Experimental vacuolar myelinopathy in red-tailed hawks

Avian vacuolar myelinopathy (AVM) was recognized in 1994 as a cause of wild bird mortality when 29 bald eagles (Haliaeetus leucocephalus) succumbed to the disease at DeGray Lake, Arkansas (USA). The cause of AVM and its source remain undetermined despite extensive diagnostic and research investigations. Two years later, when AVM killed 26 eagles in the same area in Arkansas, it became apparent that American coots (Fulica americana) had identical neurologic signs and lesions, and it was hypothesized that eagles acquired AVM via ingestion of affected coots. In order to test this hypothesis, we fed coot tissues (brain, liver, kidney, muscle, fat, and intestinal tract) to rehabilitated, non-releasable red-tailed hawks (Buteo jamaicensis). Five hawks received tissues from coots with AVM lesions, and one hawk received tissues from coots without brain lesions that had been collected at a site where AVM never has been documented. All hawks received 12-70 g/day (mean = 38 g) of coot tissues for 28 days. All six hawks remained clinically normal during the study. The birds were euthanatized on day 29 and microscopic lesions of AVM were found in all hawks that received tissues from affected coots, but not in the hawk that received tissues from unaffected coots. This marks the first time that AVM has been produced in birds under laboratory conditions and proves that birds of prey can acquire AVM via ingestion of tissues from affected coots.     

Failure to transmit avian vacuolar myelinopathy to mallard ducks

Avian vacuolar myelinopathy (AVM) is a neurologic disease that has been diagnosed in free-ranging birds in the southeastern United States. Bald eagles (Haliaeetus leuocephalus), American coots (Fulica americana), and mallards (Anas platyrhynchos) have been affected. Previous investigations have not determined the etiology of this disease. In November and December 2002, we attempted to induce AVM in game-farmed mallards through four, 7-day exposure trials. Mallards were housed in six groups of eight, with two of these groups serving as controls. One group was housed with AVM-affected coots; one group was tube fed daily with water from the lake where affected coots were captured; one group was tube fed daily with aquatic vegetation (Hydrilla verticillata) from the same lake; and another group was tube fed daily with sediment from the lake. No ducks exhibited clinical neurologic abnormalities consistent with AVM and no evidence of AVM was present at histopathologic examination of brain tissue. Although limitations in sample size, quantity of individual doses, frequency of dose administration, duration of exposure, and timing of these trials restrict the interpretation of the findings, AVM was not readily transmitted by direct contact, water, hydrilla, or sediment in this investigation.     

Attempts to identify the source of avian vacuolar myelinopathy for waterbirds

Attempts were made to reproduce avian vacuolar myelinopathy (AVM) in a number of test animals in order to determine the source of the causative agent for birds and to find a suitable animal model for future studies. Submerged vegetation, plankton, invertebrates, forage fish, and sediments were collected from three lakes with ongoing outbreaks of AVM and fed to American coots (Fulica americana), mallard ducks and ducklings (Anas platyrhynchos), quail (Coturnix japonica), and laboratory mice either via gavage or ad libitum. Tissues from AVM-affected coots with brain lesions were fed to ducklings, kestrels (Falco sparverius), and American crows (Corvus brachyrhynchos). Two mallards that ingested one sample of Hydrilla verticillata along with any biotic or abiotic material associated with its external surface developed brain lesions consistent with AVM, although neither of the ducks had clinical signs of disease. Ingestion of numerous other samples of Hydrilla from the AVM affected lakes and a lake with no prior history of AVM, other materials (sediments, algae, fish, invertebrates, and water from affected lakes), or tissues from AVM-affected birds did not produce either clinical signs or brain lesions in any of the other test animals in our studies. These results suggest that waterbirds are most likely exposed to the causative agent of AVM while feeding on aquatic vegetation, but we do not believe the vegetation itself is the agent. We hypothesize that the causative agent of AVM might either be accumulated by aquatic vegetation, such as Hydrilla, or associated with biotic or abiotic material on its external surfaces. In support of that hypothesis, two coots that ingested Hydrilla sampled from a lake with an ongoing AVM outbreak in wild birds developed neurologic signs within 9 days (ataxia, limb weakness, and incoordination), and one of two coots that ingested Hydrilla collected from the same site 13 days later became sick and died within 38 days. None of these three sick coots had definitive brain lesions consistent with AVM by light microscopy, but they had no gross or histologic lesions in other tissues. It is unclear if these birds died of AVM. Perhaps they did not ingest a dose sufficient to produce brain lesions or the lesions were ultrastructural. Alternatively, it is possible that a separate neurotoxic agent is responsible for the morbidity and mortality observed in these coots.     

