Species Of Freshwater Copepods Research Articles

Loss of a freshwater copepod species from El Junco Lake, Galápagos following the introduction and eradication of the Nile tilapia

Abstract An undescribed diaptomid copepod probably belonging to a new Mastigodiaptomus species has been discovered and was very abundant in El Junco Lake (San Cristóbal Island, Ecuador) from 1966 until 2004. The species was not found in samples from 2007, 2008 or 2018. The loss of this key species from the lake coincides with the illegal introduction of Nile tilapia to El Junco Lake in 2005 and its subsequent eradication in 2008. The disappearance of this biogeographically and ecologically important copepod population may be explained by direct mechanisms of predation and competition, by a combination of both processes, and by indirect mechanisms linked to alterations in the lake ecosystem. The effects of fish eradication using rotenone may have contributed to the loss of the diaptomid population and to preventing its recovery. This article discusses the search for sources of propagules for recolonization and possible reintroduction scenarios and procedures.

Zooplankton Fluctuations in the Surface Waters of the Estuary of a Large Subtropical Urban River

The Danshuei River has a third largest catchment area and third longest in Taiwan. It flows through the capital, Taipei, and more than six million people live within its catchment area. Its estuary is characterized by a highly variable chemical and physical environment that is affected by the interaction of inland freshwater runoff with wastewater, and toward the coast is also influenced by the China Coastal Current and the Kuroshio Current. By collecting zooplankton bimonthly in 2014 from the surface layer (0–2 m depth) at five sites in the estuary, we were able to demonstrate that the composition of the zooplankton, and particularly its copepod fraction, varied significantly among sampling stations and months, thereby revealing seasonal succession. Fourteen higher taxa or other categories of zooplankter were identified, with the following being most common taxa: Decapoda, Copepoda (including Calanoida, Cyclopoida, and Harpacticoida), and “other larvae.” The Copepoda comprised 44 taxa (including eight only identified to genus) belonging to 3 orders, 17 families, and 29 genera, the five most abundant of which wereBestiolinan. sp. (undescribed),Corycaeusspp.,Parvocalanus crassirostris,Acartiasp., andParacalanus parvus. The highest and lowest copepod abundances were recorded in July (2557.88 inds. m–3) and January (1.3 inds. m–3), respectively. Observed changes in abundance of many kinds of copepod appeared to be significantly related to changes in physico-chemical parameters (e.g., salinity, temperature, pH, and dissolved oxygen concentration). Cluster analysis confirmed the existence of distinct copepod communities, each characterized by a preference for a different set of environmental conditions. Our comprehensive literature review of the copepod biodiversity of Taiwan’s major rivers for comparison with similar data compiled for other estuaries in the world, the first time such a review has been compiled, shows that 32 copepod taxa have been recorded from the brackish and freshwater parts of the Danshuei River. They represent 58.2% of the total number of brackish- and freshwater copepod species in Taiwan, and five of them have so far only been recorded in the Danshuei River: the calanoidsAcartiella sinensisandPseudodiaptomus forbesi, the cyclopoidsOithona fragilisandOithona simplex, and the harpacticoidTachidius(Tachidius)discipes.

Differential intraspecific genetic variations of the closely related, wide-ranged freshwater copepods Cyclops vicinus Uljanin, 1875 and C. kikuchii Smirnov, 1932

Although Cyclops vicinus Uljanin, 1875 and C. kikuchii Smirnov, 1932 are broadly distributed in Eurasia, the genetic divergences between European and Asian populations have been investigated in neither species. In Japan, the nomenclature and distinction between these two congeners are still questionable (thus, hereafter C. vicinus s.l.). We determined the taxonomic position of the Japanese C. vicinus s.l. by morphological analyses and by sequencing nuclear internal transcribed spacer 1(ITS-1) and the mitochondrial 12S (mt12S) genes. The ITS-1 phylogeny separated Japanese C. vicinus s.l. into two genetic groups; one was clustered with European C. kikuchii (thus, CkikJPN), while the other was clustered with European C. vicinus (thus, CvicJPN). Morphological analyses using the lengths of terminal furcal setae revealed that CkikJPN and CvicJPN correspond to C. kikuchii and C. vicinus, respectively. These results revealed that C. vicinus and C. kikuchii in Japan are confidently the same species as those in Europe. The degree of divergence in the mt12S between Japanese and European populations varied largely between the species, as it was nearly at the interspecific level in C. kikuchii, while it was at the intraspecific level in C. vicinus; it is the first case in which the genetic divergence between the European and Asian population is greatly different among closely related species of freshwater copepods.

