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Geology topics

Matthew M. Smith

Publications and source records attributed to Matthew M. Smith.

14 recordsLinked to original sources

Paralytic shellfish toxins and seabirds: Evaluating sublethal effects, behavioral responses, and ecological implications of saxitoxin ingestion by common murres (Uria aalge)

Paralytic shellfish toxins (PSTs), including saxitoxin (STX) and its congeners, are neurotoxins that can be produced during harmful algal blooms and cause illness or death in humans, fish, seabirds, and marine mammals. Since 2014, multiple large-scale seabird mortality events have occurred in Alaska waters, with STXs detected in some carcasses. To investigate the sublethal behavioral and ecological effects of STX on seabirds, we conducted captive dosing trials with common murres ( Uria aalge ). We gavaged purified STX (dehydrated STX dihydrocholoride, STX-diHCl) or an Alexandrium catenella culture extract into murres, monitored behavioral responses and recovery times, and assessed tissue concentrations in individuals that died or were euthanized. Using a modified up-and-down dose-finding scheme, we estimated a median effective dose (ED 50 ) of 89 µg STX-equivalents (eq) kg -1 for STX-diHCl and 366 µg STX-eq kg -1 for the A. catenella extract based on ecologically relevant behavior. Differences between the ED 50 estimates could reflect uncertainties in toxin equivalency factors for PST congeners, which are based on studies using purified toxins in mice and may vary across taxa or toxin matrices. Post-dosing concentrations of STX varied by tissue type across individuals, with quantifiable levels ranging from 3 to 379 µg STX-eq 100g -1 . Evidence of biotransformation of STX in A. catenella extract-dosed birds was observed. We also measured the chronic effects of dosing with sublethal levels of STX-diHCl over seven-days, which resulted in lower fish intake among treatment birds compared to controls (-187 g day -1 ). This investigation improves our understanding of the ecological effects of PSTs on seabird health.

Alaska

Partnering in search of answers: Seabird die-offs in the Bering and Chukchi Seas

Prior to 2015, seabird die-offs in Alaskan waters were rare; they typically occurred in mid-winter, linked to epizootic disease events or above-average ocean temperatures associated with strong El Nino-Southern Oscillation events (Bodenstein et al. 2015, Jones et al. 2019, Romano et al. 2020). Since 2015, the U.S. Fish and Wildlife Service (USFWS) has monitored mortality events that have become annual occurrences in Alaska (Fig. 1). Since 2017, communities on the coasts of the northern Bering and southern Chukchi Seas have annually observed dead and dying seabirds along their coasts, although such die-offs have not been reported from communities north of Point Hope. (Fig. 2). Affected species included planktivorous birds such as auklets ( Aethia spp.) and shearwaters ( Ardenna spp.), piscivorous murres ( Uria spp.), puffins ( Fratercula spp.), and kittiwakes ( Rissa spp.), as well as low numbers of benthic feeding sea ducks ( Somateria spp.). The range of seabird species and the different prey species involved, with localized events throughout summer and over widespread areas, indicate environmental causes at multiple trophic levels. Such wildlife mortality events are a public health concern for coastal communities that rely on ocean resources for their nutritional, cultural, and economic well-being. They have also been seen as a harbinger of concern for the state of the Arctic Ocean itself.

