Long-Term Competitive Dynamics of Two Cryptic Rotifer Species: Diapause and Fluctuating Conditions

Life-history traits may have an important role in promoting species coexistence. However, the complexity of certain life cycles makes it difficult to draw conclusions about the conditions for coexistence or exclusion based on the study of short-term competitive dynamics. Brachionus plicatilis and B. manjavacasare two cryptic rotifer species co-occurring in many lakes on the Iberian Peninsula. They have a complex life cycle in which cyclical parthenogenesis occurs with diapausing stages being the result of sexual reproduction. B. plicatilis and B. manjavacasare identical in morphology and size, their biotic niches are broadly overlapping, and they have similar competitive abilities. However, the species differ in life-history traits involving sexual reproduction and diapause, and respond differently to salinity and temperature. As in the case of certain other species that are extremely similar in morphology, a fluctuating environment are considered to be important for their coexistence. We studied the long-term competitive dynamics of B. plicatilis and B. manjavacas under different salinity regimes (constant and fluctuating). Moreover, we focused on the dynamics of the diapausing egg bank to explore how the outcome of the entire life cycle of these rotifers can work to mediate stable coexistence. We demonstrated that these species do not coexist under constant-salinity environment, as the outcome of competition is affected by the level of salinity—at low salinity, B. plicatilis excluded B. manjavacas, and the opposite outcome occurred at high salinity. Competitive dynamics under fluctuating salinity showed that the dominance of one species over the other also tended to fluctuate. The duration of co-occurrence of these species was favoured by salinity fluctuation and perhaps by the existence of a diapausing egg bank. Stable coexistence was not found in our system, which suggests that other factors or other salinity fluctuation patterns might act as stabilizing processes in the wild.     

Niche diversity in crustacean cryptic species: complementarity in spatial distribution and predation risk

Recent genetic studies indicate that species with very close phenotypic similarity (“cryptic species”) are a common feature of nature, and that such cryptic species often coexist in communities. Because traditional views of species coexistence demand that species differ in phenotype to coexist stably, the existence of sympatric cryptic species appears to challenge traditional perspectives of coexistence. We evaluated niche diversity in three recently discovered species of Hyalella amphipods that occur sympatrically in lakes and share close phenotypic similarity. We found that, in some cases, these species exhibited strong complementary spatial distributions within the littoral zone of lakes, both across a distance-from-shore gradient, and a vertical depth gradient. Additionally, we compared fish stomach contents with habitat samples and found that species differed in their vulnerability to predation from sunfish (Lepomis spp.). Complementarity among species across axes of spatial distribution and predation risk, two important niche components, suggests that species with close phenotypic similarity may differ appreciably along ecologically relevant axes. Our results, considered in the light of previous studies, suggest a community structured by predator-mediated coexistence or sequential dominance across environmental gradients in the littoral zone.     

Barcoding rotifer biodiversity in Mediterranean ponds using diapausing egg banks

The biodiversity of Mediterranean freshwater bodies is among the most threatened worldwide; therefore, its accurate estimation is an urgent issue. However, traditional methods are likely to underestimate freshwater zooplankton biodiversity due to its high species seasonality and cryptic diversity. We test the value of applying DNA barcoding to diapausing egg banks, in combination with the creation of a reference collection of DNA barcodes using adult individual samples, to characterize rotifer communities. We use monogonont rotifers from two lakes in Doñana National Park and one from Ruidera Natural Park in Spain as models to create a reference collection of DNA barcodes for taxonomically diagnosed adult individuals sampled from the water column, to compare with the sequences obtained from individual eggs from the diapausing egg banks. We apply two different approaches to carry out DNA taxonomy analyses, the generalized mixed Yule coalescent method (GMYC) and the Automatic Barcode Gap Discovery (ABGD), to the obtained sequences and to publicly available rotifer sequences. We obtained a total of 210 new rotifer COI sequences from all three locations (151 diapausing eggs and 59 adults). Both GMYC and ABGD generated the same 35 operational taxonomic units (OTUs), revealing four potential cryptic species. Most sequences obtained from diapausing eggs (85%) clustered with sequences obtained from morphologically diagnosed adults. Our approach, based on a single sediment sample, retrieved estimates of rotifer biodiversity higher than or similar to those of previous studies based on a number of seasonal samples. This study shows that DNA barcoding of diapausing egg banks is an effective aid to characterize rotifer diversity in Mediterranean freshwater bodies.     