The role of freshwater copepods in the environmental risk assessment of caffeine and propranolol mixtures in the surface water bodies of Spain

In this study we aimed at assessing: (i) the environmental risk posed by mixtures of caffeine and propranolol to the freshwater ecosystems of Spain; (ii) the sensitivity of freshwater copepod species to the two compounds; (iii) if the toxicity of caffeine and propranolol to freshwater copepods contributes to the environmental risk posed by the two compounds in the freshwater bodies of Spain. The environmental risk was computed as the ratio of MECs (i.e. the measured environmental concentrations) to PNECs (i.e. the respective predicted no-effect concentrations). The effects of caffeine and propranolol on the freshwater cyclopoid Diacyclops crassicaudis crassicaudis were tested both individually and in binary mixtures. Propranolol posed an environmental risk in some but not in all the surface water ecosystems of Spain investigated in this study, while caffeine posed an environmental risk to all the investigated freshwater bodies, both as single compound and in the mixture with propranolol. Propranolol was the most toxic compound to D. crassicaudis crassicaudis, while caffeine was non-toxic to this species. The CA model predicted the toxicity of the propranolol and caffeine mixture for this species. D. crassicaudis crassicaudis was much less sensitive than several other aquatic species to both compounds. The sensitivity of D. crassicaudis crassicaudis does not increase the environmental risk posed by the two compounds in the freshwater bodies of Spain, however, further testing is recommended since the effect of toxicants on freshwater copepods can be more pronounced under multiple stressors and temperature increasing due to climate change.

The ecotoxicity of binary mixtures of Imazamox and ionized ammonia on freshwater copepods: Implications for environmental risk assessment in groundwater bodies

Groundwater bodies are impacted by substances such as pesticides and N-fertilizers, which usually occur in the environment as complex mixtures rather than isolated pollutants. The threat that these mixtures pose to groundwater-dwelling organisms is still poorly understood. The aims of the present study were to test the acute effect of a binary mixture of a herbicide (Imazamox) and NH4+ on epigean (Eucyclops serrulatus) and hypogean (Diacyclops belgicus) freshwater copepod species. In addition, to evaluate if the effect of the mixture can be explained by referencing non-interaction models or by more complex interaction models; and the implications for groundwater risk assessment. Compared with the action of the compounds evaluated separately, the effects of Imazamox and NH4+ in the binary mixture were more than additive or synergistic for both species. MixTox models evidenced a dose ratio and dose level deviations from concentration addition and independent action traditional models. The hypogean species was three times more sensitive to NH4+ that the epigean species when assayed as a single chemical. However, D. belgicus was only 1.13 times more sensitive than E. serrulatus when NH4+ was assayed in the mixture. The use of an integrated approach for substances that are known to interact in groundwater, should include copepods species as test organisms.

Features of the fine structure and Si content of the mandibular gnathobase of four freshwater species of Epischura (Copepoda: Calanoida)

The cutting edge of the mandibular gnathobase in many marine and some freshwater copepods is fortified with opal crowns for holding and grinding food. There is evidence of silica in these opal crowns for only seven species of freshwater copepods. Distinguishing characteristics of the structure and silicon (Si) content of the mandible’s cutting edge were analysed in four species of Calanoida of one genus from two lakes in Russia ( Epischura chankensis and E. baicalensis ) and two lakes in North America ( E. lacustris and E. nevadensis ). The morphology of the mandibular gnathobase is described in detail for each species. Differences in the mandible characteristics and the level of crown silicification are observed within the genus Epischura . The highest content of silica is recorded in the crowns of E. baicalensis , which feeds on diatoms with thick frustules in Lake Baikal.