Alaska

Paralytic shellfish toxins associated with Arctic Tern mortalities in Alaska

Harmful algal blooms produce biotoxins that can injure or kill fish, wildlife, and humans. These blooms occur naturally but have intensified in many locations globally due to recent climatic changes, including ocean warming. Such changes are especially pronounced in northern regions, where the effects of paralytic shellfish toxins (PSTs) on marine wildlife are of growing concern. In Alaska, seabird mortality events have increased in frequency, magnitude, and duration since 2015 alongside anomalously high ocean temperatures. Although starvation has been implicated as the apparent cause of death in many of these die-offs, saxitoxin (STX) and other PSTs have been identified as possible contributing factors. Here, we describe a mortality event at a nesting colony of Arctic Terns ( Sterna paradisaea ) near Juneau, Alaska in 2019 and report elevated concentrations of PSTs in bird, forage fish, and mussel samples. Concentrations of STX and other PSTs in tern tissues (2.5–51.2 µg 100g −1 STX-equivalents [STX-eq]) were of similar magnitude to those reported from other PST-induced bird die-offs. We documented high PST concentrations in blue mussels (>11,000 µg 100g −1 STX-eq; Mytilus edulis spp.) collected from nearby beaches, as well as in forage fish (up to 494 µg 100g −1 STX-eq) retrieved from Arctic Tern nests, thereby providing direct evidence of PST exposure via the terns’ prey. At maximum concentrations measured in this study, a single 5 g Pacific Sand Lance ( Ammodytes personatus ) could exceed the median lethal STX dose (LD 50 ) currently estimated for birds, offering strong support for PSTs as a likely source of tern mortality. In addition to describing this localized bird mortality event, we used existing energetics data from adult and nestling Arctic Terns to calculate estimated cumulative daily PST exposure based on ecologically relevant concentrations in forage fish. Our estimates revealed potentially lethal levels of PST exposure even at relatively low (≤30 ug 100g −1 STX-eq) toxin concentrations in prey. These findings suggest that PSTs present a significant hazard to Arctic Terns and other northern seabirds and should be included in future investigations of avian mortality events as well as assessments of population health.

Alaska

A serological survey of Francisella tularensis exposure in wildlife on the Arctic Coastal Plain of Alaska

Tularemia is an infectious zoonotic disease caused by one of several subspecies of Francisella tularensis bacteria. Infections by F. tularensis are common throughout the northern hemisphere and have been detected in more than 250 wildlife species. In Alaska, US, where the pathogen was first identified in 1938, studies have identified F. tularensis antibodies in a diverse suite of taxa, including insects, birds, and mammals. However, few such investigations have been conducted recently and knowledge about the current distribution and disease ecology of F. tularensis is limited, particularly in Arctic Alaska, an area undergoing rapid environmental changes from climate warming. To help address these information gaps and provide insights about patterns of exposure among wildlife, we assessed the seroprevalence of F. tularensis antibodies in mammals and tundra-nesting geese from the Arctic Coastal Plain of Alaska, 2014–17. With a commercially available slide agglutination test, we detected antibodies in 14.7% of all individuals sampled ( n =722), with titers ranging from 1:20 to 1:320. We detected significant differences in seroprevalence between family groups, with Canidae (foxes, Vulpes spp.) and Sciuridae (Arctic ground squirrel, Spermophilus parryii ) having the highest seroprevalence at 21.5% and 33.3%, respectively. Mean seroprevalence for Ursidae (polar bears, Ursus maritimus ) was 13.3%, whereas Cervidae (caribou, Rangifer tarandus ) had comparatively low seroprevalence at 6.5%. Antibodies were detected in all Anatidae species sampled, with Black Brant ( Branta bernicla nigricans ) having the highest seroprevalence at 13.6%. The detection of F. tularensis antibodies across multiple taxa from the Arctic Coastal Plain and its nearshore marine region provides evidence of exposure to this pathogen throughout the region and highlights the need for renewed surveillance in Alaska.

