Predator-induced phenotypic plasticity in the exotic cladoceran Daphnia lumholtzi

1. The exotic cladoceran Daphnia lumholtzi has recently invaded freshwater systems throughout the United States. Daphnia lumholtzi possesses extravagant head spines that are longer than those found on any other North American Daphnia. These spines are effective at reducing predation from many of the predators that are native to newly invaded habitats; however, they are plastic both in nature and in laboratory cultures. The purpose of this experiment was to better understand what environmental cues induce and maintain these effective predator‐deterrent spines. We conducted life‐table experiments on individual D. lumholtzi grown in water conditioned with an invertebrate insect predator, Chaoborus punctipennis, and water conditioned with a vertebrate fish predator, Lepomis macrochirus. 2. Daphnia lumholtzi exhibited morphological plasticity in response to kairomones released by both predators. However, direct exposure to predator kairomones during postembryonic development did not induce long spines in D. lumholtzi. In contrast, neonates produced from individuals exposed to Lepomis kairomones had significantly longer head and tail spines than neonates produced from control and Chaoborus individuals. These results suggest that there may be a maternal, or pre‐embryonic, effect of kairomone exposure on spine development in D. lumholtzi. 3. Independent of these morphological shifts, D. lumholtzi also exhibited plasticity in life history characteristics in response to predator kairomones. For example, D. lumholtzi exhibited delayed reproduction in response to Chaoborus kairomones, and significantly more individuals produced resting eggs, or ephippia, in the presence of Lepomis kairomones.     

Linking biotic interactions and climate change to the success of exotic Daphnia lumholtzi

1. Warmer temperatures may increase cyanobacterial blooms in freshwater ecosystems, yet few ecological studies examine how increases in temperature and cyanobacterial blooms will alter the performance of non‐native species. We evaluated how competitive interactions and interactions between these two drivers of ecological change influence the performance of non‐native species using the native zooplankton Daphnia pulex and the non‐native zooplankton Daphnia lumholtzi as a model system. Based on the literature, we hypothesised that D. lumholtzi would perform best in warmer temperatures and in the presence of cyanobacteria. 2. Laboratory competition experiments showed that in the absence of competitors, growth rates of D. pulex (but not D. lumholtzi) were reduced at higher temperatures and with the cyanobacterial foods Anabaena flos‐aquae and Microcystis aeruginosa. In the presence of competitors, however, D. pulex emerged as the superior resource competitor at both temperatures with cyanobacterial food. We therefore predicted that, if competitive interactions are important to its establishment, D. lumholtzi would perform best in the absence of cyanobacteria in heated environments. 3. As predicted, when both species were introduced at low densities in field mesocosms, D. lumholtzi performed best at high temperatures without added cyanobacteria and worst at ambient temperatures with added cyanobacteria, indicating that competitive interactions are likely to be important for its establishment. 4. Taken together, these studies indicate that, while D. lumholtzi may benefit from increases in temperature, associated increased cyanobacterial blooms may hinder its performance. Thus, our findings underscore the importance of considering biotic interactions such as competition when predicting the future establishment of non‐native species in response to climate warming.     

Daphnia lumholtzi and Daphnia ambigua: population comparisons of an exotica and a native cladoceran in Lake Okeechobee, Florida

The population dynamics of an exotic cladoceran (Daphnialumholtzi Sars) and a native cladoceran (Daphniaambigua) were studied over a 12 month period in subtropical LakeOkeechobee, Florida (USA), to quantify the extent of invasion of the exoticspecies and compare ecological niches. Daphnialumholtzi accounted for up to 70% of theDaphnia assemblage during the summer months(June-August), while D.ambigua accounted for up to 97%of the Daphnia assemblage from fall to spring(October-April). The densities of the two species were inversely corelated.The exotic species was most concentrated in the shallower, warmer, northand south ends of the lake during the summer. It also was present, but atmuch lower densities, in the central lake region during the fall. Thenative species displayed a ubiquitous distribution throughout the lakeduring spring and winter, but was concentrated in the deeper, cooler,central region during the summer. Relationships of the two species withenvironmental conditions indicate that water column temperature mightaffect the seasonal and spatial distribution of the twoDaphnia species. The results also indicate thatD.lumholtzi may be filling a 'vacant' seasonal orspatial niche when conditions are unfavorable forD.ambigua.     

