turtles more susceptible to the Epistylis spp. infestation. Further research on causes for these severe infestations are warranted because they contribute to changes in behavior of the heavily infested turtles and may contribute to morbidity in Kinosternon spp. when mud turtles inhabit extremely warm, shallow, eutrophic aquatic habitats, such as livestock ponds.

Arizona

A novel gonadotropic microsporidian parasite (Microsporidium clinchi n. sp.) infecting a declining population of pheasantshell mussels (Actinonaias pectorosa) (Unioinidae) from the Clinch River, USA

Freshwater mussels of the order Unionida are among the most endangered animal groups globally, but the causes of their population decline are often enigmatic, with little known about the role of disease. In 2018, we collected wild adult pheasantshell ( Actinonaias pectorosa ) and mucket ( Actinonaias ligamentina ) during an epidemiologic survey investigating an ongoing mussel mass mortality event in the Clinch River, Virginia and Tennessee, USA. Histopathology and transmission electron microscopy showed a novel microsporidian parasite primarily infecting the ovary of pheasantshell. Sequencing of the small subunit rRNA gene produced a 1333 bp sequence with the greatest similarity to Pseudonosema cristatellae (AF484694.1; 86.36%; e-value = 0), a microsporidium infecting the freshwater bryozoan ( Cristatella mucedo ). Microsporidia were observed in 65% (17/26) of the examined female pheasantshell ( A. pectorosa ) and in no (0/2) female muckets ( A. ligamentina ) and occurred at mortality and non-mortality sites. Our findings indicate that a novel parasite, Microsporidium clinchi n. sp., is present in pheasantshell in the Clinch River, and while likely not a cause of mass mortality, could reduce fecundity and recruitment in this declining population and threaten the success of reintroductions. Surveillance of M. clinchi n. sp. and evaluation of broodstock and their progeny for microsporidia would therefore be prudent.

Tennessee, Virginia

Acute mortality in California tiger salamander (Ambystoma californiense) and Santa Cruz long-toed salamander (Ambystoma macrodactylum croceum) caused by Ribeiroia ondatrae (Class: Trematoda)

In early September 2019, a morbidity and mortality event affecting California tiger salamanders ( Ambystoma californiense ) and Santa Cruz long-toed salamanders ( Ambystoma macrodactylum croceum ) in late stages of metamorphosis was reported at a National Wildlife Refuge in Santa Cruz County, California, U.S.A. During the postmortem disease investigation, severe integumentary metacercarial (Class: Trematoda) infection, associated with widespread skin lesions, was observed. Planorbid snails collected from the ponds of the refuge within seven days of the mortality event were infected with Ribeiroia ondatrae, a digenetic trematode that can cause malformation and death in some amphibians. We suggest sustained seasonal high-water levels due to active habitat management along with several years of increased rainfall led to increased bird visitation, increased over-wintering of snails, and prolonged salamander metamorphosis, resulting in a confluence of conditions and cascading of host-parasite dynamics to create a hyper-parasitized state.

California

Gapeworm (Syngamus spp.) prevalence in Wisconsin greater prairie chickens (Tympanuchus cupido pinnatus)

Under Wisconsin state law, the greater prairie chicken (GRPC; Tympanuchus cupido pinnatus ) has been listed as a threatened species since 1976. In 2014–15, we conducted a pilot study to determine the prevalence and intensity of gapeworms ( Syngamus spp.) in female Wisconsin GRPCs collected from 2 monitored populations. We captured 62 female GRPCs using walk-in-style traps for females and night lighting for juveniles ≥45 days of age. From these individuals, we collected 15 carcasses of radio-marked birds, most of whom died due to predation events. Through dissection, we identified gapeworm in 20% of examined carcasses and report an intensity ranging between 4 and 74 worms.

Wisconsin

Diplotriaena obtusa (Nematoda: Diplotriaenidae) from barn swallows (Hirundo rustica) and cliff swallows (Petrochelidon pyrrhonota) collected during mortality events in the Upper Midwest, USA

Several mortality events involving barn swallows ( Hirundo rustica ) and cliff swallows ( Petrochelidon pyrrhonota ) were reported in the Upper Midwestern states in 2017 and 2018. Barn swallow mortality followed unseasonal cold snaps, with the primary cause of death being emaciation with concurrent air sac nematodiasis. Lesions in cliff swallows were consistent with blunt force trauma from suspected car impacts. Examination of air sac nematodes from both bird species revealed morphological characters consistent with Diplotriaena obtusa . Sequence analysis of the partial 18S rRNA gene indicated the samples clustered with other species in the genus Diplotriaena . These nematodes provide a link between morphological specimens and DNA sequence data for D. obtusa .