Alaska

Acute oral toxicity and tissue residues of saxitoxin in the mallard (Anas platyrhynchos)

Since 2014, widespread, annual mortality events involving multiple species of seabirds have occurred in the Gulf of Alaska, Bering Sea, and Chukchi Sea. Among these die-offs, emaciation was a common finding with starvation often identified as the cause of death. However, saxitoxin (STX) was detected in many carcasses, indicating exposure of these seabirds to STX in the marine environment. Few data are available that describe the effects of STX in birds, thus presenting challenges for determining its contributions to specific mortality events. To address these knowledge gaps, we conducted an acute oral toxicity trial in mallards ( Anas platyrhynchos ), a common laboratory avian model, using an up-and-down method to estimate the median lethal dose (LD 50 ) for STX. Using an enzyme-linked immunosorbent assay (ELISA), we tested select tissues from all birds and feces from those individuals that survived initial dosing. Samples with an ELISA result that exceeded approximately 10 µg 100 g −1 STX and randomly selected ELISA negative samples were further tested by high-performance liquid chromatography (HPLC). Tissues collected from mallards were also examined grossly at necropsy and then later by microscopy to identify lesions attributable to STX. The estimated LD 50 was 167 µg kg −1 (95% CI = 69–275 µg kg −1 ). Saxitoxin was detected in fecal samples of all mallards tested for up to 48 h after dosing and at the end of the sampling period (7 d) in three birds. In those individuals that died or were euthanized <2 h after dosing, STX was readily detected throughout the gastrointestinal tract but only infrequently in heart, kidney, liver, lung, and breast muscle. No gross or microscopic lesions were observed that could be attributable to STX exposure. Given its acute toxicity, limited detectability, and frequent occurrence in the Alaska marine environment, additional research on STX in seabirds is warranted.

Harmful Algae

Investigation of algal toxins in a multispecies seabird die-off in the Bering and Chukchi seas

Between 2014 and 2017, widespread seabird mortality events were documented annually in the Bering and Chukchi seas, concurrent with dramatic reductions of sea ice, warmer than average ocean temperatures, and rapid shifts in marine ecosystems. Among other changes in the marine environment, harmful algal blooms (HABs) that produce the neurotoxins saxitoxin (STX) and domoic acid (DA) have been identified as a growing concern in this region. Although STX and DA have been documented in Alaska (US) for decades, current projections suggest that the incidence of HABs is likely to increase with climate warming and may pose a threat to marine birds and other wildlife. In 2017, a multispecies die-off consisting of primarily Northern Fulmars ( Fulmarus glacialis ) and Short-tailed Shearwaters ( Ardenna tenuirostris ) occurred in the Bering and Chukchi seas. To evaluate whether algal toxins may have contributed to bird mortality, we tested carcasses collected from multiple locations in western and northern Alaska for STX and DA. We did not detect DA in any samples, but STX was present in 60% of all individuals tested and in 88% of Northern Fulmars. Toxin concentrations in Northern Fulmars were within the range of those reported from other STX-induced bird die-offs, suggesting that STX may have contributed to mortalities. However, direct neurotoxic action by STX could not be confirmed and starvation appeared to be the proximate cause of death among birds examined in this study.

Journal of Wildlife Diseases

Algal toxins in Alaskan seabirds: Evaluating the role of saxitoxin and domoic acid in a large-scale die-off of Common Murres

Elevated seawater temperatures are linked to the development of harmful algal blooms (HABs), which pose a growing threat to marine birds and other wildlife. During late 2015 and early 2016, a massive die-off of Common Murres (Uria algae; hereafter, murres) was observed in the Gulf of Alaska coincident with a strong marine heat wave. Previous studies have documented illness and death among seabirds resulting from exposure to the HAB neurotoxins saxitoxin (STX) and domoic acid (DA). Given the unusual mortality event, corresponding warm water anomalies, and recent detection of STX and DA throughout coastal Alaskan waters, HABs were identified as a possible factor of concern. To evaluate whether algal toxins may have contributed to murre deaths, we tested for STX and DA in a suite of tissues obtained from beach-cast murre carcasses associated with the die-off as well as from apparently healthy murres and Black-legged Kittiwakes (Rissa tridactyla; hereafter, kittiwakes) in the preceding and following summers. We also tested forage fish and marine invertebrates collected in the Gulf of Alaska in 2015–2017 to evaluate potential sources of HAB toxin exposure for seabirds. Saxitoxin was present in multiple tissue types of both die-off (36.4%) and healthy (41.7%) murres and healthy kittiwakes (54.2%). Among birds, we detected the highest concentrations of STX in liver tissues (range 1.4 –10.8 µg 100 g-1) of die-off murres. Saxitoxin was relatively common in forage fish (20.3%) and marine invertebrates (53.8%). No established toxicity limits currently exist for seabirds, but concentrations of STX in birds and forage fish in our study were lower than values reported from most other bird die-offs in which STX intoxication was causally linked. We detected low concentrations of DA in a single bird sample and in 33.3% of marine invertebrates and 4.0% of forage fish samples. Although these results do not support the hypothesis that acute exposure to STX or DA was a primary factor in the 2015–2016 die-off event, additional information about the sensitivity of murres to these toxins is needed before we can discount their potential role in the die-off. The widespread occurrence of STX in seabirds, forage fish, and marine invertebrates in the Gulf of Alaska indicates that algal toxins should be considered in future assessments of seabird health, especially given the potential for greater occurrence of HABs in the future.

