Susan B. Wilde

Harmful algal blooms in South Carolina residential and golf course ponds

The South Carolina coastal zone is among the fastest growing areas in the U.S., and population epicenters are marked by dense brackish water pond (lagoon) coverage associated with housing complexes and golf courses. Surveillance efforts in 2001–2002 documented the widespread occurrence of several types of potentially or measurably toxic harmful algal blooms (HABs) in these ponds. These man-made retention ponds were constructed in order to serve as a buffer between developed areas and open estuaries or for aesthetic reasons. However, the combination of restricted tidal flow and nutrient and/or contaminant deposition creates a stimulatory environment for potential HAB formation. These discoveries introduce the need to consider mitigation measures to existing ponds and HAB preventive strategies for future pond construction.

Climate and pH predict the potential range of the invasive apple snail (Pomacea insularum) in the southeastern United States.

Predicting the potential range of invasive species is essential for risk assessment, monitoring, and management, and it can also inform us about a species’ overall potential invasiveness. However, modeling the distribution of invasive species that have not reached their equilibrium distribution can be problematic for many predictive approaches. We apply the modeling approach of maximum entropy (MaxEnt) that is effective with incomplete, presence-only datasets to predict the distribution of the invasive island apple snail, Pomacea insularum. This freshwater snail is native to South America and has been spreading in the USA over the last decade from its initial introductions in Texas and Florida. It has now been documented throughout eight southeastern states. The snail’s extensive consumption of aquatic vegetation and ability to accumulate and transmit algal toxins through the food web heighten concerns about its spread. Our model shows that under current climate conditions the snail should remain mostly confined to the coastal plain of the southeastern USA where it is limited by minimum temperature in the coldest month and precipitation in the warmest quarter. Furthermore, low pH waters (pH <5.5) are detrimental to the snail’s survival and persistence. Of particular note are low-pH blackwater swamps, especially Okefenokee Swamp in southern Georgia (with a pH below 4 in many areas), which are predicted to preclude the snail’s establishment even though many of these areas are well matched climatically. Our results elucidate the factors that affect the regional distribution of P. insularum, while simultaneously presenting a spatial basis for the prediction of its future spread. Furthermore, the model for this species exemplifies that combining climatic and habitat variables is a powerful way to model distributions of invasive species.

Cyanobacteria and BMAA: Possible linkage with avian vacuolar myelinopathy (AVM) in the south-eastern United States

Abstract Avian vacuolar myelinopathy (AVM) is a neurological disease that produces uncoordinated behavior in affected birds in wetland ecosystems of the south-eastern United States. Feeding and sentinel trials, field surveys, and genetic studies have implicated the introduced flowering plant species Hydrilla verticillata (Hydrocharitaceae) and an associated epiphytic cyanobacterial species (Order Stigonematales) as a causal link to AVM. All five morphotypes of cyanobacteria have been shown to produce the neurotoxic amino acid BMAA, including cyanobacteria of the Stigonematales that are epiphytic on Hydrilla verticillata. If biomagnification of BMAA occurs in these wetland ecosystems, as has been observed in the Guam ecosystem, then the consumption of fish (e.g. shad and herring) and waterfowl (e.g. Canada geese and mallards) from AVM-confirmed reservoirs in Arkansas, Texas, Georgia, North Carolina and South Carolina could represent a significant human health risk.

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.

An extract of Hydrilla verticillata and associated epiphytes induces avian vacuolar myelinopathy in laboratory mallards.

Avian vacuolar myelinopathy (AVM) is a neurological disease affecting bald eagles (Haliaeetus leucocephalus), American coots (Fulica americana), waterfowl, and other birds in the southeastern United States. The cause of the disease is unknown, but is thought to be a naturally produced toxin. AVM is associated with aquatic macrophytes, most frequently hydrilla (Hydrilla verticillata), and researchers have linked the disease to an epiphytic cyanobacterial species associated with the macrophytes. The goal of this study was to develop an extraction protocol for separating the putative toxin from a hydrilla‐cyanobacterial matrix. Hydrilla samples were collected from an AVM‐affected reservoir (J. Strom Thurmond Lake, SC) and confirmed to contain the etiologic agent by mallard (Anas platyrhynchos) bioassay. These samples were then extracted using a solvent series of increasing polarity: hexanes, acetone, and methanol. Control hydrilla samples from a reference reservoir with no history of AVM (Lake Marion, SC) were extracted in parallel. Resulting extracts were administered to mallards by oral gavage. Our findings indicate that the methanol extracts of hydrilla collected from the AVM‐affected site induced the disease in laboratory mallards. This study provides the first data documenting for an “extractable” AVM‐inducing agent.

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.