Genetic Diversity and Population Structure of Two Freshwater Copepods (Copepoda: Diaptomidae), Neodiaptomus schmackeri (Poppe and Richard, 1892) and Mongolodiaptomus birulai (Rylov, 1922) from Taiwan

We used the mitochondria DNA COI (cytochrome c oxidase subunit I) sequence as a genetic marker to analyze the population genetic structure of two species of freshwater copepods, Neodiaptomus schmackeri (Poppe and Richard, 1892) and Mongolodiaptomus birulai (Rylov, 1922) from Taiwan. Four populations with 51 individuals of N. schmackeri and five populations with 65 individuals of M. birulai were included. We compared the nucleotide sequences of a 635-bp fragment of the COI gene of N. schmackeri and a 655-bp fragment of the COI gene of M. birulai, and eight and 14 unique haplotypes were recorded, respectively. Tseng-Wen reservoir and Wu-San-Tao reservoir are linked by a channel, and the gene flow between them was unrestricted (Fst = 0.058; Nm = 4.04; Fst, population differentiation parameter; Nm, the number of succesfull migrants per generation); the gene flow between all other populations of both species was restricted (Fst = 0.4–0.99; Nm = 0–0.37). Based on the COI gene diversification pattern, we suggest that most populations of N. schmackeri and M. birulai are isolated from each other. According to the neighbor-joining tree and the minimum spanning network (MSN), the species have similar metapopulation genetic structures. Genetic distance was not found to be correlated with geographical distance. The genetic diversification pattern was not shown to be comparable with geographical isolation owing to long-distance separation. The genetic structure of the present populations may result from serial extinction and redistribution of the populations formed in each reservoir relative to time. Human activity in the reservoirs with regards to water resource management and the fishery industry also exerts an effect on population redistribution.

Small effective population sizes in two planktonic freshwater copepod species (Eudiaptomus) with apparently large census sizes

In small planktonic organisms, large census sizes (N(c)) suggest large effective population sizes (N(e)), but reliable estimates are rare. Here, we present N(e)/N(c) ratios for two freshwater copepod species (Eudiaptomus sp.) using temporal samples of multilocus microsatellite genotypes and a pseudo-likelihood approach. N(e)/N(c) ratios were very small in both Eudiaptomus species (10(-7)-10(-8)). Although we hypothesized that the species producing resting eggs (E. graciloides) had a larger N(e) than the other (E. gracilis), estimates were not statistically different (E. graciloides: N(e) = 672.7, CI: 276-1949; E. gracilis: N(e) = 1027.4, CI: 449-2495), suggesting that the propagule bank of E. graciloides had no detectable influence on N(e).

Reply to the comment by Reid and Hudson on “Rate of species introductions in the Great Lakes via ships’ ballast water and sediments”