Maintenance of clonal diversity in Dipsa bifurcata (Fallén, 1810) (Diptera: Lonchopteridae). II. Diapause stabilizes clonal coexistence

We analyze a selection model analogous to a one-locus, two-allele haploid system that can explain recurrent seasonal changes in diversity for communities with diapausing species or populations with diapausing clones. The model demonstrates the potential influence of differential diapause on the stability of species and clonal coexistence and, by extension, on the maintenance of genetic polymorphism in general. Using estimates of clonal fitness values from populations of the parthenogenetic spear-winged fly Dipsa bifurcata (Fallén, 1810) (Diptera: Lonchopteridae), the model explains the long-term stable oscillation of clonal frequencies exhibited by these populations. In general, clones or species that share the same spatial habitat can persist in stable coexistence if there are differences not only in their temporarily fluctuating fitness values but also in their dormancy patterns.     

Persistent genetic signatures of colonization in Brachionus manjavacas rotifers in the Iberian Peninsula

Recent phylogeographical assessments have consistently shown that continental zooplankton display high levels of population subdivision, despite the high dispersal capacity of their diapausing propagules. As such, there is an apparent paradox between observed cosmopolitanism in the zooplankton that is associated with long-distance dispersal, and strong phylogeographical structures at a regional scale. Such population dynamics, far from migration-drift equilibrium, have been shown in the rotifer species complex Brachionus plicatilis, a group of over a dozen species inhabiting salt lakes and coastal lagoons worldwide. Here we present the mitochondrial DNA phylogeography of one of these species, Brachionus manjavacas, in the Iberian Peninsula, where it often co-occurs with the morphologically similar species B. plicatilis sensu stricto. We obtained sequences from 233 individuals from diapausing eggs and clonal cultures from 16 lakes in the Iberian Peninsula, and a Tunisian lake. Two strongly supported deep mitochondrial DNA clades were found (A and B). Phylogenetic and nested clade analysis showed that clade A has a strong phylogeographical structure, with a strong similarity of phylogeographical patterns between B. manjavacas clade A and B. plicatilis s.s. These include (i) signatures of allopatric fragmentation between central and southern populations, and (ii) range expansions in the Iberian Peninsula, both likely to have occurred during the Pleistocene. We find evidence for a glacial refugium in the Guadiana basin. Clades A and B co-occurred in several of these lakes because of range expansion and secondary contact between both clades. The co-occurrence between B. plicatilis s.s. and B. manjavacas is not recent, and both species might have experienced similar environmental challenges during the Pleistocene. The strong correlation of genetic and geographical distance found suggests that historical events can lead to such correlation, mirroring the effects of 'isolation by distance' in equilibrium populations.     

Species size affects hatching response to different temperature regimes in a rotifer cryptic species complex

The strategy of decreasing size with increasing temperature known as Bergmann’s rule operates at geographic scale and in spite of extensive studies still presents a puzzle to researches. The aim of this work was to verify whether patterns of diapausing egg hatching of closely related species are consistent with the expectations from Bergmann’s rule. In a laboratory study of the cryptic species complex of the rotifer Brachionus plicatilis, the response to temperature (17.5, 22.5, and 25.0 °C) of diapausing eggs collected in a pond where the three tested species coexist was assessed by (1) the number of hatchlings emerging or (2) the time needed to hatch. Our results show that the response to temperature from the sediment egg bank is species-dependent. In line with Bergmann’s rule, an association was observed between the hatching response to temperature and organism size. The biggest species increased its proportion in the hatchlings as temperature decreased, and vice versa. The intermediate size species showed an intermediate pattern. Nevertheless, temperature showed a general positive effect on hatching success. Time needed to hatch suggests a signature of Bergmann’s rule, but other factors seem to be affecting this parameter. This is the first study to demonstrate differences in the thermal dependence of diapausing egg hatching among closely related species with different body sizes, and it supports that Bergmann’s rule can be applied to diapause, an important phase in many invertebrate lifecycles.     

