The lateral export of an algal bloom toxin into the terrestrial ecosystem via food web interactions
Emerging aquatic insects are a substantial food source for bats, reptiles, amphibians, spiders, and birds and can account for 50-90% of the monthly energy budget for some terrestrial riparian species. As this energy flux crosses habitat boundaries it is shadowed by the movement of pollutants such as heavy metals and polychlorinated biphenyls; this has been referred to as the dark side of subsides. This study expands this developing field to address toxins associated with harmful algal blooms (HABs).
The geographical extent of human-induced HABs has increased over the last several decades and has become a global concern. These blooms are directly related to human-caused nutrient enrichment of freshwaters and can be toxic. The green-blue algae species Microcystis aeruginosa produces microcystin, a toxin that has been linked with mass mortalities and illness in wild and farmed fishes, aquatic wildlife, and humans making it a serious threat to public, economic, and environmental health. Aquatic ecosystems are affected at every trophic level. However, the extent to which microcystin can move into terrestrial food webs through cross-habitat subsides has yet to be explored.
Here we show that microcystin is not constrained by the aquatic terrestrial ecotone. We detected the toxin in all three taxa of a cross-habitat food chain. Toxin levels were quantified in a primary algae consumer and emerging aquatic invertebrate (Hexagenia Mayfly), a terrestrial insect and obligate aquatic insect consumer (Tetragnathidae Spider), and a vertebrate consumer that consumes a combination of aquatic and terrestrial food (Prothonotary Warbler). The study was conducted during the 2014 prothonotary warbler breeding season at two locations on the lower tidal James River near Richmond, Virginia, USA.
Microcystin in the water column reached a peak of 0.146 μg/L at one site on July 15th. Mayfly microcystin levels peaked late July mirroring water column concentrations (mean= 0.182 μg/g DW, n=20). Tetragnathidae spider toxin concentration mirrored that of Mayflies - a known prey item (mean= 0.198 μg/g DW, n=13). The concentrations of microcystin in prothonotary warbler livers varied by site and by the individual’s age (mean= 0.078 μg/g DW, n=74) with nestlings showing the highest levels compared with fledglings and adults. Warbler body condition was not related to liver microcystin levels and for nestlings it was not related to the proportion of aquatic prey it was fed. This study shows that human-induced algal blooms have impacts outside of aquatic ecosystems.