Drake and David M. Lodge 555 With Reid and Hudson (2008), we lament the weak representation of taxonomic expertise in modern biology. In fact, we have advocated increased funding for research in systematics and programs for training taxonomists (Lodge 2002). We are cognizant of our own lack of expertise in taxonomy and how the lack of taxonomic information and expertise hinders progress in research and management of biological invasions. Nevertheless, taxonomic expertise does not explain the differences between the conclusions of our papers (Drake and Lodge 2007a, 2007b) and the conclusions Reid and Hudson think we ought to have drawn. Rather, their disagreement is with our conceptual framework for thinking about invasive species and the uncertainties concerning species that might establish in regions outside their native ranges. Specifically, they assess invasion potential differently than we did. That is, to categorize species that have not invaded the Great Lakes, and for which a paucity of distributional and ecological information exists, we adopted different conceptual criteria than Reid and Hudson to designate these species as indigenous or nonindigenous. In addition, for species that have not invaded the Great Lakes, it is impossible to say if they might become established if they were to be introduced, leaving room for informed judgments and improvement of those judgments as new information becomes available. At issue are four species of freshwater copepods that we collected from the ballast water of ships entering the Great Lakes: Microcyclops rubellus, Microcyclops varicans, Paracyclops chiltoni, and Maraenobiotus insignipes. Reid and Hudson believe the first three should be considered indigenous to the Great Lakes because they occur elsewhere in North America and are reported from the Great Lakes in Hudson and Lesko (2003). Unfortunately, Hudson and Lesko (2003), an Internet source, was not available when the taxonomic component of this work was being performed, does not appear in a peer-reviewed journal, and does not refer to previously published reports of these species. Furthermore, Hudson and Lesko (2003) indicate that these species were not collected in the Great Lakes prior to 1984. Thus, we were and are justified in considering these species to be nonindigenous to the Great Lakes. Proper analysis and publication of previously collected specimens may yet reveal that these species were established prior to our collection of them from ballast water, in which case we would consider them as established, nonindigenous species. Concerning Maraenobiotus insignipes, Reid and Hudson concede that it has not been reported from the Great Lakes, but think we should have excluded it on the basis of its habitat, which Reid and Hudson report is primarily “streams, seeps, and damp moss”. Ideally, for all species we collected, we would have attempted to indicate their ability to establish in various Great Lakes habitats. Unfortunately, the Great Lakes ecosystem is so heterogeneous and the habitat tolerances of zooplankton are so poorly documented that we concluded that the only designation we could reliably apply to all the species we collected was whether or not they were known to tolerate fresh waters. Of course, the species we collected are just a sample of a much larger species pool, for which our primary goal was to estimate its size. An unknown fraction of this pool will not be able to inhabit the Great Lakes for various reasons. That this fraction is unknown is nonetheless a poor reason for rejecting our estimate of the total pool. Reid and Hudson also object to our categorization of Oithona similis as “freshwater” (Drake and Lodge 2007b). As can be understood from the context and the more complete listing in Annex 1 of Drake and Lodge (2007b), our designation indicates we were unable to rule out freshwater tolerance. This is different than asserting it to prefer fresh-

Photoprotective compounds in weakly and strongly pigmented copepods and co‐occurring cladocerans

Summary1. The prevalence of mycosporine‐like amino acids (MAAs) – a group of potential ultraviolet (UV)‐photoprotective compounds – was surveyed across 11 species of freshwater copepods from 20 lakes of varying ultraviolet radiation (UVR) transparency in North America, New Zealand and Argentina. Co‐occurring cladocerans were also analysed (seven species from 12 lakes). Many of the calanoid copepod populations were red with carotenoid pigmentation, allowing comparison of MAA and carotenoid accumulation as photoprotective strategies.2. In two Pennsylvania (U.S.A.) lakes, MAA and carotenoid contents were followed during the early spring to mid‐summer period of lake warming. A pronounced seasonal pattern of higher carotenoid/low MAA content in spring, shifting to low carotenoid/higher MAA content in summer, was observed in calanoids from the more UV transparent lake.3. All copepod samples contained MAAs. Visibly red calanoids, especially southern Hemisphere Boeckella, often had moderate to high concentrations (2.5–11 μg MAA mg−1 dw), but low concentrations (0.04–1 μg MAA mg−1 dw) in some N. American red calanoids show that high carotenoid pigmentation (e.g. 5–10 μg carotenoid mg−1 dw) does not necessarily imply high MAA content.4. No cladoceran sample had more than trace amounts of MAAs (<0.05 μg mg−1 dw). Therefore, MAA accumulation does not seem to be a photoprotective strategy utilized by Daphnia (five species from nine lakes) or other cladocerans.5. Seven identifiable MAAs were widely distributed among both calanoids and cyclopoids. Shinorine was ubiquitous and was usually the most abundant MAA in N. American samples. In contrast, porphyra‐334 was the predominant MAA in the southern Hemisphere Boeckella.6. Copepods from higher UVR lakes tended to have a higher MAA content, but this relationship was statistically weak overall and taxon‐specific when found.