Speciation in ancient cryptic species complexes: evidence from the molecular phylogeny of Brachionus plicatilis (Rotifera)

Continental lake-dwelling zooplanktonic organisms have long been considered cosmopolitan species with little geographic variation in spite of the isolation of their habitats. Evidence of morphological cohesiveness and high dispersal capabilities support this interpretation. However, this view has been challenged recently as many such species have been shown either to comprise cryptic species complexes or to exhibit marked population genetic differentiation and strong phylogeographic structuring at a regional scale. Here we investigate the molecular phylogeny of the cosmopolitan passively dispersing rotifer Brachionus plicatilis (Rotifera: Monogononta) species complex using nucleotide sequence variation from both nuclear (ribosomal internal transcribed spacer 1, ITS1) and mitochondrial (cytochrome c oxidase subunit I, COI) genes. Analysis of rotifer resting eggs from 27 salt lakes in the Iberian Peninsula plus lakes from four continents revealed nine genetically divergent lineages. The high level of sequence divergence, absence of hybridization, and extensive sympatry observed support the specific status of these lineages. Sequence divergence estimates indicate that the B. plicatilis complex began diversifying many millions of years ago, yet has showed relatively high levels of morphological stasis. We discuss these results in relation to the ecology and genetics of aquatic invertebrates possessing dispersive resting propagules and address the apparent contradiction between zooplanktonic population structure and their morphological stasis.     

Untangling the mechanisms of cryptic species coexistence in a nematode community through individual-based modelling

Cryptic species are morphologically identical but genetically distinct, and are prominent across numerous phyla. The coexistence of such closely related species on local scales would seem to run counter to traditional coexistence and competition theory; it has been hypothesized as a consequence of differences in their resource use or tolerances to environmental conditions. We developed an individual-based model of a community of three cryptic Litoditis marina (nematode) species, to understand how individual-level interspecific and intraspecific interactions might explain the coexistence of these closely related species. The model incorporates individuals' reproduction, competition, dispersal and resource use. Data characterizing the cryptic species (growth rates, dispersal ability, competitive interactions and responses to changing environmental conditions) were obtained from laboratory experiments involving both mono- and multispecific nematode cultures, and are used to parameterize the model. Simulation studies are used to investigate which individual-level mechanisms of dispersal and interaction lead to the characteristic population-level patterns observed experimentally. Our results highlight the key role of intraspecific competition in mediating dispersal and therefore co-occurrence of the cryptic species. The differences in dispersal also influence the response of the cryptic species to competition, a combination of factors that provides an explanation for their co-occurrence. These results provide insights into how changes in individual-level processes can be amplified to affect population-level co-occurrence.     

Experimental evolution of bet hedging in rotifer diapause traits as a response to environmental unpredictability

The adaptive response of organisms to unpredictable environments is increasingly recognized as a central topic in fundamental and applied evolutionary ecology. Selection due to environmental unpredictability can act on multiple traits of an organism's life cycle to reduce the impact of high environmental variance. The aim of this research was to study how unpredictability selects for diapause traits: 1) the timing of sex (a proxy of the timing of diapausing egg production), and 2) the diapausing egg hatching fraction (a proxy of diapause duration). We used an experimental evolution approach with the facultative sexual rotifer Brachionus plicatilis. Laboratory populations experiencing two contrasting regimes of environmental fluctuation (predictable versus unpredictable) evolved divergently over a short time span (< 77 days). The populations under the unpredictable regime showed an earlier initiation of sexual reproduction and a lower hatching fraction of diapausing eggs than populations under the predictable regime. These findings demonstrate empirically the existence of bet‐hedging strategies in B. plicatilis regarding both traits, consistent with theoretical predictions of bet‐hedging evolution under conditions of unpredictable environmental variance. Given that scenarios of increased environmental variability are expected to occur in the near future, a comprehensive understanding of the role of bet‐hedging strategies is necessary for predicting population responses to environmental change.     

Cryptic diversity with wide salinity tolerance in the putative euryhaline Testudinella clypeata (Rotifera,Monogononta)

Aquatic faunas in fresh, brackish, and salt waters are usually well defined and differ amongst these three habitats. Nonetheless, some animals are known to be euryhaline, namely present across wide salinity ranges. The wide tolerance of putative euryhaline species has, however been refuted in some cases by DNA taxonomy, which has uncovered cryptic diversity with narrow ecological niches. We aim to improve knowledge on the putative euryhalinism of microinvertebrates and test whether it might actually be a real phenomenon or if euryhaline species are mostly a consequence of our previous inability to identify cryptic species with narrow salinity ranges, as discovered in Brachionus plicatilis. Using morphological analyses and DNA taxonomy, we investigated the species reality and distribution of a putative euryhaline rotifer species, Testudinella clypeata, and evaluated whether cryptic species are ecologically and/or geographically segregated. Different DNA taxonomy approaches concurred in revealing the presence of seven cryptic species within the T. clypeata morphospecies, which, in contrast to what has been previously detected, are actually euryhaline. Moreover, differences in analysed morphological traits were not significantly different amongst cryptic species. This suggests that DNA taxonomy improves our estimates of the actual diversity of microscopic species, in contrast to the morphological approach. © 2013 The Linnean Society of London     