Factors which affect the abundance of an invasive cladoceran, Daphnia lumholtzi, in U.S. reservoirs

1.  Daphnia lumholtzi is a subtropical, Old World species which is rapidly spreading throughout reservoirs in the southern U.S.A. It was first recorded in Lake Texoma (Oklahoma–Texas) in September 1991.
2. Southern U.S. reservoirs typically have strong spatial and temporal gradients in temperature, conductivity, turbidity and in the distribution of organisms. Therefore, the present experiments examined the reproductive and moulting rates, and survival of D . lumholtzi in relation to extremes of food concentration, temperature, conductivity and turbidity.
3. Increases in temperature (range = 15–29 °C) and decreases in turbidity (range = 0.6–470 NTU) increased reproductive and moulting rates, whereas food concentration only affected the rate of reproduction, while conductivity had no effects. Survival was affected only by temperature.
4.  Daphnia lumholtzi tolerates high temperatures (27–30 °C) at which other cladocerans in Lake Texoma disappear. Therefore, D . lumholtzi may exploit resources in midsummer, when there are few potential competitors.     

Invasibility of a reservoir to exotic Daphnia lumholtzi: experimental assessment of diet selection and life history responses to cyanobacteria

SUMMARY 1. In reservoirs of the south-central United States, the exotic cladoceran Daphnia lumholtzi is common during warm midsummer conditions, when cyanobacteria are abundant and native Daphnia are rare. In the current study, we employed surveys, field experiments, and a life table experiment to investigate the role of food quality in explaining the distribution and phenology of D. lumholtzi , relative to two native species ( Daphnia parvula and Daphnia mendotae ).
2. During May–September 2000 in eutrophic McDaniel Lake, Missouri U.S.A., cyanobacteria (primarily Oscillatoria ) first appeared at 6-m depth and then became abundant throughout the epilimnion.
3. During the May field experiment, D. lumholtzi , D. parvula and D. mendotae all consumed a similar diet of algae, showing positive selection for small greens (chlorophytes and cryptophytes <20 μm). During the July experiment, when the epilimnion exceeded 25 °C and cyanobacteria were common in the lake, D. lumholtzi consumed significantly more total algae and more cyanobacteria than the two native species. Although the Daphnia selected against cyanobacteria, all three species consumed about 25% of this food in their diet.
4. A life table experiment compared the responses of D. lumholtzi and D. parvula with variation in density of high-quality food ( Ankistrodesmus ) and concentration of a toxic strain of cyanobacteria ( Anabaena flos-aquae ). Both Daphnia species showed reduced survivorship, fertility and intrinsic rates of increase in response to elevated concentrations of cyanobacteria, particularly at the higher food level.
5. The results suggest that D. lumholtzi shows similar inhibition from cyanobacteria as does the native Daphnia . However, their continued high in situ feeding rates imply that D. lumholtzi is less affected by midsummer conditions in warm-water reservoirs than are native Daphnia .     

Seasonal shifts in genotype frequencies in the invasive cladoceran Daphnia lumholtzi in Lake Texoma,U.S.A.

