Subscriber access provided by Northern Illinois University
Article
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
Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a free service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are accessible to all readers and citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.
Environmental Science & Technology is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.
Page 1 of 24
Environmental Science & Technology
BIOTRANSPORT OF ALGAL TOXINS TO RIPARIAN FOOD WEBS
1 2
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
TOC Art 3
1 ACS Paragon Plus Environment
Environmental Science & Technology
ABSTRACT 4
The occurrence of harmful algal blooms has resulted in growing world-wide concern
5
about threats to aquatic life and human health. Microcystin (MC), a cyanotoxin, is the most
6
widely reported algal toxin in freshwaters. Prior studies have documented its presence in aquatic
7
food webs including commercially important fish and shellfish. In this paper we present the first
8
evidence that algal toxins propagate into riparian food webs. We show that MC is present in
9
emerging aquatic insects (Hexagenia Mayfly) from the James River Estuary and their consumers
10
(Tetragnathidae Spider, Prothonotary Warbler; Protonotaria citrea). MC levels in Prothonotary
11
Warblers varied by age class, with nestlings having the highest levels. At the site where
12
nestlings received a higher proportion of aquatic prey (i.e., mayflies) in their diet, we observed
13
higher MC concentrations in liver tissue and fecal matter. Warbler body condition and growth
14
rate were not related to liver MC levels suggesting that aquatic prey may provide dietary benefits
15
which offset potential deleterious effects of the toxin. This study provides evidence that threats
16
posed by algal toxins extend beyond the aquatic environments in which blooms occur.
2 ACS Paragon Plus Environment
Page 2 of 24
Page 3 of 24
17 18
Environmental Science & Technology
INTRODUCTION Emerging aquatic insects are an important food source for bats, reptiles, amphibians,
19
spiders, and, in riparian birds, can account for 50-90% of the monthly energy budget.1,2 As
20
emerging aquatic insects cross habitat boundaries, this food subsidy can be shadowed by the
21
movement of pollutants (e.g., mercury, PCBs).3,4 The export of aquatic contaminants to
22
consumers outside of the aquatic realm has been referred to as the “dark side of subsidies”,
23
whereby benefits of greater prey availability are offset by exposure to potentially toxic
24
contaminants4. For example, higher mercury levels in insectivorous birds were linked to a diet
25
consisting mainly of emerged aquatic insects.5,6 Prior studies on this topic have focused on
26
persistent and bioaccumulative contaminants such as mercury and organic chemicals
27
delivered to aquatic systems and exported to terrestrial food webs. In this study, we expand on
28
the concept of the “dark side of subsidies” to assess the exposure of riparian consumers to algal-
29
derived toxins produced in aquatic systems.
30
Algal blooms are associated with a range of deleterious effects including the proliferation
31
of harmful algae which produce toxic secondary metabolites.7 The occurrence of harmful algal
32
blooms (HABs) has been increasing worldwide raising concerns for aquatic life and human
33
health.8-10 Some cyanobacteria, including the genus Microcystis, produce microcystins (MC), a
34
class of monocyclic heptapeptide hepatotoxins.11 These toxins inhibit the activity of protein
35
phosphatases which are important in many cell cycles.7,12,13 MC accumulates in a variety of
36
aquatic organisms including zooplankton, bivalves, insects, wild and farmed fishes, sea otters,
37
turtles, and water birds.14-22 MC can be transported through food webs via consumption;
38
however, there is no evidence of biomagnification.12 The extent to which MC can be transported
39
out of the aquatic realm has only recently been documented and with limited scope. Takahashi et
3 ACS Paragon Plus Environment
Environmental Science & Technology
40
al.23 found low levels of MC in midge-flies and dragonflies as aquatic-stage juveniles, as well as
41
in a riparian predator (Tetragnathidae spiders).
42
In this study we describe the movement of algal toxins from an aquatic food web into a
43
riparian food web by measuring MC concentrations in adult (emergent) aquatic insects
44
(Hexagenia mayfly, Chironomidae nidges and Trichoptera caddisflies), an invertebrate riparian
45
predator (Tetragnathidae spider), and a vertebrate riparian predator (Prothonotary Warbler;
46
Protonotaria citrea). We also analyze variation in MC concentrations among nestling warblers
47
in relation to diet (aquatic vs. terrestrial prey) to determine whether body condition and growth
48
rates are affected by MC exposure.
49
Methods
50
Study Site
51
The James River Estuary is a freshwater-dominated sub-estuary of Chesapeake Bay with
52
low salinity zones (tidal fresh and oligohaline; salinity