Leading indicators of phytoplankton transitions caused by resource competition

Many important transitions in phytoplankton composition of lakes and oceans are related to shifts in nutrient supply ratios. Some phytoplankton transitions, such as cyanobacteria blooms in freshwater supplies and red tides in coastal oceans, are important for aquatic resource management. Therefore, it would be useful to have leading indicators which precede phytoplankton shifts and could be readily monitored in the field. We investigated potential indicators using a well-understood model of phytoplankton dynamics parameterized to mimic the transition toward cyanobacteria blooms in freshwater lakes. In stationary distributions, performance of the indicators depends on whether the species are capable of stable coexistence over a certain range of nutrient inputs. In transient simulations, however, indicators show consistent responses regardless of the possibility of stable coexistence. Leading indicators occurring 10 to 40 days prior to species shift include shift of lag-1 autoregression coefficient toward 0, low standard deviation, fluctuating skewness, and high kurtosis. These responses are different from those reported for critical transitions such as fold bifurcations. Thus, the indicators reveal clues to the mechanisms of important ecosystem transitions. In practice, indicators should be measured for multiple ecosystem variables, and interpretation of the indicators should be guided by experiments and mechanistic site-specific models to help resolve potential ambiguities.     

Coexistence of cryptic rotifer species: ecological and genetic characterisation of Brachionus plicatilis

1. The coexistence of five cryptic species of the rotifer species complex Brachionus plicatilis was investigated in four coastal Mediterranean ponds. Monthly sampling was undertaken for 15 months and species were characterised using allozyme electrophoresis. 2. We describe species‐diagnostic allozyme loci that can be used for rapid identification of these species. 3. The five species overlapped to some extent in their temporal use of the ponds, although some seasonal segregation was observed. 4. The match between temporal and spatial distribution and limnological conditions suggested ecological specialisation in some cases, although we found striking examples of extensive seasonal overlap. 5. Our results indicate that sympatry of cryptic rotifer species is largely because of seasonal ecological specialisation, which allows seasonal succession and partitioning of resources. The processes that might be involved in the long periods of overlapping seasonal distributions of species which are potentially competitors are discussed. This example illustrates that the ‘paradox of the plankton’ is more the rule than the exception.     

Experimental evidence that evolutionary relatedness does not affect the ecological mechanisms of coexistence in freshwater green algae

The coexistence of competing species depends on the balance between their fitness differences, which determine their competitive inequalities, and their niche differences, which stabilise their competitive interactions. Darwin proposed that evolution causes species' niches to diverge, but the influence of evolution on relative fitness differences, and the importance of both niche and fitness differences in determining coexistence have not yet been studied together. We tested whether the phylogenetic distances between species of green freshwater algae determined their abilities to coexist in a microcosm experiment. We found that niche differences were more important in explaining coexistence than relative fitness differences, and that phylogenetic distance had no effect on either coexistence or on the sizes of niche and fitness differences. These results were corroborated by an analysis of the frequency of the co‐occurrence of 325 pairwise combinations of algal taxa in > 1100 lakes across North America. Phylogenetic distance may not explain the coexistence of freshwater green algae.     

Competition in variable environments: experiments with planktonic rotifers

1. In a constant environment, competition often tends to reduce species diversity. However, several theories predict that temporal variation in the environment can slow competitive exclusion and allow competing species to coexist. This study reports on laboratory competition experiments in which two pairs of planktonic rotifer species competed for a phytoplankton resource under different conditions of temporal variability in resource supply.
2. For both species pairs, Keratella cochlearis dominated under all conditions of temporal variability, and the other species ( Brachionus calyciflorus or Synchaeta sp.) almost always went extinct. Increasing temporal variation in resource supply slowed competitive exclusion but did not change competitive outcome or allow coexistence.
3. Rotifers show a gleaner–opportunist trade-off, because gleaner species have low threshold resource levels ( R *) and low maximum population growth rates, while opportunist species have the opposite characteristics. In the competition experiments, the gleaner always won and the opportunists always lost. Thus, a gleaner–opportunist trade-off was not sufficient to facilitate coexistence under conditions of resource variability. Instead, the winning species had both the lowest R * and the greatest ability to store resources and ration their use during times of extreme resource scarcity.     