1. We examined the ecological genetics of the invasive cladoceran Daphnia lumholtzi in a reservoir (Lake Texoma) in the southern USA. This species originates from the Old World subtropics and has spread across North America since the late 1980s after its inadvertent introduction to a reservoir in northeastern Texas. 2. The population genetic structure of D. lumholtzi was examined seasonally on 22 dates over a 3‐year period along a natural temperature and salinity gradient. 3. A two‐allele polymorphism at the phosphoglucose isomerase (PGI) locus was detected, while other loci tested showed no variation. Significant temporal heterogeneity existed in genotype frequencies with a major shift between summer and autumn. 4. Results of a multiple linear regression analysis revealed that a significant amount of variation was explained by day length, temperature and conductivity. Additionally, significant spatial heterogeneity of genotype frequencies between lake stations was observed, but was restricted to the summer. 5. Clonal isolates were used in controlled laboratory temperature and salinity tolerance experiments. Results suggest that salinity and temperature tolerance differed between PGI genotypes. 6. Genotype × environment interactions may play a significant role in the micro‐evolutionary dynamics of this invasive species and may have facilitated its rapid expansion across the North American continent.     

Natural dispersal mechanisms and dispersal potential of the invasive ascidian Didemnum vexillum

Over the past decade, several species of non-indigenous ascidians have had adverse effects on a range of coastal ecosystems, and associated industries like aquaculture. One such species, the colonial ascidian Didemnum vexillum, poses a threat to the highly-valued New Zealand green-lipped mussel industry, and there is interest in whether and to what extent its spread can be managed at a regional scale (<100 km). An important component in the decision-making process for managing human-mediated pathways of spread is an understanding of D. vexillum’s natural dispersal potential. Here we use a weight-of-evidence approach, combining laboratory and field studies, to assess the role of natural dispersal mechanisms in the spread of D. vexillum. Under laboratory conditions, >70 % of D. vexillum larvae remained viable and were able to settle and undergo metamorphosis successfully following an artificial delay of 2 h. Larval viability decreased with increasing delay duration, although 10 % of larvae remained viable following a 36 h delay. A field-based study documented larval dispersal from two discrete source populations, with recruitment consistently detected on settlement plates at 250 m from source populations at one experimental site. Exponential decay models used to predict maximum larval dispersal distances at this site indicated that dispersal greater than 250 m is theoretically possible (>1 km in some situations). That being so, we recognise that the successful establishment and persistence of populations will depend on a wide range of processes not taken into account here. Our findings are supported by surveillance of D. vexillum spread in the wider study region; there are a number of instances where the species established on artificial structures that were several kilometres from known source populations, at a time when intensive regional-scale management of anthropogenic vectors was underway. Collectively, our findings indicate that D. vexillum has the ability to spread further by natural dispersal than previously assumed; probably hundreds of metres to kilometres depending on the local hydrological conditions, which has important implications for the ongoing management of this pest species world-wide.     

The outcome of the invasion of Florida lakes by Daphnia lumholtzi

1. We examined 7–12 years of monthly to quarterly historical data from 15 lakes in FL, U.S.A. to determine the extent and outcome of invasion by the alien cladoceran Daphnia lumholtzi Sars. 2. The alien species was found in 10 of the 15 lakes, including Florida’s three largest lakes: Okeechobee, George and Apopka. All the surveyed lakes had resident populations of the smaller native species Daphnia ambigua Scourfield. 3. In most of the lakes, D. ambigua occurred seven to ninefold more often in plankton samples than D. lumholtzi, and at 10‐ to 100‐fold higher maximal densities. One exception was a small lake in central Florida (Lake Jesup), where D. lumholtzi attained high densities on several occasions in the 10 years of sampling. 4. In Lake Okeechobee, where data were of sufficient quality and quantity to perform statistical analyses, the results of canonical correlation analysis indicated that high densities of D. lumholtzi were correlated with lower concentrations of suspended solids, high algal biomass and higher temperature, whereas the opposite conditions were correlated with high densities of D. ambigua. 5. Based on the majority of data, D. lumholtzi has successfully invaded many lakes in Florida, yet it has not become a substantive component of the zooplankton. Additional research is needed to determine whether resources, fish predation or some other factor is responsible for this outcome of invasion.     