Alaska

Prevalence and diversity of avian blood parasites in a resident northern passerine

Background: Climate-related changes are expected to influence the prevalence and distribution of vector-borne haemosporidian parasites at northern latitudes, although baseline information about resident birds is still lacking. In this study, we investigated prevalence and genetic diversity of Plasmodium, Haemoproteus, and Leucocytozoon parasites infecting the Northwestern Crow (Corvus caurinus), a non-migratory passerine with unique life-history characteristics. This species occupies both intertidal and forested habitats and is subject to high prevalence of avian keratin disorder (AKD), a disease that causes gross beak deformities. Investigation of avian blood parasites in Northwestern Crows at sites broadly distributed across coastal Alaska provided an opportunity to evaluate specific host factors related to parasite infection status and assess geographic patterns of prevalence. Results: We used molecular methods to screen for haemosporidian parasites in Northwestern Crows and estimated genus-specific parasite prevalence with occupancy modeling that accounts for imperfect detection of parasite infection. We observed considerable geographic and annual variation in prevalence of Plasmodium, Haemoproteus, and Leucocytozoon , but these patterns were not correlated with indices of local climatic conditions. Our models also did not provide support for relationships between the probability of parasite infection and body condition or the occurrence of co-infections with other parasite genera or clinical signs of AKD. In our phylogenetic analyses, we identified multiple lineages of each parasite genus, with Leucocytozoon showing greater diversity than Plasmodium or Haemoproteus. Conclusions: Results from this study expand our knowledge about the prevalence and diversity of avian blood parasites in northern resident birds as well as corvids worldwide. We detected all three genera of avian haemosporidians in Northwestern Crows in Alaska, although only Leucocytozoon occurred at all sites in both years. Given the strong geographic and interannual variation in parasite prevalence and apparent lack of correlation with climatic variables, it appears that there are other key factors responsible for driving transmission dynamics in this region. Thus, caution is warranted when using standard climatic or geographic attributes in a predictive framework. Our phylogenetic results demonstrate lower host specificity for some lineages of Leucocytozoon than is typically reported and provide insights about genetic diversity of local haemosporidian parasites in Alaska.

