Biotransport of Algal Toxins to Riparian Food Webs - Environmental

Aug 23, 2016 - (7) The occurrence of harmful algal blooms (HABs) has been increasing worldwide raising concerns for aquatic life and human health.(8-1...
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BIOTRANSPORT OF ALGAL TOXINS TO RIPARIAN FOOD WEBS Nicholas J Moy, Jenna Dodson, Spencer Tassone, Paul A Bukaveckas, and Lesley P Bulluck Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.6b02760 • Publication Date (Web): 23 Aug 2016 Downloaded from http://pubs.acs.org on August 27, 2016

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Environmental Science & Technology

BIOTRANSPORT OF ALGAL TOXINS TO RIPARIAN FOOD WEBS

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Nicholas J. Moy1 Jenna Dodson2 Spencer J. Tassone1 Paul A. Bukaveckas 1,2,* Lesley P. Bulluck 1.2 Department of Biology1, Center for Environmental Studies2 Virginia Commonwealth University Richmond, Virginia *Author for Correspondence: Virginia Commonwealth University, 1000 West Cary Street, Richmond, VA, 23284, 804-828-0168, [email protected].

Submitted for Review to Environmental Science and Technology revised August 2016

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ABSTRACT 4

The occurrence of harmful algal blooms has resulted in growing world-wide concern

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about threats to aquatic life and human health. Microcystin (MC), a cyanotoxin, is the most

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widely reported algal toxin in freshwaters. Prior studies have documented its presence in aquatic

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food webs including commercially important fish and shellfish. In this paper we present the first

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evidence that algal toxins propagate into riparian food webs. We show that MC is present in

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emerging aquatic insects (Hexagenia Mayfly) from the James River Estuary and their consumers

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(Tetragnathidae Spider, Prothonotary Warbler; Protonotaria citrea). MC levels in Prothonotary

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Warblers varied by age class, with nestlings having the highest levels. At the site where

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nestlings received a higher proportion of aquatic prey (i.e., mayflies) in their diet, we observed

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higher MC concentrations in liver tissue and fecal matter. Warbler body condition and growth

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rate were not related to liver MC levels suggesting that aquatic prey may provide dietary benefits

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which offset potential deleterious effects of the toxin. This study provides evidence that threats

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posed by algal toxins extend beyond the aquatic environments in which blooms occur.

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Environmental Science & Technology

INTRODUCTION Emerging aquatic insects are an important food source for bats, reptiles, amphibians,

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spiders, and, in riparian birds, can account for 50-90% of the monthly energy budget.1,2 As

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emerging aquatic insects cross habitat boundaries, this food subsidy can be shadowed by the

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movement of pollutants (e.g., mercury, PCBs).3,4 The export of aquatic contaminants to

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consumers outside of the aquatic realm has been referred to as the “dark side of subsidies”,

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whereby benefits of greater prey availability are offset by exposure to potentially toxic

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contaminants4. For example, higher mercury levels in insectivorous birds were linked to a diet

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consisting mainly of emerged aquatic insects.5,6 Prior studies on this topic have focused on

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persistent and bioaccumulative contaminants such as mercury and organic chemicals

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delivered to aquatic systems and exported to terrestrial food webs. In this study, we expand on

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the concept of the “dark side of subsidies” to assess the exposure of riparian consumers to algal-

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derived toxins produced in aquatic systems.

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Algal blooms are associated with a range of deleterious effects including the proliferation

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of harmful algae which produce toxic secondary metabolites.7 The occurrence of harmful algal

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blooms (HABs) has been increasing worldwide raising concerns for aquatic life and human

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health.8-10 Some cyanobacteria, including the genus Microcystis, produce microcystins (MC), a

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class of monocyclic heptapeptide hepatotoxins.11 These toxins inhibit the activity of protein

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phosphatases which are important in many cell cycles.7,12,13 MC accumulates in a variety of

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aquatic organisms including zooplankton, bivalves, insects, wild and farmed fishes, sea otters,

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turtles, and water birds.14-22 MC can be transported through food webs via consumption;

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however, there is no evidence of biomagnification.12 The extent to which MC can be transported

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out of the aquatic realm has only recently been documented and with limited scope. Takahashi et

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al.23 found low levels of MC in midge-flies and dragonflies as aquatic-stage juveniles, as well as

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in a riparian predator (Tetragnathidae spiders).

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In this study we describe the movement of algal toxins from an aquatic food web into a

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riparian food web by measuring MC concentrations in adult (emergent) aquatic insects

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(Hexagenia mayfly, Chironomidae nidges and Trichoptera caddisflies), an invertebrate riparian

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predator (Tetragnathidae spider), and a vertebrate riparian predator (Prothonotary Warbler;

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Protonotaria citrea). We also analyze variation in MC concentrations among nestling warblers

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in relation to diet (aquatic vs. terrestrial prey) to determine whether body condition and growth

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rates are affected by MC exposure.

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Methods

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Study Site

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The James River Estuary is a freshwater-dominated sub-estuary of Chesapeake Bay with

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low salinity zones (tidal fresh and oligohaline; salinity