Avian vacuolar myelinopathy linked to exotic aquatic plants and a novel cyanobacterial species

Abstract

Invasions of exotic species have created environmental havoc through competition and displacement of native plants and animals. The introduction of hydrilla (Hydrilla verticillata) into the United States in the 1960s has been detrimental to navigation, power generation, water intake, and water quality (McCann et al., 1996). Our field surveys and feeding studies have now implicated exotic hydrilla and associated epiphytic cyanobacterial species as a link to avian vacuolar myelinopathy (AVM), an emerging avian disease affecting herbivorous waterbirds and their avian predators. AVM, first reported in 1994, has caused the death of at least 100 bald eagles (Haliaeetus leucocephalus) and thousands of American coots (Fulica americana) at 11 sites from Texas to North Carolina (Thomas et al., 1998; Rocke et al., 2002). Our working hypothesis is that the agent of this disease is an uncharacterized neurotoxin produced by a novel cyanobacterial epiphyte of the order Stigonematales. This undescribed species covers up to 95% of the surface area of leaves in reservoirs where bird deaths have occurred from the disease. In addition, this species is rare or not found on hydrilla collected at sites where AVM disease has not been diagnosed. Laboratory feeding trials and a sentinel bird study using naturally occurring blooms of cyanobacteria on hydrilla leaves and farm-raised mallard ducks (Anas platyrhynchos) induced the disease experimentally. Since 1994 AVM has been diagnosed in additional sites from Texas to North Carolina. Specific site characteristics that produce the disjunct distribution of AVM are unknown, but it is probable that the incidence of this disease will increase with the introduction of hydrilla and associated cyanobacterial species into additional ponds, lakes, and reservoirs.

Aetokthonos hydrillicola gen. et sp. nov.: Epiphytic cyanobacteria on invasive aquatic plants implicated in Avian Vacuolar Myelinopathy

“…During an extensive survey of the planktonic, benthic and epiphytic cyanobacteria, a novel species of epiphytic cyanobacteria was noted on hydrilla (Hydrilla verticillata (Linnaeus 1782: 416) Royle (1839: 376)) from Lake J. Strom Thurmond (GA/SC). Subsequent investigations confirmed that the previously undescribed cyanobacterial species was growing on invasive aquatic vegetation in all locations where birds were dying from AVM (Wilde et al 2005). DeGray Lake was dominated by non-native Brazilian elodea (Egeria densa Planchon (1849: 80)) during 1994-1996, but hydrilla was also present and by 2000 was the dominant submerged aquatic plant in that system.…”

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

“…Species that specialize on dietary items that contain high levels of AVM toxin are most at risk (e.g., coots [hydrilla], and eagles [coots]; Birrenkott et al 2004;Lewis-Weis et al 2004). The density of A. hydrillicola colonies observed on Toho hydrilla is comparable to those in AVM reservoirs in South Carolina and Georgia (Wilde et al 2005). Exotic applesnails are distributed lake-wide in Toho, including areas where the highest densities of A. hydrillicola have been observed.…”

“…Although other species of native and invasive SAV can host A. hydrillicola, we used hydrilla because this is the dominant vegetation in all sites where AVM bird deaths have been documented since 2000 (Wilde et al 2005). Because we propose that the toxin is only associated with the combination of SAV and A. hydrillicola, material containing both is considered ''treatment hydrilla'' and hydrilla lacking the A. hydrillicola, where disease has never been documented, is considered ''control hydrilla.''…”

“…Comprehensive surveys revealed that all AVM sites are dominated by dense infestations of one of three types of invasive exotic submerged aquatic vegetation (SAV): hydrilla (Hydrilla verticillata), Brazilian elodea (Egeria densa), and Eurasian watermilfoil (Myriophyllum spicatum) (Wilde et al 2005). Additionally, SAV in each site serves as a substrate for the newly described genus and species Aetokthonos hydrillicola .…”

“…Aetokthonos hydrillicola dominates the epiphyte community on the leaves of SAV in AVM sites but is rare or not present in sites where AVM deaths have not occurred (Wilde et al 2005Williams et al 2007). Feeding studies have implicated food chain transfer (via ingestion of the gastrointestinal tract of diseased birds) of a toxin produced by a cyanobacterium associated with submerged aquatic vegetation growing in waterbodies where AVM-positive birds were previously diagnosed Birrenkott et al 2004;Lewis-Weis et al 2004;Rocke et al 2005;Wilde et al 2005Wilde et al , 2014. Thus, the working hypothesis of all ongoing AVM investigations is that waterbirds develop AVM by ingesting SAV and A. hydrillicola either directly or via predation on other birds that have recently fed on this material.…”