Zebra or quagga mussel dominance depends on trade-offs between growth and defense-Field support from Onondaga Lake, NY.

Two invasive mussels (zebra mussel, Dreissena polymorpha and quagga mussel D. rostriformis bugensis) have restructured the benthic habitat of many water bodies in both Europe and North America. Quagga mussels dominate in most lakes where they co-occur even though zebra mussels typically invade lakes first. A reversal to zebra mussel over time has rarely been observed. Laboratory experiments have shown that quagga mussels grow faster than zebra mussels when predator kairomones are present and this faster growth is associated with lower investment in anti-predator response in quagga mussels than zebra mussels. This led to the hypothesis that the dominance of quagga mussels is due to faster growth that is not offset by higher vulnerability to predators when predation rates are low, as may be expected in newly colonized lakes. It follows that in lakes with high predation pressure, the anti-predatory investments of zebra mussels should be more advantageous and zebra mussels should be the more abundant of the two species. In Onondaga Lake, NY, a meso-eutrophic lake with annual mussel surveys from 2005 to 2018, quagga mussels increased from less than 6% of the combined mussel biomass in 2007 to 82% in 2009 (from 3 to 69% by number), rates typical of this displacement process elsewhere, but then declined again to 11-20% of the mussel biomass in 2016-2018. Average total mussel biomass also declined from 344-524 g shell-on dry weight (SODW)/m2 in 2009-2011 to 34-73 g SODW/m2 in 2016-2018, mainly due to fewer quagga mussels. This decline in total mussel biomass and a return to zebra mussel as the most abundant species occurred as the round goby (Neogobius melanostomus) increased in abundance. Both the increase to dominance of quagga mussels and the subsequent decline following the increase in this molluscivorous fish are consistent with the differences in the trade-off between investment in growth and investment in defenses of the two species. We predict that similar changes in dreissenid mussel populations will occur in other lakes following round goby invasions, at least on the habitats colonized by both species.

Environmental transcriptomes of invasive dreissena, a model species in ecotoxicology and invasion biology.

Dreissenids are established model species for ecological and ecotoxicological studies, since they are sessile and filter feeder organisms and reflect in situ freshwater quality. Despite this strong interest for hydrosystem biomonitoring, omics data are still scarce. In the present study, we achieved full de novo assembly transcriptomes of digestive glands to gain insight into Dreissena polymorpha and D. rostriformis bugensis molecular knowledge. Transcriptomes were obtained by Illumina RNA sequencing of seventy-nine organisms issued from fifteen populations inhabiting sites that exhibits multiple freshwater contamination levels and different hydrosystem topographies (open or closed systems). Based on a recent de novo assembly algorithm, we carried out a complete, quality-checked and annotated transcriptomes. The power of the present study lies in the completeness of transcriptomes gathering multipopulational organisms sequencing and its full availability through an open access interface that gives a friendly and ready-to-use access to data. The use of such data for proteogenomic and targeted biological pathway investigations purpose is promising as they are first full transcriptomes for this two Dreissena species.

Multilocus phylogeny of the zebra mussel family Dreissenidae (Mollusca: Bivalvia) reveals a fourth Neotropical genus sister to all other genera.

Dreissenidae is one of the most economically and ecologically important families of freshwater and estuarine mollusks. Fourteen extant species and three genera are currently recognized: Congeria contains three species from karst caves along the eastern Adriatic coast and one from the Orinoco River of Venezuela, Dreissena contains six species native to Eastern European rivers and estuaries, and Mytilopsis contains three species from the Gulf of Mexico, Caribbean, and northwestern coast of South America and one from the Tocantins River of Brazil. Previous molecular phylogenetic studies have examined all species except those from South American rivers, and found each genus to be monophyletic with Congeria and Mytilopsis forming a clade sister to Dreissena. We present the first multilocus phylogeny of Dreissenidae inclusive of South American riverine species. Bayesian and maximum likelihood analyses of a 3085 bp alignment consisting of mitochondrial (COI and 16S) and nuclear (18S and 28S) gene regions found Neotropical species to be consistently and strongly supported as sister to all other dreissenids, although incomplete sequencing of the single Orinoco specimen obscured Neotropical monophyly. Our intergeneric relationships are inconsistent with an extensive fossil record suggesting that dreissenids originated in Europe approximately 30 My before dispersing to the Western Hemisphere. Fossil-calibrated analyses indicated that Neotropical dreissenids diverged from European lineages in the mid to late Eocene (∼39.3 Ma), and Brazilian and Guiana shield populations diversified during the Oligocene to Miocene. We erect the new genus Rheodreissena for all Neotropical freshwater dreissenids and present haplotype data indicative of at least three species. Widespread anthropogenic alteration of the middle Xingu River and lower Amazon threatens the persistence of these endemic, poorly studied mussels and may facilitate introduction beyond their native range.