Establishing a food-chain link between aquatic plant material and avian vacuolar myelinopathy in mallards (Anas platyrhynchos)

Avian vacuolar myelinopathy (AVM) is a neurologic disease primarily affecting bald eagles (Haliaeetus leucocephalus) and American coots (Fulica americana). The disease was first characterized in bald eagles in Arkansas in 1994 and then in American coots in 1996. To date, AVM has been confirmed in six additional avian species. Attempts to identify the etiology of AVM have been unsuccessful to date. The objective of this study was to evaluate dermal and oral routes of exposure of birds to hydrilla (Hydrilla verticillata) and associated materials to evaluate their ability to induce AVM. Mallards (Anas platyrhynchos) were used in all trials; bobwhite quail (Colinus virginianus) also were used in one fresh hydrilla material exposure trial. Five trials were conducted, including two fresh hydrilla material exposure trials, two cyanobacteria exposure trials, and a frozen hydrilla material exposure trial. The cyanobacteria exposure trials and frozen hydrilla material trial involved gavaging mallards with either Pseudanabaena catenata (live culture), Hapalosiphon fontinalis, or frozen hydrilla material with both cyanobacteria species present. With the exception of one fresh hydrilla exposure trial, results were negative or inconclusive. In the 2002 hydrilla material exposure trial, six of nine treated ducks had histologic lesions of AVM. This established the first cause-effect link between aquatic vegetation and AVM and provided evidence supporting an aquatic source for the causal agent.     

Investigation of the link between avian vacuolar myelinopathy and a novel species of cyanobacteria through laboratory feeding trials

Avian vacuolar myelinopathy (AVM) is a neurologic disease affecting Bald Eagles (Haliaeetus leucocephalus), American Coots (Fulica americana), and other birds in the southeastern United States. The cause of the disease has not yet been determined, although it is generally thought to be a natural toxin. Previous studies have linked AVM to aquatic vegetation, and the current working hypothesis is that a species of cyanobacteria growing epiphytically on that vegetation is producing a toxin that causes AVM. Surveys of epiphytic communities have identified a novel species of cyanobacteria in the order Stigonematales as the most likely suspect. The purpose of this study was to further examine the relationship between the suspect Stigonematales species and induction of AVM, by using animal feeding trials. Adult Mallards and domestic chickens were fed aquatic vegetation from two study sites containing the suspect cyanobacterial epiphyte, as well as a control site that did not contain the Stigonematales species. Two trials were conducted. The first trial used vegetation collected during mid-October 2003, and the second trial used vegetation collected during November and December 2003. Neither treatment nor control birds in the first trial developed AVM lesions. Ten of 12 treatment Mallards in the second trial were diagnosed with AVM, and control birds were not affected. This study provides further evidence that the novel Stigonematales species may be involved with AVM induction, or at the least it is a good predictor of AVM toxin presence in a system. The results also demonstrate the seasonal nature of AVM events.     