A comparative population genetic study on calanoid freshwater copepods: Investigation of isolation-by-distance in two Eudiaptomus species with a different potential for dispersal

We examined patterns of genetic isolation-by-distance in two sister species of freshwater copepods, Eudiaptomus graciloides and Eudiaptomus gracilis, using the polymorphism of microsatellite markers. We assumed an enhanced dispersal potential of the species possessing diapausing eggs (E. graciloides) compared with E. gracilis with no diapause. On a longitudinal gradient spanning from northern Germany to Russia, we sampled 17 E. graciloides populations and 16 E. gracilis populations in order to investigate the scale dependence of isolation-by-distance from 0.4 to 1,340 km distance. In the 100–1,000 km range, no isolation could be detected in either Eudiaptomus species, suggesting either similar moderate gene flow over large geographic distances or persistence of historic patterns after postglacial recolonization. Our hypothesis was partly supported at the small-scale level (100 km range) where differences in population structure among species existed. We found isolation-by-distance in E. graciloides, the species with resting eggs, whereas E. gracilis exhibited a pattern of persistent founder effects. Further, in E. graciloides we found significant isolation-by-distance in the 1,340 km range with significantly reduced gene flow at distances >1,000 km. In E. gracilis, isolation-by-distance at distances >1,000 km could not be detected with our data because this species was not found in the Russian lakes. Our results suggest that short- and long-distance dispersal in Eudiaptomus are due to different processes, with diapausing eggs only being advantageous for shortdistance dispersal. We also argue that different spatial scales must be sampled to understand the geographic partitioning of genetic variance at marker loci.

Impact of copepod predation on the fecundity of Keratella cochlearis (Rotifera)

Copepod predation on rotifers affects the dynamics and structure of zooplankton communities. Many experimental studies have analysed the feeding behaviour of some calanoid and cyclopoid copepod species on different rotifer prey types. However, considerations of the impact of predation by these invertebrates on rotifer populations have generally neglected possible additional effects of this predation through differential predation mortality between eggs, egg-bearing females and females without eggs. The present study used direct observations to describe the predatory effect of two freshwater copepod species, Lovenula alluaudi (Calanoida) and Acanthocyclops vernalis (Cyclopoida), on egg-bearing females of the rotifer Keratella cochlearis. Both copepod species ingested Keratella eggs and egg-bearing females, i. e. the female plus its egg. However, in the case of the calanoid copepod, there was a significantly greater probability of suppression of Keratella eggs after capture, including direct predation and separation of the eggs from their mothers, than of Keratella females plus attached eggs. In contrast, the probability of suppression of Keratella eggs by the cyclopoid copepod did not significantly differ from that of whole Keratella females. These results are discussed in terms of the impact of this predation pattern on the fecundity of K. cochlearis populations in natural ecosystems. Rotifer reproduction may be regulated not only by food availability but also by copepod predation.

Phenotypic variation in metamorphosis in four species of freshwater copepods

SUMMARY1. Physiological metamorphosis accompanied by an ecological habitat shift is a widespread life‐history phenomenon, and both age and size at metamorphosis are highly variable in many organisms. In this study, age and size at metamorphosis (defined as the transition from the last naupliar to the first copepodite stage) were quantified for four species of freshwater copepods to determine the scale on which these two traits vary, if age and size at metamorphosis are equally variable, and if variation at metamorphosis is related to variation in newborn size.2. Measurements of laboratory‐reared and field‐caught individuals show that age and size at metamorphosis, together with newborn size, vary among siblings, between families within a population, between populations of one species and between closely related species.3. In all populations, age at metamorphosis was the most variable trait, a result observed in many other organisms. Most of the variation in age at metamorphosis could be explained by differences between families within a population, while differences among siblings from the same clutch accounted for most of the variation in size at metamorphosis.4. Although newborn size was variable, differences in this trait could not fully account for variation observed at metamorphosis. Newborn size differed among populations, but most interpopularional differences disappeared by the rime metamorphosis was reached. In particular, size at metamorphosis appears to be tightly constrained in freshwater copepods.5. Age and size at metamorphosis were not equally variable among species, either. Species‐specific metamorphic envelopes (joint distributions of age and size at metamorphosis) result from differences in trait means, variances and covariances, and suggest very different larval growth trajectories among three of the species examined.

