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Concept: Daphnia

176

The nanoparticle industry is expected to become a trillion dollar business in the near future. Therefore, the unintentional introduction of nanoparticles into the environment is increasingly likely. However, currently applied risk-assessment practices require further adaptation to accommodate the intrinsic nature of engineered nanoparticles. Combining a chronic flow-through exposure system with subsequent acute toxicity tests for the standard test organism Daphnia magna, we found that juvenile offspring of adults that were previously exposed to titanium dioxide nanoparticles exhibit a significantly increased sensitivity to titanium dioxide nanoparticles compared with the offspring of unexposed adults, as displayed by lower 96 h-EC(50) values. This observation is particularly remarkable because adults exhibited no differences among treatments in terms of typically assessed endpoints, such as sensitivity, number of offspring, or energy reserves. Hence, the present study suggests that ecotoxicological research requires further development to include the assessment of the environmental risks of nanoparticles for the next and hence not directly exposed generation, which is currently not included in standard test protocols.

Concepts: Environment, Natural environment, Data, Assessment, Titanium dioxide, Star Trek: The Next Generation, Daphnia, Jonathan Frakes

166

BACKGROUND: The gene doublesex (dsx) is known as a key factor regulating genetic sex determination in many organisms. We previously identified two dsx genes (DapmaDsx1 and DapmaDsx2) from a freshwater branchiopod crustacean, Daphnia magna, which are expressed in males but not in females. D. magna produces males by parthenogenesis in response to environmental cues (environmental sex determination) and we showed that DapmaDsx1 expression during embryonic stages is responsible for the male trait development. The D. magna dsx genes are thought to have arisen by a cladoceran-specific duplication; therefore, to investigate evolutionary conservation of sex specific expression of dsx genes and to further assess their functions in the environmental sex determination, we searched for dsx homologs in four closely related cladoceran species. RESULTS: We identified homologs of both dsx genes from, D. pulex, D. galeata, and Ceriodaphnia dubia, yet only a single dsx gene was found from Moina macrocopa. The deduced amino acid sequences of all 9 dsx homologs contained the DM and oligomerization domains, which are characteristic for all arthropod DSX family members. Molecular phylogenetic analysis suggested that the dsx gene duplication likely occurred prior to the divergence of these cladoceran species, because that of the giant tiger prawn Penaeus monodon is rooted ancestrally to both DSX1 and DSX2 of cladocerans. Therefore, this result also suggested that M. macrocopa lost dsx2 gene secondarily. Furthermore, all dsx genes identified in this study showed male-biased expression levels, yet only half of the putative 5' upstream regulatory elements are preserved in D. magna and D. pulex. CONCLUSIONS: The all dsx genes of five cladoceran species examined had similar amino acid structure containing highly conserved DM and oligomerization domains, and exhibited sexually dimorphic expression patterns, suggesting that these genes may have similar functions for environmental sex determination in cladocerans.

Concepts: DNA, Evolution, Amino acid, Crustacean, Branchiopoda, Penaeus monodon, Cladocera, Daphnia

165

It is known that cyanobacteria negatively affect herbivores due to their production of toxins such as protease inhibitors. In the present study we investigated potential interspecific differences between two major herbivores, Daphnia magna and Daphnia pulex, in terms of their tolerance to cyanobacteria with protease inhibitors. Seven clones each of D. magna and of D. pulex were isolated from different habitats in Europe and North America. To test for interspecific differences in the daphnids' tolerance to cyanobacteria, their somatic and population growth rates were determined for each D. magna and D. pulex clone after exposure to varying concentrations of two Microcystis aeruginosa strains. The M. aeruginosa strains NIVA and PCC(-) contained either chymotrypsin or trypsin inhibitors, but no microcystins. Mean somatic and population growth rates on a diet with 20% NIVA were significantly more reduced in D. pulex than in D. magna. On a diet with 10% PCC(-), the population growth of D. pulex was significantly more reduced than that of D. magna. This indicates that D. magna is more tolerant to cyanobacteria with protease inhibitors than D. pulex. The reduction of growth rates was possibly caused by an interference of cyanobacterial inhibitors with proteases in the gut of Daphnia, as many other conceivable factors, which might have been able to explain the reduced growth, could be excluded as causal factors. Protease assays revealed that the sensitivities of chymotrypsins and trypsins to cyanobacterial protease inhibitors did not differ between D. magna and D. pulex. However, D. magna exhibited a 2.3-fold higher specific chymotrypsin activity than D. pulex, which explains the observed higher tolerance to cyanobacterial protease inhibitors of D. magna. The present study suggests that D. magna may control the development of cyanobacterial blooms more efficiently than D. pulex due to differences in their tolerance to cyanobacteria with protease inhibitors.

