Trophic transfer of cyanobacterial toxins from zooplankton to planktivores: Consequences for pike larvae and mysid shrimps

Abstract

The aim of this study was to evaluate the potentially harmful effects of zooplankton preexposed to cyanobacteria on two planktivorous animals: a fish larva (pike, Esox lucius) and a mysid shrimp (Neomysis integer). The planktivores were fed zooplankton from a natural community that had been preexposed to cell-free extract or to purified toxin (nodularin) of the cyanobacterium Nodularia spumigena, and the growth, feeding, and pellet production of the planktivores, as well as the toxin content of the pellets, were measured. In addition, radiolabeled nodularin ((3)H-dihydronodularin) was used in separate experiments to measure the vector transfer of nodularin from zooplankton to their predators. During 11-day exposures, dissolved nodularin was transferred to pike larvae and N. integer via zooplankton at very low rates of accumulation. Treatment with N. spumigena extract decreased the ingestion and feces production rates of pike larvae. With purified nodularin alone, no such effect could be observed. No effect on molting cycle length, fecal pellet production, C:N ratio, or growth of N. integer was detected. The results suggest that dissolved cyanobacterial toxins released during bloom decay can have a negative impact on feeding and, hence, on the growth of fish larvae via zooplankton, even without direct contact between cyanobacteria and the fish.

Planktonic and benthic cyanobacteria of European brackish waters: a perspective on estuaries and brackish seas

“…In a work by Karjalainen et al (2005), blue mussels presented the highest amount of accumulated NOD, up to 13 800 mg kg À1 dry weight, while mysid shrimps accumulated more NOD than zebra mussels or the muddy sediment bivalve Macoma balthica. In fish, NOD accumulation can range from 0.1-2230 mg kg À1 dry weight, depending on the organs analysed and the technique used.…”

“…Juvenile flounders can show high concentrations of NOD even if they are not in direct contact with Nodularia (Karjalainen et al, 2007). Moreover, benthic filter-feeding organisms seem to be more efficient in uptake of NOD than the pelagic ones Karjalainen et al, 2005).…”

“…In contrast, primary producers such as Cladophora fracta and Fucus vesiculosus accumulate the lowest amounts of the toxin (Sipia¨et al, 2001(Sipia¨et al, , 2002(Sipia¨et al, , 2007Karjalainen et al, 2005;Strogyloudi et al, 2006;Mazur-Marzec et al, 2007;Pflugmacher et al, 2007). Despite the low NOD concentrations reported for the lower trophic levels, it has been suggested that zooplankton may act as a toxin vector, increasing its range (Karjalainen et al, 2005). Nevertheless, the high degree of depuration and/or detoxication processes across trophic levels observed in both field and experimental studies could explain the tolerance of some zooplankton species to Nodularia (Karjalainen et al, 2007).…”

“…NOD transfer among pelagic organisms is quite slow, although negative effects on the feeding and growth rates of fish larvae have been described (Karjalainen et al, 2005(Karjalainen et al, , 2007. This may be due to the high energy cost associated with NOD detoxification, leading to a decrease in the growth rate of fish larvae and increased vulnerability to predation (Karjalainen et al, 2007).…”

“…E-mail: vmvascon@ fc.up.pt Tan, 2007). The cyanobacteria of brackish waters (including estuaries), however, remain under-investigated, particularly in Europe, despite a number of significant contributions (Sivonen et al, 1989;Nehring, 1993;Lehtima¨ki et al, 1994Lehtima¨ki et al, , 1997Lehtima¨ki et al, , 2000Wille´n & Mattson, 1997;Sivonen & Jones, 1999;Sipia¨et al, 2001Sipia¨et al, , 2002Sipia¨et al, , 2006Sipia¨et al, , 2007Sipia¨et al, , 2008Vasconcelos & Cerqueira, 2001;Laamanen et al, 2002;Rocha et al, 2002;Geiss et al, 2003;Hobson & Fallowfield, 2003;Lehtonen et al, 2003;Stal et al, 2003;Sobrino et al, 2004;Herfindal et al, 2005;Kankaanpa¨a¨et al, 2005;Karjalainen et al, 2005Karjalainen et al, , 2007Karlsson et al, 2005;Pere´z & Carrilo, 2005;Surakka et al, 2005;Marino et al, 2006;Mazur-Marzec et al, 2007Paoli et al, 2007;Halinen et al, 2008;Ibelings & Havens, 2008;Jo´z´wiak et al, 2008;Lopes et al, 2010;Oftedal et al, 2010;). This lack of information for brackish-water cyanobacteria is especially significant in relation to the potential for production of new bioactive compounds.…”