The invasion history of the exotic freshwater zooplankter Daphnia lumholtzi (Cladocera, Crustacea) in North America: a genetic analysis

Daphnia lumholtzi is a planktonic crustacean native to subtropical regions in Africa, Asia and Australia. Since its invasion to the southern USA in ~1990 it has spread across North America as far north as the Laurentian Great Lakes. We assessed invasion history using microsatellite makers and to explore the influence of mean annual temperature on the genetic structure along a latitudinal gradient in North America. Genotypic data were obtained from 9 microsatellite markers for 178 individuals from 13 populations (eight populations introduced to North America and five populations in the native range). Pairwise F_st values as well as Bayesian clustering showed a strong subdivision between native and introduced populations. Bayesian clustering identified multiple genetic clusters in recently invaded locations, suggestive of multiple invasions from various sources, including Asia and Africa. Using variation partitioning, we determined the amount of variation for genetic clusters of populations in the invaded range due to mean annual air temperature and the year of first detection. The results point to a primary introduction into the southern range of North America, with a subsequent northward expansion, and multiple introductions possibly from both the native range and by secondary spread from previously-invaded locations. Separate analysis of genetic clusters within the invaded range suggests additional effects of temperature conditions on geographic genetic structure, possibly as a consequence of D. lumholtzi’s tropical origin.     

Influence of Temperature on Exotic Daphnia lumholtzi and Implications for Invasion Success

We investigated the effects of water temperature on the exoticcladoceran Daphnia lumholtzi in a eutrophic Kansas reservoir(USA) and under laboratory conditions. Daphnia lumholtzi demonstrateda distinct late summer appearance in the reservoir at temperaturesbetween 26 and 31°C, which corresponded with steep declinesin the densities of native Daphnia spp. Laboratory life-tableexperiments confirmed that D. lumholtzi performs well at elevatedwater temperatures. The intrinsic rate of increase (r), netreproductive rate (R_o), age at first reproduction, survivorship(l_x) and molting rates all demonstrate that D. lumholtzi hasa high temperature optimum between 20 and 30°C. A comparisonof literature-reported r-values indicates that the reproductiverate of D. lumholtzi is comparable with other Daphnia spp. between20 and 25°C, but also implies that D. lumholtzi may out-performsome Daphnia spp. at temperatures >25°C. Collectively,these results suggest that D. lumholtzi may be taking advantageof a late summer thermal niche, and that this invader may continueto colonize lakes and reservoirs in the southern US. However,life table data also indicate that D. lumholtzi performs poorlyat temperatures < 10°C, which may inhibit the range expansionof this invader into northern waters.     

The productivity and carbon budget of a natural population of Daphnia lumholtzi Sars

D. lumholtzi in Lake Samsonvale, Queensland, Australia, is a small species (max. size approx. 7 µgC) that occurs in low abundance (max. abundance 6400 m^–3), with an average daily biomass of 3.32 mgC m^–3. Its annual rates of carbon assimilation, production and respiration, are 166, 110, and 56 mgC m^–3 y^–1 respectively. Annual biomass turnover (annual production/average daily biomass) is 33 and production efficiency is 50–66%. The population may consume 1.65–2.20 mgC m^–3 daily, equivalent to about 1% of the average daily standing crop of phytoplankton. Clutch size is small, 2 eggs, but represents 30–80% of a female's weight. A female may only produce 8–10 offspring in a full lifespan, nevertheless egg production may account for 56% of total production. The population shows autumn and spring peaks in abundance, and is believed to oversummer (4 months) as ephippia.     