Will the Displacement of Zebra Mussels by Quagga Mussels Increase Water Clarity in Shallow Lakes during Summer? Results from a Mesocosm Experiment.

Zebra mussels (Dreissena polymorpha) are known to increase water clarity and affect ecosystem processes in invaded lakes. During the last decade, the conspecific quagga mussels (D. rostriformis bugensis) have displaced zebra mussels in many ecosystems including shallow lakes such as Oneida Lake, New York. In this study, an eight-week mesocosm experiment was conducted to test the hypothesis that the displacement of zebra mussels by quagga mussels leads to further decreases in phytoplankton and increases in water clarity resulting in increases in benthic algae. We found that the presence of zebra mussels alone (ZM), quagga mussels alone (QM), or an equal number of both species (ZQ) reduced total phosphorus (TP) and phytoplankton Chl a. Total suspended solids (TSS) was reduced in ZM and ZQ treatments. Light intensity at the sediment surface was higher in all three mussel treatments than in the no-mussel controls but there was no difference among the mussel treatments. There was no increase in benthic algae biomass in the mussel treatments compared with the no-mussel controls. Importantly, there was no significant difference in nutrient (TP, soluble reactive phosphorus and NO3-) levels, TSS, phytoplankton Chl a, benthic algal Chl a, or light intensity on the sediment surface between ZM, QM and ZQ treatments. These results confirm the strong effect of both mussel species on water clarity and indicate that the displacement of zebra mussel by an equivalent biomass of quagga mussel is not likely to lead to further increases in water clarity, at least for the limnological conditions, including summer temperature, tested in this experiment.

Abcb and Abcc transporter homologs are expressed and active in larvae and adults of zebra mussel and induced by chemical stress.

Multixenobiotic resistance (MXR) of aquatic invertebrates has so far been associated with cellular efflux activity mediated by P-glycoprotein (ABCB1) and MRP (multidrug resistance protein; ABCC) type ABC (ATP binding cassette) transporters. Expression and activity of an abcb1/Abcb1 homolog has been shown in eggs and larvae of the zebra mussel Dreissena polymorpha. Here we report identification of a partial cDNA sequence of an abcc/Abcc homolog from zebra mussel that is transcribed and active as a cellular efflux transporter in embryos and gill tissue of adult mussels. Transcript expression levels were comparatively low in eggs and sharply increased after fertilization, then maintaining high expression levels in 1 and 2 dpf (days post fertilization) larvae. MK571, a known inhibitor of mammalian ABCC transporters, blocks efflux of calcein-am in larvae and gill tissue as indicated by elevated calcein fluorescence; this indicates the presence of active Abcc protein in cells of the larvae and gills. Dacthal and mercury used as chemical stressors both induced expression of abcb1 and abcc mRNAs in larvae; accordingly, assays with calcein-am and ABCB1 inhibitor reversin 205 and ABCC inhibitor MK571 indicated enhanced Abcb1 and Abcc efflux activities. Responses to chemicals were different in gills, where abcb1 transcript abundances were enhanced in dacthal and mercury treatments, whereas abcc mRNA was only increased with mercury. Abcb1 and Abcc activities did not in all cases show increases that were according to respective mRNA levels; thus, Abcc activity was significantly higher with dacthal, whereas Abcb1 activity was unchanged with mercury. Our data indicate that abcb1/Abcb1 and abcc/Abcc transporters are expressed and active in larvae and adult stages of zebra mussel. Expression of both genes is induced as cellular stress response, but regulation appears to differ in larvae and tissue of adult stages.

Phylogeography and systematics of zebra mussels and related species.

The genus Dreissena includes two widespread and aggressive aquatic invaders, the zebra mussel, Dreissena polymorpha, and the quagga mussel, Dreissena bugensis. This genus evolved in the Ponto-Caspian Sea basin, characterized by dynamic instability over multiple timescales and a unique evolutionary environment that may predispose to invasiveness. The objectives of this study were to gain insights into the demographic history of Dreissena species in their endemic range, to reconstruct intraspecific phylogeographic relationships among populations, and to clarify systematics of the genus, using DNA sequences from the mitochondrial cytochrome oxidase I (COI) gene. We found four deeply diverged clades within this genus, with a basal split that approximately coincided with the Cretaceous-Tertiary boundary. Divergence events within the four base clades were much more recent, corresponding to geographically disjunct sets of populations, which might represent species complexes. Across all taxa, populations of Dreissena shared a common pattern of genetic signatures indicating historical population bottlenecks and expansions. Haplotype diversity was relatively low in Ponto-Caspian drainages relative to more stable tectonic lakes in Greece, Macedonia, and Turkey. The phylogeographic and demographic patterns in the endemic range of Dreissena might have resulted from vicariance events, habitat instability, and the high fecundity and passive dispersal of these organisms.