Avian vacuolar myelinopathy outbreaks at a southeastern reservoir

Avian vacuolar myelinopathy (AVM) is a neurologic disease of unknown etiology that affects bald eagles (Haliaeetus leucocephalus), American coots (Fulica americana), and several species of waterfowl. An unidentified neurotoxin is suspected as the cause of AVM, which has been documented at several reservoirs in the southeastern United States. We conducted diagnostic and epidemiologic studies annually during October-March from 1998-2004 at Clarks Hill/Strom Thurmond Lake on the Georgia/South Carolina border to better understand the disease. Avian vacuolar myelinopathy was confirmed or suspected as the cause of morbidity and mortality of 28 bald eagles, 16 Canada geese (Branta canadensis), six American coots, two great-horned owls (Bubo virginianus), and one killdeer (Charadrius vociferus). Active surveillance during the outbreaks yielded annual average prevalence of vacuolar lesions in 17-94% of coots, but not in 10 beavers (Castor canadensis), four raccoons (Procyon lotor), and one gray fox (Urocyon cinereoargenteus) collected for the study. Brain lesions were not apparent in 30 Canada geese collected and examined in June 2002. The outbreaks at this location from 1998-2004 represent the most significant AVM-related bald eagle mortality since the Arkansas epornitics of 1994-95 and 1996-97, as well as the first confirmation of the disease in members of Strigiformes and Charadriiformes.     

Epizootiologic studies of avian vacuolar myelinopathy in waterbirds

Epizootic avian vacuolar myelinopathy (AVM) was first recognized as a neurologic disease in bald eagles (Haliaeetus leucocephalus) and American coots (Fulica americana) in Arkansas, USA in 1994 and 1996, respectively, but attempts to identify the etiology of the disease have been unsuccessful to date. Between 1998 and 2001, wing clipped sentinel birds (wild American coots and game farm mallards [Anas platyrhynchos]) were released at Lake Surf, North Carolina, a lake with recurrent outbreaks of AVM, in order to gain a better understanding of the epizootiology of the disease. As early as 5-7 days post-release, sentinel coots and mallards showed neurologic signs of disease and were confirmed with AVM upon histologic examination of their brains. Serial releases of sentinel mallards during the summer, fall, and winter of 2000-01 demonstrated that exposure to the causative agent at a threshold sufficient to manifest disease was seasonal and occurred over about a 2 mo period, during November and December. Our findings that disease onset can be very rapid (5-7 days) and that exposure to the causative agent of AVM is site-specific, seasonal (late fall to early winter), and occurs over a relatively short duration (several months) supports the hypothesis that the disease is caused by a chemical substance, most likely of natural origin.     

Experimental Feeding of Hydrilla verticillata Colonized by Stigonematales Cyanobacteria Induces Vacuolar Myelinopathy in Painted Turtles (Chrysemys picta)

Vacuolar myelinopathy (VM) is a neurologic disease primarily found in birds that occurs when wildlife ingest submerged aquatic vegetation colonized by an uncharacterized toxin-producing cyanobacterium (hereafter “UCB” for “uncharacterized cyanobacterium”). Turtles are among the closest extant relatives of birds and many species directly and/or indirectly consume aquatic vegetation. However, it is unknown whether turtles can develop VM. We conducted a feeding trial to determine whether painted turtles (Chrysemys picta) would develop VM after feeding on Hydrilla (Hydrilla verticillata), colonized by the UCB (Hydrilla is the most common “host” of UCB). We hypothesized turtles fed Hydrilla colonized by the UCB would exhibit neurologic impairment and vacuolation of nervous tissues, whereas turtles fed Hydrilla free of the UCB would not. The ability of Hydrilla colonized by the UCB to cause VM (hereafter, “toxicity”) was verified by feeding it to domestic chickens (Gallus gallus domesticus) or necropsy of field collected American coots (Fulica americana) captured at the site of Hydrilla collections. We randomly assigned ten wild-caught turtles into toxic or non-toxic Hydrilla feeding groups and delivered the diets for up to 97 days. Between days 82 and 89, all turtles fed toxic Hydrilla displayed physical and/or neurologic impairment. Histologic examination of the brain and spinal cord revealed vacuolations in all treatment turtles. None of the control turtles exhibited neurologic impairment or had detectable brain or spinal cord vacuolations. This is the first evidence that freshwater turtles can become neurologically impaired and develop vacuolations after consuming toxic Hydrilla colonized with the UCB. The southeastern United States, where outbreaks of VM occur regularly and where vegetation colonized by the UCB is common, is also a global hotspot of freshwater turtle diversity. Our results suggest that further investigations into the effect of the putative UCB toxin on wild turtles in situ are warranted.     