Triploid Grass Carp Susceptibility and Potential for Disease Transfer when used to Control Aquatic Vegetation in Reservoirs with Avian Vacuolar Myelinopathy

Avian vacuolar myelinopathy (AVM) is an often-lethal neurologic disease that affects waterbirds and their avian predators (i.e., bald eagles Haliaeetus leucocephalus) in the southern United States. Feeding trials and field surveys provided evidence that AVM is caused by a toxin-producing, undescribed cyanobacterium (UCB), which grows as an epiphyte on the leaves of submerged aquatic vegetation (SAV). Reservoirs with documented AVM epornitics support dense growth of nonnative SAV. Waterbirds ingest the toxin when feeding on aquatic plants with the epiphytic UCB, and secondary intoxication occurs when raptors consume these birds. Vegetation management has been proposed as a means to reduce waterbird exposure to the putative toxin. We fed aquatic vegetation with and without the UCB to triploid Grass Carp Ctenopharyngodon idella in laboratory and field trials. Only Grass Carp that ingested aquatic vegetation with the UCB developed lesions in the central nervous system. The lesions (viewed using light microscopy) appeared similar to those in birds diagnosed with AVM. Grass Carp that received aquatic vegetation without the UCB were unaffected. Grass Carp tissues from each treatment were fed to domestic chickens Gallus domesticus (an appropriate laboratory model for AVM) in a laboratory trial; the chickens displayed no neurologic signs, and histology revealed a lack of the diagnostic lesions in brain tissues. Results from our trials suggest that (1) triploid Grass Carp are susceptible to the AVM toxin, although no fish mortalities were documented; and (2) the toxin was not accumulated in Grass Carp tissues, and the risk to piscivorous avifauna is likely low. However, a longer exposure time and analysis of sublethal effects may be prudent to further evaluate the efficacy and risk of using triploid Grass Carp to manage aquatic vegetation in a system with frequent AVM outbreaks.

Changes in submerged aquatic vegetation (SAV) coverage caused by extended drought and flood pulses

ABSTRACT Shivers SD, Golladay SW, Waters MN, Wilde SB, Ashford PD, Covich AP. 2018. Changes in submerged aquatic vegetation (SAV) coverage caused by extended drought and flood pulses. Lake Reserv Manage. 34:199—210. Previous studies demonstrated that submerged aquatic vegetation (SAV) affects productivity and biogeochemical cycling within freshwater ecosystems. Some invasive submerged macrophytes dominate shallow water bodies and are known to compete for nutrients with native macrophytes and phytoplankton. To evaluate variation in SAV coverage, annual whole-reservoir vegetation surveys were conducted during the peak of the growing season over a 3-yr period that included drought and years with seasonal flood pulses. Physical parameters were directly measured (Photosynthetically Active Radiation: PAR) or obtained from USGS river gauges (river discharge and turbidity) to investigate the relationship between hydrology and SAV coverage. Precipitation was lower in the first year of the study compared to the following 2 yr causing the lowest river discharge observed over the 3-yr study. First-year discharge was also lower than the 50-yr median daily Q (discharge). SAV coverage, particularly of dioecious Hydrilla verticillata, was the greatest during the reduced flow period (35.5 km2). With increasing precipitation and river discharge, SAV coverage was reduced during subsequent years (22.9 km2 and 18.3 km2, respectively). Increased discharge caused turbidity to increase, which reduced light availability during the early growing season, causing a delay in germination and subsequent reduction in SAV coverage. In shallow reservoirs, SAV is capable of extensive coverage. Thus, large variation in coverage can alter ecosystem functionality. In regulated river systems, managing late spring flood pulses may provide some control of SAV coverage in shallow reservoirs, in addition to providing other environmental flow benefits.

ALTERNATE FOOD-CHAIN TRANSFER OF THE TOXIN LINKED TO AVIAN VACUOLAR MYELINOPATHY AND IMPLICATIONS FOR THE ENDANGERED FLORIDA SNAIL KITE (ROSTRHAMUS SOCIABILIS)

Abstract Avian vacuolar myelinopathy (AVM) is a neurologic disease causing recurrent mortality of Bald Eagles (Haliaeetus leucocephalus) and American Coots (Fulica americana) at reservoirs and small impoundments in the southern US. Since 1994, AVM is considered the cause of death for over 170 Bald Eagles and thousands of American Coots and other species of wild birds. Previous studies link the disease to an uncharacterized toxin produced by a recently described cyanobacterium, Aetokthonos hydrillicola gen. et sp. nov. that grows epiphytically on submerged aquatic vegetation (SAV). The toxin accumulates, likely in the gastrointestinal tract of waterbirds that consume SAV, and birds of prey are exposed when feeding on the moribund waterbirds. Aetokthonos hydrillicola has been identified in all reservoirs where AVM deaths have occurred and was identified growing abundantly on an exotic SAV hydrilla (Hydrilla verticillata) in Lake Tohopekaliga (Toho) in central Florida. Toho supports a breeding population of a federally endangered raptor, the Florida Snail Kite (Rostrhamus sociabilis) and a dense infestation of an exotic herbivorous aquatic snail, the island applesnail (Pomacea maculata), a primary source of food for resident Snail Kites. We investigated the potential for transmission in a new food chain and, in laboratory feeding trials, confirmed that the AVM toxin was present in the hydrilla/A. hydrillicola matrix collected from Toho. Additionally, laboratory birds that were fed apple snails feeding on hydrilla/A. hydrillicola material from a confirmed AVM site displayed clinical signs (3/5), and all five developed brain lesions unique to AVM. This documentation of AVM toxin in central Florida and the demonstration of AVM toxin transfer through invertebrates indicate a significant risk to the already diminished population of endangered Snail Kites.