Concepts: Protease inhibitor, Enzyme, Serine protease, Trypsin, Branchiopoda, Proteolysis, Daphnia, Population growth

164

INTRODUCTION: One of the most interesting riddles within crustaceans is the origin of Cladocera (water fleas). Cladocerans are morphologically diverse and in terms of size and body segmentation differ considerably from other branchiopod taxa (Anostraca, Notostraca, Laevicaudata, Spinicaudata and Cyclestherida). In 1876, the famous zoologist Carl Claus proposed with regard to their origin that cladocerans might have evolved from a precociously maturing larva of a clam shrimp-like ancestor which was able to reproduce at this early stage of development. In order to shed light on this shift in organogenesis and to identify (potential) changes in the chronology of development (heterochrony), we investigated the external and internal development of the ctenopod Penilia avirostris and compared it to development in representatives of Anostraca, Notostraca, Laevicaudata, Spinicaudata and Cyclestherida. The development of the nervous system was investigated using immunohistochemical labeling and confocal microscopy. External morphological development was followed using a scanning electron microscope and confocal microscopy to detect the autofluorescence of the external cuticle. RESULTS: In Anostraca, Notostraca, Laevicaudata and Spinicaudata development is indirect and a free-swimming nauplius hatches from resting eggs. In contrast, development in Cyclestherida and Cladocera, in which non-swimming embryo-like larvae hatch from subitaneous eggs (without a resting phase) is defined herein as pseudo-direct and differs considerably from that of the other groups. Both external and internal development in Anostraca, Notostraca, Laevicaudata and Spinicaudata is directed from anterior to posterior, whereas in Cyclestherida and Cladocera differentiation is more synchronous. CONCLUSIONS: In this study, developmental sequences from representatives of all branchiopod taxa are compared and analyzed using a Parsimov event-pairing approach. The analysis reveals clear evolutionary transformations towards Cladocera and the node of Cladoceromorpha which correspond to distinct heterochronous signals and indicate that the evolution of Cladocera was a stepwise process. A switch from a strategy of indirect development to one of pseudo-direct development was followed by a shift in a number of morphological events to an earlier point in ontogenesis and simultaneously by a reduction in the number of pre-metamorphosis molts. A compression of the larval phase as well as a shortening of the juvenile phase finally leads to a precocious maturation and is considered as a gradual progenetic process.

Concepts: Developmental biology, Larva, Crustacean, Branchiopoda, Cladocera, Daphnia, Clam shrimp, Phyllopoda

160

Within arthropods, several crustacean groups are unique in their early development due to their stereotyped cell division patterns and cell lineages. However, it is still unclear whether these cell division patterns are homologous between the various crustacean groups and whether they could indicate the ground pattern of Tetraconata (Crustacea and Hexapoda). In this study we describe the early development of the raptorial water flea Bythotrephes longimanus as a representative of the Cladocera within branchiopods.

Concepts: Insect, Arthropod, Crustacean, Branchiopoda, Cladocera, Daphnia, Antenna, Phyllopoda

154

The cladoceran crustacean Daphnia pulex produces female offspring by parthenogenesis under favorable conditions, but in response to various unfavorable external stimuli, it produces male offspring (environmental sex determination: ESD). We recently established an innovative system for ESD studies using D. pulex WTN6 strain, in which the sex of the offspring can be controlled simply by changes in the photoperiod: the long-day and short-day conditions can induce female and male offspring, respectively. Taking advantage of this system, we demonstrated that de novo methyl farnesoate (MF) synthesis is necessary for male offspring production. These results indicate the key role of innate MF signaling as a conductor between external environmental stimuli and the endogenous male developmental pathway. Despite these findings, the molecular mechanisms underlying up- and downstream signaling of MF have not yet been well elucidated in D. pulex.

Concepts: Male, Reproduction, Sex, NMDA receptor, Sex-determination system, Branchiopoda, Daphnia, Temperature-dependent sex determination

154

The use of ecotoxicological techniques for the evaluation of the quality of limnetic waters allows the early detection of toxic agents that pose risks to human health. In this study Moina micrura (two clones), Daphnia laevis (two clones) and Daphnia similis, a temperate species, were used to evaluate the toxicity of six Microcystis extracts from two Colombian reservoirs. Toxin was detected and quantified by HPLC. Microcystin-LR was found in all extracts with the highest concentrations in one sample from each reservoir (434 μg g(-1) and 538 μg g(-1)). The extracts that had the highest toxin concentration also had the highest toxicities to cladocerans. Measurement of 48-h LC50 showed consistent differences between cladoceran species but not clones, Also, reproduction data in two species were consistent with the MC-LR content of one sample tested, with decreased reproduction and disruption of egg production. However, only some growth results of neonates exposed to extracts were consistent with the acute response. In conclusion, Daphnia species are a good model for monitoring cyanotoxins as they respond in a sensitive way to natural phytoplankton samples containing microcystin-LR.