Illinois, Minnesota, Nebraska, South Dakota

Loop-mediated isothermal amplification (LAMP) assay for detection of Asian fish tapeworm, Schyzocotyle acheilognathi (Yamaguti, 1934) [syn. Bothriocephalus acheilognathi]

The Asian fish tapeworm ( Schyzocotyle acheilognathi syn. Bothriocephalus acheilognathi ) (AFT) is an invasive parasite that can infect many species of fish, although most hosts are primarily members of Cyprinidae. Pathogenicity has most often been reported in aquaculture settings in fry and fingerling stages of carp ( Cyprinus spp.). More recently, it has been shown to cause growth retardation in the endangered bonytail chub ( Gila elegans ) and found to be widespread in populations of endangered humpback chub ( Gila cypha ) in the Colorado River, Grand Canyon, Arizona. AFT spreads most often through the transport of infected fish, particularly baitfish. Despite its harmful potential, there is no efficient or accurate ante mortem test to detect AFT in water or fish samples before transport. Herein, we report on the development of a sensitive and specific loop-mediated isothermal amplification (LAMP) assay to detect the parasite in under 30 min from laboratory prepared samples. Six LAMP primers were designed to amplify a variable region of the 18S ribosomal RNA gene in AFT with the detection and quantification of DNA on a real-time fluorometer. The limit of detection was 1 × 10 1 copies/µl of DNA extracted from as few as 2 AFT eggs. Future application of our assay would be a low-cost test to rapidly and accurately detect AFT DNA from environmental samples on-site so that preventive actions can be taken to halt the spread of the AFT through the movement of infected fish.

Journal of Parasitology

Life cycle of the trout cecal nematode, Truttaedacnitis truttae (Nematoda: Cucullanidae): Experimental and field observations

Truttaedacnitis truttae is a cucullanid nematode of primarily salmonine fishes. Brown trout ( Salmo trutta ) in Europe reportedly become parasitized by ingesting lampreys ( Lampetra planeri ) carrying infective larvae. However, our field and laboratory observations suggested that North American specimens of T. truttae have an alternative life cycle. High abundances and potential impact of T. truttae in rainbow trout, Oncorhynchus mykiss , in the Colorado River drainage in Grand Canyon, where there are no lampreys, prompted a study on the transmission dynamics of this nematode. Eggs of T. truttae , collected from live gravid females, were incubated in the laboratory. Snails, Physa gyrina and Lymnaea sp., were exposed to T. truttae larvae 3–4 wk later. Active larvae of T. truttae were observed penetrating the intestinal wall of exposed snails, and worm larvae were found in the visceral tissues when examined 1 wk after exposure. Larvae in snails showed little growth and development 2 wk later and corresponded to L3 larvae. Infected snails were fed to hatchery-reared juvenile rainbow trout. Developing stages were subsequently found in the mucosal lining and lumen of trout intestines. Adult male and female (gravid) worms were found in the ceca of trout examined 5–6 mo after consuming infected snails. Larvae found in pepsin/trypsin digests and mucosal scrapings from wild, naturally infected, trout corroborate laboratory findings. Screening of Physa sp. and gammarids collected from Colorado River, Grand Canyon, for natural infections with T. truttae using the ITS1 rDNA marker gave positive results. Truttaedacnitis truttae is the second species, after Truttaedacnitis clitellarius of lake sturgeon, capable of using a snail first intermediate/paratenic host and is similar to several other cucullanids in having a histotropic phase of development in the definitive fish host.

Arizona

Associations of intestinal helminth infections with health parameters of spring-migrating female lesser scaup (Aythya affinis) in the upper Midwest, USA

