What doesn’t kill you doesn’t make you stronger: Parasites modify interference competition between two invasive amphipods

We used a freshwater amphipod-microsporidian model (Ponto-Caspian hosts: Dikerogammarus villosus and D. haemobaphes, parasite: Cucumispora dikerogammari) to check whether parasites affect biological invasions by modulating behaviour and intra- and interspecific interactions between the invaders. We tested competition for shelter in conspecific and heterospecific male pairs (one or both individuals infected or non-infected). In general, amphipods of both species increased their shelter occupancy time when accompanied by infected rather than non-infected conspecifics and heterospecifics. Infected amphipods faced lower aggression from non-infected conspecifics. Moreover, D. villosus was more aggressive than D. haemobaphes and more aggressive towards conspecifics vs. heterospecifics. In summary, infection reduced the intra- and interspecific competitivity of amphipods, which became less capable of defending their shelters, despite their unchanged need for shelter occupancy. Dikerogammarus haemobaphes, commonly considered as a weaker competitor, displaced by D. villosus from co-occupied locations, was able to compete efficiently for the shelter with D. villosus when microsporidian infections appeared on the scene. This suggests that parasites may be important mediators of biological invasions, facilitating the existence of large intra- and interspecific assemblages of invasive alien amphipods.

SPREAD RATE OF ALIEN AMPHIPODS AND MYSIDS IN THE MAIN RIVERS OF BELARUS

The spread rates of alien species of Amphipoda and Mysida were calculated for the Dnieper, Pripyat and Neman rivers in the territory of Belarus. The maximal values of spread rate were obtained for Dikerogammarus villosus (in the Pripyat River - 37.8 km/year, in the Dnieper River - 17 km/year) and Dikerogammarus haemobaphes (in the Pripyat River - 53.6 km/year, in the Dnieper River - 17 km/year), while the minimal values of spread rate were calculated for mysids Paramysis lacustris (in the Dnieper River - 0.4 km/year) and Limnomysis benedeni (in the Dnieper River - 0.6 km/year), also for amphipods Chelicorophium robustum (in the Dnieper River - 0.5 km/year) and Echinogammarus trichiatus (in the Dnieper River - 1.3 km/year). The differences in the spread rates of species connected with the time of their first records at the monitoring points and the intensity of economic activities in the studied rivers.

A novel nudivirus infecting the invasive demon shrimp Dikerogammarus haemobaphes (Amphipoda)

The Nudiviridae are a family of large double-stranded DNA viruses that infects the cells of the gut in invertebrates, including insects and crustaceans. The phylogenetic range of the family has recently been enhanced via the description of viruses infecting penaeid shrimp, crangonid shrimp, homarid lobsters and portunid crabs. Here we extend this by presenting the genome of another nudivirus infecting the amphipod Dikerogammarus haemobaphes. The virus, which infects cells of the host hepatopancreas, has a circular genome of 119,754 bp in length, and encodes a predicted 106 open reading frames. This novel virus encodes all the conserved nudiviral genes (sharing 57 gene homologues with other crustacean-infecting nudiviruses) but appears to lack the p6.9 gene. Phylogenetic analysis revealed that this virus branches before the other crustacean-infecting nudiviruses and shares low levels of gene/protein similarity to the Gammanudivirus genus. Comparison of gene synteny from known crustacean-infecting nudiviruses reveals conservation between Homarus gammarus nudivirus and Penaeus monodon nudivirus; however, three genomic rearrangements in this novel amphipod virus appear to break the gene synteny between this and the ones infecting lobsters and penaeid shrimp. We explore the evolutionary history and systematics of this novel virus, suggesting that it be included in the novel Epsilonnudivirus genus (Nudiviridae).

Cryptic diversity and mtDNA phylogeography of the invasive demon shrimp, Dikerogammarus haemobaphes (Eichwald, 1841), in Europe

The regions of the Black, Caspian, and Azov seas are known for being both (i) the place of extensive crustacean radiation dated to the times of Paratethys and Sarmatian basins, and (ii) present donors of alien and invasive taxa to many areas worldwide. One amphipod morphospecies, Dikerogammarus haemobaphes, is known both as native to rivers draining to the Black and Caspian seas as well as a successful invader (nicknamed demon shrimp) in Central and Western European rivers. Based on mitochondrial (COI and 16S) and nuclear (28S) datasets and 41 sampling sites, representing both the native (19) and the invaded (22) range, we assessed cryptic diversity, phylogeography and population genetics of this taxon. First, we revealed the presence of two divergent lineages supported by all markers and all species delimitation methods. The divergence between the lineages was high (18.3% Kimura 2-parameter distance for COI) and old (ca. 5.1 Ma), suggesting the presence of two cryptic species within D. haemobaphes. Lineage A was found only in a few localities in the native range, while lineage B was widespread both in the native and in the invaded range. Although genetic divergence within lineage B was shallow, geographic distribution of 16S and COI haplotypes was highly heterogeneous, leading us to the definition of four Geo-Demographic Units (GDUs). Two GDUs were restricted to the native range: GDU-B1 was endemic for the Durugöl (aka Duruşu) Liman in Turkey, whereas GDU-B2 occurred only in the Dniester River. GDU-B3 was both present in several localities in the native range in the Black Sea drainage area and widespread in Central and Western Europe. The GDU-B4 was found exclusively in the Moskva River in Russia. Extended Bayesian Skyline Plot indicated steady growth of GDU-B3 population size since 30 ka, pointing to the rather old history of its expansion, first in the late Pleistocene in the native range and nowadays in Central and Western Europe. The analysis of haplotype distribution across the present distribution range clearly showed two invasion routes to Central and Western Europe. The first one, originating from the lower Dnieper, allowed the demon shrimp to colonize Polish rivers and the Mittellandkanal in Germany. The second one, originating from the Danube delta, allowed to colonize the water bodies in the upper Danube basin. The UK population has originated from the Central Corridor, as only a haplotype found exclusively along this route was recorded in the UK. Population genetics analysis showed that the invasion of the demon shrimp along the Central Corridor was not associated with the loss of genetic diversity, which might contribute to the success of this invader in the newly colonized areas.