Parasites & Vectors

Evidence of Culiseta mosquitoes as vectors for Plasmodium parasites in Alaska

Mosquito vectors play a crucial role in the distribution of avian Plasmodium parasites worldwide. At northern latitudes, where climate warming is most pronounced, there are questions about possible changes in the abundance and distribution of Plasmodium parasites, their vectors, and their impacts to avian hosts. To better understand the transmission of Plasmodium among local birds and to gather baseline data on potential vectors, we sampled a total of 3,909 mosquitoes from three locations in south‐central Alaska during the summer of 2016. We screened mosquitoes for the presence of Plasmodium parasites using molecular techniques and estimated Plasmodium infection rates per 1,000 mosquitoes using maximum likelihood methods. We found low estimated infection rates across all mosquitoes (1.28 per 1,000), with significantly higher rates in Culiseta mosquitoes (7.91 per 1,000) than in Aedes mosquitoes (0.57 per 1,000). We detected Plasmodium in a single head/thorax sample of Culiseta , indicating potential for transmission of these parasites by mosquitoes of this genus. Plasmodium parasite DNA isolated from mosquitoes showed a 100% identity match to the BT7 Plasmodium lineage that has been detected in numerous avian species worldwide. Additionally, microscopic analysis of blood smears collected from black‐capped chickadees ( Poecile atricapillus ) at the same locations revealed infection by parasites preliminarily identified as Plasmodium circumflexum . Results from our study provide the first information on Plasmodium infection rates in Alaskan mosquitoes and evidence that Culiseta species may play a role in the transmission and maintenance of Plasmodium parasites in this region.

Alaska

Evidence for haemosporidian parasite infections in Spectacled Eiders (Somateria fischeri) sampled in Alaska during the breeding season

We assessed hematozoa infection in Spectacled Eiders ( Somateria fischeri ) at two areas in Alaska. No Haemoproteus or Plasmodium species were detected. Leucocytozoon prevalence was 6.5% for adults across sites and 41.9% for juveniles sampled in the Arctic, providing evidence for local transmission. All Leucocytozoon haplotypes were previously detected in waterfowl.

Alaska

Detection, prevalence, and transmission of avian hematozoa in waterfowl at the Arctic/sub-Arctic interface: co-infections, viral interactions, and sources of variation.

Background: The epidemiology of avian hematozoa at high latitudes is still not well understood, particularly in sub-Arctic and Arctic habitats, where information is limited regarding seasonality and range of transmission, co-infection dynamics with parasitic and viral agents, and possible fitness consequences of infection. Such information is important as climate warming may lead to northward expansion of hematozoa with unknown consequences to northern-breeding avian taxa, particularly populations that may be previously unexposed to blood parasites. Methods: We used molecular methods to screen blood samples and cloacal/oropharyngeal swabs collected from 1347 ducks of five species during May-August 2010, in interior Alaska, for the presence of hematozoa, Influenza A Virus (IAV), and IAV antibodies. Using models to account for imperfect detection of parasites, we estimated seasonal variation in prevalence of three parasite genera (Haemoproteus, Plasmodium, Leucocytozoon) and investigated how co-infection with parasites and viruses were related to the probability of infection. Results: We detected parasites from each hematozoan genus in adult and juvenile ducks of all species sampled. Seasonal patterns in detection and prevalence varied by parasite genus and species, age, and sex of duck hosts. The probabilities of infection for Haemoproteus and Leucocytozoon parasites were strongly positively correlated, but hematozoa infection was not correlated with IAV infection or serostatus. The probability of Haemoproteus infection was negatively related to body condition in juvenile ducks; relationships between Leucocytozoon infection and body condition varied among host species. Conclusions: We present prevalence estimates for Haemoproteus, Leucocytozoon, and Plasmodium infections in waterfowl at the interface of the sub-Arctic and Arctic and provide evidence for local transmission of all three parasite genera. Variation in prevalence and molecular detection of hematozoa parasites in wild ducks is influenced by seasonal timing and a number of host traits. A positive correlation in co-infection of Leucocytozoon and Haemoproteus suggests that infection probability by parasites in one or both genera is enhanced by infection with the other, or that encounter rates of hosts and genus-specific vectors are correlated. Using size-adjusted mass as an index of host condition, we did not find evidence for strong deleterious consequences of hematozoa infection in wild ducks.