Concepts: Human, Egg, Crustacean, Toxicology, Toxicity, Branchiopoda, Cladocera, Daphnia

150

Aquatic microcosm studies often increase either chamber height or base diameter (to increase water volume) to test spatial ecology theories such as “scale” effects on ecological processes, but it is unclear whether the increase of chamber height or base diameter have the same effect on the processes, i.e., whether the effect of the shape of three-dimensional spaces is significant. We orthogonally manipulated chamber height and base diameter and determined swimming activity, average swimming velocity and grazing rates of the cladocerans Daphnia magna and Moina micrura (on two algae Scenedesmus quadricauda and Chlorella vulgaris; leading to four aquatic algae-cladoceran systems in total) under different microcosm conditions. Across all the four aquatic systems, increasing chamber height at a given base diameter significantly decreased the duration and velocity of horizontal swimming, and it tended to increase the duration but decrease the velocity of vertical swimming. These collectively led to decreases in both average swimming velocity and grazing rate of the cladocerans in the tall chambers (at a given base diameter), in accordance with the positive relationship between average swimming velocity and grazing rate. In contrast, an increase of base diameter at a given chamber height showed contrasting effects on the above parameters. Consistently, at a given chamber volume increasing ratio of chamber height to base diameter decreased the average swimming velocity and grazing rate across all the aquatic systems. In general, increasing chamber depth and base diameter may exert contrasting effects on zooplankton behavior and thus phytoplankton-zooplankton interactions. We suggest that spatial shape plays an important role in determining ecological process and thus should be considered in a theoretical framework of spatial ecology and also the physical setting of aquatic microcosm experiments.

Concepts: Time, Water, Ecology, Length, Branchiopoda, Cladocera, Daphnia, Chlorella

148

Predation is one of the most important drivers of natural selection. In consequence a huge variety of anti-predator defenses have evolved in prey species. Under unpredictable and temporally variable predation pressure, the evolution of phenotypically plastic defensive traits is favored. These “inducible defenses”, range from changes in behavior, life history, physiology to morphology and can be found in almost all taxa from bacteria to vertebrates. An important group of model organisms in ecological, evolutionary and environmental research, water fleas of the genus Daphnia (Crustacea: Cladocera), are well known for their ability to respond to predators with an enormous variety of inducible morphological defenses. Here we report on the “twist”, a body torsion, as a so far unrecognized inducible morphological defense in Daphnia, expressed by Daphnia barbata exposed to the predatory tadpole shrimp Triops cancriformis. This defense is realized by a twisted carapace with the helmet and the tail spine deviating from the body axis into opposing directions, resulting in a complete abolishment of bilateral symmetry. The twisted morphotype should considerably interfere with the feeding apparatus of the predator, contributing to the effectiveness of the array of defensive traits in D. barbata. As such this study does not only describe a completely novel inducible defense in the genus Daphnia but also presents the first report of a free living Bilateria to flexibly respond to predation risk by abandoning bilateral symmetry.

Concepts: Evolution, Biology, Species, Predation, Ecology, Crustacean, Branchiopoda, Daphnia

147

Species of the genus Moina Baird (Cladocera: Moinidae) often dominate freshwater crustacean communities in temporary water bodies. Several species of Moina are used as food for fish larvae in aquaculture, as bioindicators in toxicological studies, and as common subjects for physiological studies. The aim of this paper is to estimate biodiversity of Moina in northern Eurasia using the standard DNA barcoding approach based on the cytochrome c oxidase subunit I (COI) gene. We analysed 160 newly obtained and 157 existing COI sequences, and found evidence for 21 phylogroups of Moina, some of which were detected here for the first time. Our study confirmed the opinion that the actual species diversity of cladocerans is several times higher than is presently accepted. Our results also indicated that Moina has the second richest species diversity among the cladoceran genera (with only Daphnia O. F. Mueller having a greater diversity of species). Our study strongly supports division of Moina into two faunistic groups: European-Western Siberian and Eastern Siberian-Far Eastern, with a transitional zone at the Yenisey River basin (Eastern Siberia). Here, we refrain from taxonomic descriptions of new species, as this requires a thorough morphological and taxonomic study for each putative taxon.

Concepts: Biodiversity, Species, Crustacean, Branchiopoda, Cladocera, Daphnia, Siberia, Krasnoyarsk