Differences in food assimilation between two coot species assessed with stable isotopes and particle size in faeces: linking physiology and conservation

The red-knobbed coot Fulica cristata experienced a dramatic population decline in Spain, where the common coot F. atra does not face conservation problems. This is puzzling because both species have similar ecologies. It has been suggested that habitat alterations affected the quality of food plants, and this impacted differentially both coots. To verify this, we conducted experiments to determine the assimilation efficiency of both species in relation to food quality. Two types of diets differing in fibre content (commercial food and Potamogeton pectinatus) were offered to captive red-knobbed and common coots, during both spring and autumn. We examined variations in faecal particle size among coot species and diets, indicative of the facility with which food can be assimilated, and used the stable isotope technique to study differences between coot species in stable isotope fractionations from consumption to excretion. Faecal particle size was larger in red-knobbed than in common coots when fibre content was high, but was similar when it was low. Faecal particle sizes were larger in autumn, when fibre content was higher, than in spring. In general, delta(15)N in faeces of red-knobbed coots was greater than in faeces of common coots. These results suggest that the digestive efficiency of the red-knobbed coot was lower than that of the common coot, and that the differences increased when the fibre content in food plants increased. Managers should try to make available to coots wetland habitat with high quality food, which may be facilitated by prolonging the hydroperiods.     

Native flora and fauna response to removal of the weed Hydrilla verticillata (L.f.) Royle in Lake Tutira

Hydrilla has been in New Zealand since the 1960s and formed major infestations in four lakes in the Hawkes Bay region. Challenges to controlling hydrilla in New Zealand have included a lack of tools and the changing responsibilities of local management agencies. A grass carp field trial was initiated in 1988 in the smallest of the hydrilla infested lakes to assess the feasibility of eradicating hydrilla. After the main hydrilla beds were consumed, regrowth from tubers still occurred for a further 12 years. In 2008, grass carp were released into the remaining three hydrilla-infested lakes in a central government led response to eradicate hydrilla. This paper describes the changes in the flora and fauna in the largest of these lakes, Lake Tutira, following the introduction of grass carp and the removal of the hydrilla weed beds. Annual surveys of aquatic vegetation and macroinvertebrates in the lake from 2008 to 2012 have shown that, following the removal of the hydrilla weed beds by 2010, there was a shift in grass carp grazing to marginal emergent plants, and a general increase in the distribution of the native plant vegetation, although there was some evidence of a decline in charophyte abundance. Macroinvertebrate diversity was maintained although there were changes in the relative abundance of taxa linked to changes in the littoral vegetation.     

Caryospora uptoni and Frenkelia sp.-like coccidial infections in red-tailed hawks (Buteo borealis)

The feces from 16 red-tailed hawks (Buteo borealis) were examined by fecal flotation for the presence of coccidial oocysts or sporocysts. Oocysts of Caryospora uptoni were found in five (31%), sporocysts of a Frenkelia sp.-like coccidium were found in eight (50%), and mixed infections with both species of coccidia were found in three (19%) red-tailed hawks. Neither oocysts nor sporocysts were found in six (38%) red-tailed hawks. Sexual stages of C. uptoni were found in the duodenum and jejunum of a naturally infected red-tailed hawk. Sexual stages were located in enterocytes on the distal three-fourths of the villi. This study shows that over 60% of red-tailed hawks may be passing coccidial oocysts/sporocysts in their feces and provides morphological information for diagnosing C. uptoni infections in histological sections.     

The red-tailed hawk, Buteo jamaicensis, a native definitive host of Frenkelia microti (Apicomplexa) in North America.

Oral inoculation of prairie voles, Microtus ochrogaster, with coccidian sporocysts isolated from the feces of a red-tailed hawk, Buteo jamaicensis, in Kansas, USA, resulted in formation of Frenkelia microti (Apicomplexa: Sarcocystidae) tissue cysts in the brains of the voles. Five additional isolates of morphologically similar sporocysts collected from red-tailed hawks or other Buteo spp. in Kansas failed to result in detectable infections in rodents. These results are the first to verify that red-tailed hawks are natural definitive host in North America for F. microti.     