Reaction of Gammaridae to oxygen contained in low water level in the North Caspian

The research of bottom invertebrates Gammaridae was carried out in 2013-2017 in the western part of the North Caspian. The purpose of the study was to determine the environmental tolerance of the organisms to oxygen. Oxygen deficit was caused by temperature and salinity stratification of water masses.Hypoxia was formed mainly in some areas of the shallow zone (up to 5 m) on the border of the Northern Caspian – Middle Caspian, as well as in areas with fine-grained sediments.Representatives of Gammaridae are characterized by high frequency of occur-rence.During the research period the number and biomass of the studied organisms widely varied. Gammarus Fabricius dominated by the total number, Dakerogammarus Stebbing – by the total biomass.The maximum frequency of occurrence was characteristic for Niphargoides similis (G. O. Sars).The limits of tolerance to oxygen of individual Gammaridae species living in the Northern Caspian sea have been presented.The minimum concentration of oxygen recorded for the entire period of research (1.29ml/l; 21%) is not critical for one species – Niphargoides similis (G. O. Sars). The low concentration (3 ml/l) does not inhibit the development of Niphargoides macrurus (Sars), Gammarus ischnus Stebbing, Gammarus pauxillus Grimm and Dikerogammarus haemobaphes (Eichwald). Other Gammaridae representatives living in the western part of the Northern Caspian were found in the environment with absolute oxygen concentration over 3.63 ml/l and with relative oxygen concentration over 59%.Wide ecological valency for oxygen is typical for Niphargoides similis (G. O. Sars), Gammarus pauxillus Grimm, Dikerogammarus haemobaphes (Eichwald), Gammarus ischnus Stebbing, and Niphargoides macrurus (Sars).

A New Family of DNA Viruses Causing Disease in Crustaceans from Diverse Aquatic Biomes

ABSTRACT Panulirus argus virus 1 (PaV1) is the only known virus infecting the Caribbean spiny lobster (Panulirus argus) from the Caribbean Sea. Recently, related viruses, Dikerogammarus haemobaphes virus 1 (DhV1) and Carcinus maenas virus 1 (CmV1), have been detected in the demon shrimp (Dikerogammarus haemobaphes) and the European shore crab (Carcinus maenas), respectively, from sites in the United Kingdom. The virion morphology of these crustacean viruses is similar to that of iridoviruses. However, unlike iridoviruses and other nucleocytoplasmic large DNA viruses (NCLDVs), these viruses complete their morphogenesis in the host cell nucleus rather than in the cytoplasm. To date, these crustacean viruses have remained unclassified due to a lack of genomic data. Using an Illumina MiSeq sequencer, we sequenced the complete genomes of PaV1, CmV1, and DhV1. Comparative genome analysis shows that these crustacean virus genomes encode the 10 hallmark proteins previously described for the NCLDVs of eukaryotes, strongly suggesting that they are members of this group. With a size range of 70 to 74 kb, these are the smallest NCLDV genomes identified to date. Extensive gene loss, divergence of gene sequences, and the accumulation of low-complexity sequences reflect the extreme degradation of the genomes of these “minimal” NCLDVs rather than any direct relationship with the NCLDV ancestor. Phylogenomic analysis supports the classification of these crustacean viruses as a distinct family, “Mininucleoviridae,” within the pitho-irido-Marseille branch of the NCLDVs. IMPORTANCE Recent genomic and metagenomic studies have led to a dramatic expansion of the known diversity of nucleocytoplasmic large DNA viruses (NCLDVs) of eukaryotes, which include giant viruses of protists and important pathogens of vertebrates, such as poxviruses. However, the characterization of viruses from nonmodel hosts still lags behind. We sequenced the complete genomes of three viruses infecting crustaceans, the Caribbean spiny lobster, demon shrimp, and European shore crab. These viruses have the smallest genomes among the known NCLDVs, with losses of many core genes, some of which are shared with iridoviruses. The deterioration of the transcription apparatus is compatible with microscopic and ultrastructural observations indicating that these viruses replicate in the nucleus of infected cells rather than in the cytoplasm. Phylogenomic analysis indicates that these viruses are sufficiently distinct from all other NCLDVs to justify the creation of a separate family, for which we propose the name “Mininucleoviridae” (i.e., small viruses reproducing in the cell nucleus).