Periphyton as alternative food source for the filter-feeding cladoceran Daphnia magna

1.  Daphnia magna , a well-studied primary consumer, is mainly known as a filter feeder. In this study, we investigated the ability of D. magna to use periphyton as an alternative food source to phytoplankton. We examined the development of laboratory populations fed with different food sources ( Desmodesmus subspicatus and/or periphyton or neither) over a period of 42 days, and observed the behaviour of the daphnids.
2.  The addition of periphyton to phytoplankton food led to an increase of daphnid population biomass. When fed with periphyton as the only food source, a small but stable D. magna population developed.
3.  The behaviour of daphnids fed with both food sources revealed a preference for feeding on D. subspicatus . Only below a concentration of D. subspicatus of approximately 0.05 mg C L⁻¹ (0.4 × 10⁷ cells L⁻¹) did D. magna use periphyton as an alternative food source.
4.  Periphyton showed distinct reactions to grazing by D. magna . The thickness of the periphyton layer was reduced from about 4 to 1 mm and we observed a change in species composition due to grazing.
5.  The ability of D. magna to graze on periphyton could serve to stabilize its population density and reinforce its competitive advantage over other cladocerans. By switching between food sources, D. magna can act as a coupler between pelagic and benthic habitats and food webs.     

Development of an RNA interference method in the cladoceran crustacean Daphnia magna

Daphnids are small crustaceans ubiquitous in fresh water; they have been a subject of study in ecology, evolution, and environmental sciences for decades. To understand data accumulated in daphnid biology at the molecular level, expressed sequence tags and a genome sequence have been determined. However, these discoveries lead to the problem of how to understand the functions of newly discovered genes. Double-stranded RNA (dsRNA)-mediated RNA interference (RNAi) is a useful tool to achieve specific gene silencing in nontransformable species. Hence, we established a technique to inject exogenous materials into ovulated eggs and developed a dsRNA-based RNAi method for Daphnia magna. Eggs were collected just after ovulation and injected with dsRNA specific to the Distal-less (Dll) gene, which functions in appendage development in invertebrates and vertebrates. We found that the dsRNA successfully triggered the degradation of Dll mRNAs, which induced the truncation of the second antenna in a dose-dependent manner. This effect was sequence specific in that: (1) an unrelated dsRNA did not induce any morphological abnormalities and (2) two non-overlapping Dll dsRNAs generated the same phenotype. This is the first report of an RNAi technique in D. magna and, together with the emerging genome sequences, will be useful for advancing knowledge of the molecular biology of daphnids.     

Mechanisms of energy allocation to reproduction in the cladoceran Daphnia magna Straus

Understanding rules of resource allocation within individuals is helpful in explaining population dynamics. This is particularly the case under the conditions of resource limitation that are commonly experienced by zooplankton. Here, we evaluate assumptions underlying models of resource allocation in Daphnia and test the predictions of two models of response to starvation.
We also test the predictions of two simple models concerning the mechanisms of egg provisioning in Daphnia magna. Our results: (1) demonstrate that provisioning is discontinuous, occurring over a discrete period of the instar; (2) support the hypothesis that egg production occurs in a serial fashion; (3) show that Daphnia magna responds to starvation by ceasing egg production but that there is an increase in mean size of eggs provisioned during the instar, prior to starvation; and (4) broadly support predictions that the response of Daphnia to starvation is an instantaneous cessation of reproduction but that there is a time lag before death.     

Energy allocation in the cladoceran Daphnia magna Straus,under starvation and refeeding

Summary Models incorporating the energetics of individual daphnids (Cladocera) have been developed to predict the effect of environmental variables, particularly food availability, on population dynamics. One of them, that of Kooijman (1986), assumes that all assimilated energy enters a storage compartment prior to use in production and metabolism, and that under starvation the stores are used to support maintenance, reproduction and somatic growth, in that order of priority. This predicts that, under starvation, reproduction and growth will continue for a time, and that after they cease death will be immediate. Another model, that of McCauley et al. (1990), assumes that assimilated energy is used directly for maintenance and production, and that stores are accumulated to support maintenance metabolism under starvation. This predicts that growth and reproduction should cease immediately upon starvation and that death will not be immediate. We have carried out laboratory experiments, manipulating starvation time, on Daphnia magna to distinguish between these two models. The results support features of both models in that reproduction, but not growth, ceases upon starvation. We therefore developed a third model in which both maintenance and growth are supported from stores under starvation, with maintenance taking priority over growth under these conditions.     