Fatal pox infection in a rough-legged hawk.

Natural pox infection occurred in a free-living rough-legged hawk (Buteo lagopus) in northeastern North Dakota. Gross, histological and electron microscopic findings were typical of pox infection, and characteristic lesions developed in red-tailed hawks (Buteo jamaicensis) but not in great horned owls (Bubo virginianus) following inoculation with case material. Death of the rough-legged hawk was attributed to starvation rsulting from inability to capture prey and to blood loss from foot lesions.     

安邦河自然保护区繁殖期骨顶鸡对游憩干扰的行为反应

随着湿地生态旅游的发展,水禽面临着越来越多的游憩干扰。骨顶鸡在我国北方大部分地区的湖泡沼泽繁殖,可作为湿地质量的指示物种,探讨该物种对游憩干扰的反应很有意义。在黑龙江省安邦河自然保护区的游憩区和对照区进行了繁殖期骨顶鸡日行为观察,比较分析结果显示:繁殖前期游憩区骨顶鸡的躲避行为显著高于对照区(F_(1,18)=62.364,P0.01);孵卵期骨顶鸡对游憩干扰的反应比繁殖前期更强烈,除了躲避行为显著增加(雄性F_(1,8)=40.653,P0.01;雌性F_(1,8)=32.028,P0.01),还主要表现在雌骨顶鸡孵卵时间减少(F_(1,8)=13.521,P0.01),持续孵卵时间缩短;雄骨顶鸡取食时间峰值增加,取食中断不连续;雌雄骨顶鸡繁殖期行为及对游憩干扰反应有所不同。建议通过改善游憩区的隐蔽条件,以提供躲避空间,提高生境质量,减少游憩干扰的影响。     

Serological and parasitological prevalence of Toxoplasma gondii in wild birds from Colorado

Ground-feeding birds are considered important in the epidemiology of Toxoplasma gondii because they serve as indicators of soil contamination by oocysts, and birds of prey are indicators of T. gondii prevalence in rodents and other small mammals. Cats excrete environmentally resistant oocysts after consuming tissues of T. gondii -infected birds. In the present study, sera and tissues from 382 wild birds from Colorado were tested for T. gondii infection. Antibodies to T. gondii were found in 38 birds with the use of the modified agglutination test (MAT, 1∶25 titer). Tissues (brains, hearts) of 84 birds were bioassayed in mice. Viable T. gondii was isolated from 1 of 1 barn owl (Tyto alba), 1 of 5 American kestrels (Falco sparverius), 1 of 7 ferruginous hawks (Buteo regalis), 1 of 4 rough-legged hawks (Buteo lagopus), 2 of 13 Swainson's hawks (Buteo swainsoni), and 1 of 25 red-tailed hawks (Buteo jamaicensis). This is the first time T. gondii has been isolated from the barn owl, ferruginous hawk, rough-legged hawk, and Swainson's hawk.     

Screening Evaluation of the Ecological Risks to Terrestrial Wildlife Associated with a Coal Ash Disposal Site

Between 1955 and 1989, coal ash was deposited within an impounded watershed on the U.S. Department of Energy's Oak Ridge Reservation in Tennessee, creating the 3.6?ha Filled Coal Ash Pond (FCAP). The site has subsequently become vegetated wildlife habitat. To evaluate risks that metals in ash may pose to wildlife; ash, surface water, small mammal, and vegetation samples were collected and metal residues were determined. Metal concentrations, As and Se in particular, were elevated in ash, surface water, plant foliage, and small mammals relative to reference materials. Estimates of metal exposures were calculated for short-tailed shrews, white-footed mice, white-tailed deer, red fox, and red-tailed hawks. While shrews and mice were assumed to reside exclusively at and receive 100% exposure from the site, exposure experienced by deer, fox, and hawks was assumed to be proportional to the size of the site relative to their home range. Because deer had been observed to consume ash, presumably for its high sodium content, exposure experienced by deer consuming ash to meet sodium requirements was also estimated. Exposure estimates were compared to body-size adjusted toxicity data for each metal. These comparisons suggest that metals at the site may be detrimental to reproduction and survivorship of mice, shrews, and deer consuming ash for sodium; fox and hawks do not appear to be at risk     

