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

Abstract

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.

Hunting the eagle killer: A cyanobacterial neurotoxin causes vacuolar myelinopathy

“…hydrillicola feeding trials have confirmed neuropathy and mortality in a wide variety of taxa, including amphibians, reptiles, and fish, as well as secondary disease transfer through the food chain. Thus, the disease is now referred to as vacuolar myelinopathy (VM) (21)(22)(23)(24).…”

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

“…Recent feeding studies verified that both grass carp and herbivorous turtles were susceptible to AVM toxin present in a hydrilla/A. hydrillicola complex (Haynie et al 2013, Mercurio et al 2014. The spread of invasive aquatic vegetation and the toxicity of A. hydrillicola must be evaluated to determine food chain implications.…”

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

“…While feeding trials indicate that fish and reptiles fed hydrilla collected from AVM sites develop vacuolar lesions, it has not been demonstrated that they can transmit the AVM toxin to their predators (Haynie et al 2013;Mercurio et al 2014). In a field and laboratory study, triploid grass carp (Ctenopharyngodon idella), which are frequently used as a biological control agent for dense SAV, were fed hydrilla from an AVM site.…”