Range expansion of an exotic ungulate (Ammotragus lervia) in southern Spain: ecological and conservation concerns

Evidence of aoudad Ammotragus lervia expansion in the southeastern quarter of the Iberian Peninsula is provided based on recent field surveys. Aoudad has become common in a limited region of the southeast of Spain since its introduction as a game species in Sierra Espuña Natural Park in 1970. Its adaptability enabled it to colonise nearby areas in a short period. Apart from this source of expansion, the increasing number of aoudads in Spanish private game reserves provided other centres of dispersion. In addition, aoudads were introduced on La Palma Island (Canary Islands), becoming a serious threat to endemic flora. Of great conservation concern is the species' potential as a competitor against native ungulates inhabiting the peninsula. Surveys conducted in southern Spain documented rapid colonization of new areas and established viable populations, consisting of adult males and females and the unequivocal presence of nursery groups, in the provinces of Alicante, Almería, Granada and Murcia. Also, aoudads have spread throughout the north and centre of La Palma. There are two main conservational concerns: the necessity of conducting detailed and reliable surveys in all potential regions where the species might expand, and the urgent need of changing current game policies in order to establish reliable controls on big game reserves to prevent animals from escaping.     

Differential wind dispersal of cladoceran ephippia in a rock pool metacommunity

Dispersal connects patches within metapopulations and is crucial to the persistence of many species, particularly those living in discontinuous habitat. Rock pools are excellent habitats in which to study dispersal in time as well as space, because many of the organisms that live within them make resistant long-lived dormant stages, they are often abundant, and they are easy to sample. The rock pools on Appledore Island, Gulf of Maine, USA, are home to several cladocerans, including Moina macrocopa and Daphnia pulex × pulicaria hybrids. Both taxa exist in extremely high abundances in some pools and make diapausing eggs enclosed in ephippia that are dispersed in time by hatching long after they are produced, and are also known to spatially disperse via pool overflows and by adhering to gulls. I hypothesized that ephippia of both taxa would also be spatially dispersed by wind. I found that while Moina are present in more pools, more abundant in those pools, and produce more ephippia, many more Daphnia ephippia dispersed into traps placed around the island. This may be explained, in part, by differences in the buoyancy of ephippia between the two species. A higher propensity to disperse may result in Daphnia relying more heavily on the spatial context of rock pools than Moina.     

Differing effects of suspended sediments on the performance of native and exotic Daphnia

1. Although large cladocerans are usually uncommon in large rivers, Daphnia lumholtzi (an exotic species in North America) is widespread and occasionally abundant. We collected zooplankton on the Illinois River (Illinois, U.S.A.) in 1995 and 1996 and found that the peak density of D. lumholtzi (25 L⁻¹) typically exceeded that of all native species combined. Maximum density occurred during warm periods (up to 27 °C) when concentrations of inorganic suspended sediments were high (>50 mg L⁻¹).
2. Using a life table experiment, we examined the effects of variation in suspended sediment (0 and 80 mg L⁻¹) and food (10⁴ and 10⁵ Ankistrodesmus cells mL⁻¹) on fitness of D. lumholtzi and the native Daphnia parvula. Daphnia lumholtzi had greater survivorship than D. parvula in most treatments and higher life-time fertility than D. parvula in all treatments. Both species achieved their fastest intrinsic rates of growth in treatments with high food, but their responses to suspended solids differed. The growth rate of D. lumholtzi in high food was slightly increased by higher turbidity, whereas that of D. parvula was depressed.
3. Results suggest that the ability of D. lumholtzi to tolerate suspended solids is an important factor contributing to its success in invading North American rivers.