Phylogeography of the Galápagos hawk (Buteo galapagoensis): a recent arrival to the Galápagos Islands

Galápagos hawks (Buteo galapagoensis) are one of the most inbred bird species in the world, living in small, isolated island populations. We used mitochondrial sequence and nuclear minisatellite data to describe relationships among Galápagos hawk populations and their colonization history. We sampled 10 populations (encompassing the entire current species range of nine islands and one extirpated population), as well as the Galápagos hawk's closest mainland relative, the Swainson's hawk (B. swainsoni). There was little sequence divergence between Galápagos and Swainson's hawks (only 0.42% over almost 3kb of data), indicating that the hawks colonized Galápagos very recently, likely less than 300,000 years ago, making them the most recent arrivals of the studied taxa. There were only seven, closely related Galápagos hawk haplotypes, with most populations being monomorphic. The mitochondrial and minisatellite data together indicated a general pattern of rapid population expansion followed by genetic isolation of hawk breeding populations. The recent arrival, genetic isolation, and phenotypic differentiation among populations suggest that the Galápagos hawk, a rather new species itself, is in the earliest stages of further divergence.     

Genetic implications of bottleneck effects of differing severities on genetic diversity in naturally recovering populations: An example from Hawaiian coot and Hawaiian gallinule

The evolutionary trajectory of populations through time is influenced by the interplay of forces (biological, evolutionary, and anthropogenic) acting on the standing genetic variation. We used microsatellite and mitochondrial loci to examine the influence of population declines, of varying severity, on genetic diversity within two Hawaiian endemic waterbirds, the Hawaiian coot and Hawaiian gallinule, by comparing historical (samples collected in the late 1800s and early 1900s) and modern (collected in 2012–2013) populations. Population declines simultaneously experienced by Hawaiian coots and Hawaiian gallinules differentially shaped the evolutionary trajectory of these two populations. Within Hawaiian coot, large reductions (between −38.4% and −51.4%) in mitochondrial diversity were observed, although minimal differences were observed in the distribution of allelic and haplotypic frequencies between sampled time periods. Conversely, for Hawaiian gallinule, allelic frequencies were strongly differentiated between time periods, signatures of a genetic bottleneck were detected, and biases in means of the effective population size were observed at microsatellite loci. The strength of the decline appears to have had a greater influence on genetic diversity within Hawaiian gallinule than Hawaiian coot, coincident with the reduction in census size. These species exhibit similar life history characteristics and generation times; therefore, we hypothesize that differences in behavior and colonization history are likely playing a large role in how allelic and haplotypic frequencies are being shaped through time. Furthermore, differences in patterns of genetic diversity within Hawaiian coot and Hawaiian gallinule highlight the influence of demographic and evolutionary processes in shaping how species respond genetically to ecological stressors.     

Cyclopiazonic acid production by Aspergillus flavus and its effects on broiler chickens.

Cyclopiazonic acid (CPA) was purified from cultures of Aspergillus flavus, and ca. 14 g of the toxin was collected for use in feeding studies. Chicken rations were artificially contaminated with purified CPA at concentrations of 10, 50, and 100 ppm (microgram/g) and fed ad libitum to eight groups of chickens for 7 weeks. Chickens receiving feed with 100 ppm of CPA had high mortality, decreased weight gain, and poor feed conversion when compared with birds receiving other doses. Postmortem examination showed that chickens fed the two greatest doses of CPA had proventricular lesions characterized by mucosal erosion and hyperemia (100 ppm) and by thick mucosa and dilated proventricular lumens (50 ppm). Birds given 100 ppm of CPA in feed also had numerous yellow foci in their livers and spleens. Microscopic examination of tissues of birds that received 100 ppm of CPA revealed ulcerative proventriculitis, mucosal necrosis in the gizzard, and hepatic and splenic necrosis and inflammation. Birds given 50 ppm of CPA had hyperplasia of the proventricular mucosal epithelium. Birds given 10 ppm of CPA and control birds had no significant treatment-related lesions.