Coexistence with similar life cycles in two species of freshwater copepods (Crustacea)

Two species of freshwater cyclopoid copepods, Cyclops scutifer Sars and Mesocyclops leuckarti (Claus), with different ecological requirements, coexist in three humic ponds near the timberline in boreal forests in south-central Norway. The life cycle in both species is basically regulated by complete depletion of oxygen during the long winter. There is a short period of reproduction in spring followed by a rapid development during summer and autumn to advanced instars, capable of diapause when oxygen depletion starts in early winter. Both species have an exclusive 1-yr cycle.

Effect of lipid reserves on individual carbon content of two planktonic freshwater copepod species

The effect of the variation of lipid droplet volume on individual carbon content was studied in two species of planktonic freshwater copepods, Eudiaptomus gracilis G.O. Sars and Thermocyclops oithonoides G.O. Sars. It was found, that when a multiple regression of carbon content on prosoma and lipid droplet volume instead of a simple regression of carbon content on prosoma volume was applied, the unexplainied variance of individual carbon content of Eudiaptomus gracilis could be reduced. However, the use of multiple regression on Thermocyclops oithonoides data did not lead to significantly higher coefficient of determination than was obtained by using a simple regression.

Photophobic responses of calanoid copepods: possible adaptive value

A genual pattern of photophobic responses has been observed which differs for calanoid copepods from freshwater, estuarine and oceanic environments. Using a video-computer system for motion analysis, the photophobic responses of light and dark adapted calanoid copepods were compared. Dark-adapted copepods were exposed to 600 ms flashes of dim blue light at 5 s intervals which simulated the flashes of biolumines-cent marine zooplankton. Light-adapted copepods were exposed to 600 ms intervals of darkness at 5 s intervals to simulate the shadows of organisms passing overhead. Four species of coastal marine copepods ( Acartia hudsonica, Centropages hamatus, Pseudocalanus minutus and Temora longicornis ) all showed photophobic responses to both flashes and shadows. These responses may have adaptive value to the copepods since they live in an environment with predators that are bioluminescent at night and cast shadows on their prey during the day (e.g. ctenophores and cnidarian medusae). Two species of oceanic copepods ( Euchaeta marina, Pleuromamma abdominalis ) showed strong photophobic responses to flashes but no response to shadows. This may correspond to the abundance of bioluminescent predators on copepods in the oceanic environment (fish, ctenophores, siphonophores, etc.) and their lack of exposure to the shadows of predators, since both these species are rarely found in the euphoric zone during the day. Two species of freshwater copepods ( Diaptomus sanguineus, Epishwa massachusettsensis ) showed no similar photophobic response to flashes of light. This lack of startle response may relate to the lack of bioluminescence in the freshwater environment. Freshwater copepods showed a weak photophobic response to shadows. The adaptive value of this behavior is unclear, however, since the responses seem to be too weak to function for escape, and the dominant predators large enough to cast shadows (fish) tend to approach their prey laterally.

TWO NEW SPECIES OF DIAPTOMUS FROM ARCTIC AND SUBARCTIC CANADA (CALANOIDA, COPEPODA)

Diagnoses of two new species of fresh-water copepods are presented, Diaptomus wilsonae from ponds of the Hudson Bay lowlands, and Diaptomus victoriaensis from tundra ponds on Victoria Island, N.W.T.