Thousands of lesser scaup ( Aythya affinis ) die during spring and fall migrations through the upper Midwest, USA, from infections with Cyathocotyle bushiensis and Sphaeridiotrema spp. (Class: Trematoda) after ingesting infected intermediate hosts, such as non-native faucet snails ( Bithynia tentaculata ). The lesser scaup is a species of conservation concern and is highly susceptible to these infections. We collected female lesser scaup from spring migratory stopover locations throughout Illinois and Wisconsin and assessed biochemical and morphological indicators of health in relation to intestinal helminth loads. Helminth species diversity, total trematode abundance, and the infection intensities of the trematodes C. bushiensis and Sphaeridiotrema spp. were associated with percent body fat, blood metabolites, hematological measures, and an index of foraging habitat quality. Helminth diversity was negatively associated with percent body fat, albumin concentrations, and monocytes, whereas glucose concentrations displayed a slight, positive association. Total trematode abundance was negatively associated with blood concentrations of non-esterified fatty acids and albumin. Infections of C. bushiensis were positively related to basophil levels, whereas Sphaeridiotrema spp. infection intensity was negatively associated with packed cell volume and foraging habitat quality. Thus, commonly measured health metrics may indicate intestinal parasite infections and help waterfowl managers understand overall habitat quality. Intestinal parasitic loads offer another plausible mechanism underlying the spring condition hypothesis.

Parasitology Research

Mass mortality attributed to acanthocephaliasis at a Gull-billed Tern (Gelochelidon nilotica) colony in coastal California

From 12 May 2013 to 29 May 2013, the Gull-billed Tern ( Gelochelidon nilotica ) colony at the San Diego Bay National Wildlife Refuge, California, experienced a mass die-off of at least 92 adults, representing 71–92% of the breeding population on the US west coast. Cause of death was determined to be peritonitis due to perforations of the intestine by a large quantity of acanthocephala ( Profilicolis [= Polymorphus ] altmani ). This is a unique report of P. altmani infecting G. nilotica , and a report of a great impact to a tern population in southern California. Mole crabs ( Emerita analoga ), the intermediate host for P. altmani and a major component of the Gull-billed Tern diet in San Diego, were found in the stomachs of necropsied terns along with cystacanths, and are the presumed source of the parasite infection. The tern's dietary reliance upon mole crabs likely amplified parasite transmission and infection. We suggest additional research to determine factors that influence parasite infection of intermediate and definitive hosts, particularly mole crabs, given that they are a vital resource for migrating birds within the coastal zone.

California

Spatiotemporal distributions of intestinal helminths in female lesser scaup Aythya affinis during spring migration from the upper Midwest, USA

We examined the associations between intestinal helminth infracommunity structure and infection parameters and the age, size, and year and region of collection of 130 female lesser scaup ( Aythya affinis ) during their 2014&ndash;2015 spring migrations through the upper Midwest, USA. We identified a total of 647,174 individual helminths from 40 taxa, including 20 trematodes, 14 cestodes, 4 nematodes and 2 acanthocephalans parasitizing lesser scaup within the study area. Lesser scaup were each infected with 2&ndash;23 helminth taxa. One digenean, Plenosoma minimum , is reported for the first time in lesser scaup and in the Midwest. Mean trematode abundance and total helminth abundance was significantly less in 2015 than 2014, and we suspect that colder weather late in 2015 impacted the intermediate host fauna and caused the observed differences. Brillouin's species diversity of helminths was greatest in the northernmost region of the study area, which coincides with the range of a non-indigenous snail that indirectly causes annual mortality events of lesser scaup. While host age and size were not determined to be influential factors of helminth infracommunity structure, non-parametric ordination and permutational analysis of co-variance revealed that year and region of collection explained differences in helminth infracommunities. Our results suggest that spatiotemporal variations play an important role in the structure of intestinal helminth infracommunities found in migrating lesser scaup hosts, and may therefore impact host ability to build endogenous reserves at certain stopover locations in the Midwest.

Journal of Helminthology

Genetic structure of faucet snail, Bithynia tentaculata populations in North Americal based on microsattelite markers

Bithynia tentaculata is believed to have been extirpated from North America during the last glacial maximum. It was reintroduced into North America via the Great Lakes basin in the 1800’s and has recently been expanding its geographic range. This snail serves as intermediate host for three trematodes that cause extensive recurring morbidity and mortality events in migratory water birds along the Mississippi River. Using twelve microsatellite loci for ~200 individual snails from 11 populations in North America and Europe, we examined one of the three major geographic regions from which founding populations into the Great Lakes typically originate. Our data supports a single recolonization of North America into the Great Lakes Basin followed by subsequent introduction events from the Great Lakes to other large watersheds in North America. However, additional watersheds in Europe require sampling to confirm this result. No populations with genetic signatures indicative of North American glacial relics were found. The initial invasion of North America was likely not from the Ponto-Caspian basin, the usual source of freshwater invasive species to the Laurentian Great Lakes.

Freshwater Mollusk Biology and Conservation