Parasites & Vectors

Genetic diversity and host specificity varies across three genera of blood parasites in ducks of the Pacific Americas Flyway

Birds of the order Anseriformes, commonly referred to as waterfowl, are frequently infected by Haemosporidia of the genera Haemoproteus , Plasmodium , and Leucocytozoon via dipteran vectors. We analyzed nucleotide sequences of the Cytochrome b (Cyt b ) gene from parasites of these genera detected in six species of ducks from Alaska and California, USA to characterize the genetic diversity of Haemosporidia infecting waterfowl at two ends of the Pacific Americas Flyway. In addition, parasite Cyt b sequences were compared to those available on a public database to investigate specificity of genetic lineages to hosts of the order Anseriformes. Haplotype and nucleotide diversity of Haemoproteus Cyt b sequences was lower than was detected for Plasmodium and Leucocytozoon parasites. Although waterfowl are presumed to be infected by only a single species of Leucocytozoon , L . simondi , diversity indices were highest for haplotypes from this genus and sequences formed five distinct clades separated by genetic distances of 4.9%–7.6%, suggesting potential cryptic speciation. All Haemoproteus and Leucocytozoon haplotypes derived from waterfowl samples formed monophyletic clades in phylogenetic analyses and were unique to the order Anseriformes with few exceptions. In contrast, waterfowl-origin Plasmodium haplotypes were identical or closely related to lineages found in other avian orders. Our results suggest a more generalist strategy for Plasmodium parasites infecting North American waterfowl as compared to those of the genera Haemoproteus and Leucocytozoon .

PLoS ONE

Prevalence and genetic diversity of haematozoa in South American waterfowl and evidence for intercontinental redistribution of parasites by migratory birds

To understand the role of migratory birds in the movement and transmission of haematozoa within and between continental regions, we examined 804 blood samples collected from eleven endemic species of South American waterfowl in Peru and Argentina for infection by Haemoproteus , Plasmodium , and/or Leucocytozono blood parasites. Infections were detected in 25 individuals of six species for an overall apparent prevalence rate of 3.1%. Analysis of haematozoa mitochondrial DNA revealed twelve distinct parasite haplotypes infecting South American waterfowl, four of which were identical to lineages previously observed infecting ducks and swans sampled in North America. Analysis of parasite mitochondrial DNA sequences revealed close phylogenetic relationships between lineages originating from waterfowl samples regardless of continental affiliation. In contrast, more distant phylogenetic relationships were observed between parasite lineages from waterfowl and passerines sampled in South America for Haemoproteus and Leucocytozoon , suggesting some level of host specificity for parasites of these genera. The detection of identical parasite lineages in endemic, South American waterfowl and North American ducks and swans, paired with the close phylogenetic relationships of haematozoa infecting waterfowl on both continents, provides evidence for parasite redistribution between these regions by migratory birds.

International Journal for Parasitology: Parasites

A real-time, quantitative PCR protocol for assessing the relative parasitemia of Leucocytozoon in waterfowl

Microscopic examination of blood smears can be effective at diagnosing and quantifying hematozoa infections. However, this method requires highly trained observers, is time consuming, and may be inaccurate for detection of infections at low levels of parasitemia. To develop a molecular methodology for identifying and quantifying Leucocytozoon parasite infection in wild waterfowl (Anseriformes), we designed a real-time, quantitative PCR protocol to amplify Leucocytozoon mitochondrial DNA using TaqMan fluorogenic probes and validated our methodology using blood samples collected from waterfowl in interior Alaska during late summer and autumn (n = 105). By comparing our qPCR results to those derived from a widely used nested PCR protocol, we determined that our assay showed high levels of sensitivity (91%) and specificity (100%) in detecting Leucocytozoon DNA from host blood samples. Additionally, results of a linear regression revealed significant correlation between the raw measure of parasitemia produced by our qPCR assay (Ct values) and numbers of parasites observed on blood smears (R2 = 0.694, P = 0.003), indicating that our assay can reliably determine the relative parasitemia levels among samples. This methodology provides a powerful new tool for studies assessing effects of haemosporidian infection in wild avian species.

Journal of Microbiological Methods