Rotifer communities from some Araucanian lakes of southern Chile

During the last decade much information has been produced about the zooplankton communities in southern Chile; however, most of this is related to the crustacean assemblages. The present communication examines the spatial and temporal distribution of rotifer assemblages and their relation to the environmental variables during one-year period in four Araucanian lakes. A total of 19 species was found in these oligotrophic lakes. Keratella cochlearis, Synchaeta stylata, Trichocerca porcellus, Conochilus unicornis and Collotheca pelagica were widespread, and seven species exhibited a more restricted distribution among the lakes. Species richness varied from 6 to 12; similarly, one or two dominant species usually accounted for more than 80% of the total annual abundance. Similar dominant species occurred in two lakes, but their maximum peaks of abundance differed in time; in the remaining lakes the most important species were different. Calculated rotifer diversity showed a fluctuating pattern, with low values during the year in three lakes, and high ones in Lake Llanquihue. Species diversity was significantly related to species richness in all lakes. Discriminant analysis based on the occurrence and abundances of species throughout the year revealed that the rotifer assemblage in Lake Llanquihue was different from that in the rest of the Araucanian lakes. Furthermore, the same analysis using environmental variables showed that this lake is clearly discriminated from the others on the basis of the ionic composition of the water (i.e. Cl^–, Na⁺, Mg²⁺). Rotifer abundances in these lakes were significantly influenced by a number of abiotic variables, including those related to water ionic composition. These relationships may imply that the small differences in chemical characteristics of these lakes influence the structure of the rotifer community.     

Deterioration patterns in diapausing egg banks of Brachionus (Müller, 1786) rotifer species

Rotifers are cyclical parthenogens that produce sexual diapausing eggs at some stage in their life cycle. These eggs are encysted embryos that remain viable for extended periods in lake and pond sediments, thus acting as an egg bank with many ecological and evolutionary consequences. Despite its importance to rotifer evolution, there are no studies on resting egg deterioration and associated processes in natural environments. In this study, more than 4000 diapausing eggs of species from the Brachionus plicatilis complex, which includes several closely related cryptic species, were collected from different sediment depths in 15 ponds in eastern Spain and were classified according to three features thought to be related to their viability: shell integrity, embryo size, and embryo colour. A positive association was found between embryo size and hatching success in those eggs having an intact shell. Diapausing eggs that showed good shell integrity and no more than a 25% reduction of multinuclear embryo maximum size were classified as healthy and 98.9% hatched. Darkening of diapausing egg embryo was an indicator of viability loss. A decreasing frequency of healthy-looking diapausing eggs was observed with increasing sediment depth, although some exceptions were found.     

Differences in Life-Histories Refute Ecological Equivalence of Cryptic Species and Provide Clues to the Origin of Bathyal Halomonhystera (Nematoda)

The discovery of morphologically very similar but genetically distinct species complicates a proper understanding of the link between biodiversity and ecosystem functioning. Cryptic species have been frequently observed to co-occur and are thus expected to be ecological equivalent. The marine nematode Halomonhystera disjuncta contains five cryptic species (GD1-5) that co-occur in the Westerschelde estuary. In this study, we investigated the effect of three abiotic factors (salinity, temperature and sulphide) on life-history traits of three cryptic H. disjuncta species (GD1-3). Our results show that temperature had the most profound influence on all life-cycle parameters compared to a smaller effect of salinity. Life-history traits of closely related cryptic species were differentially affected by temperature, salinity and presence of sulphides which shows that cryptic H. disjuncta species are not ecologically equivalent. Our results further revealed that GD1 had the highest tolerance to a combination of sulphides, high salinities and low temperatures. The close phylogenetic position of GD1 to Halomonhystera hermesi, the dominant species in sulphidic sediments of the Håkon Mosby mud volcano (Barent Sea, 1280 m depth), indicates that both species share a recent common ancestor. Differential life-history responses to environmental changes among cryptic species may have crucial consequences for our perception on ecosystem functioning and coexistence of cryptic species.     

Evolutionary coexistence in a fluctuating environment by specialization on resource level

Microbial communities in fluctuating environments, such as oceans or the human gut, contain a wealth of diversity. This diversity contributes to the stability of communities and the functions they have in their hosts and ecosystems. To improve stability and increase production of beneficial compounds, we need to understand the underlying mechanisms causing this diversity. When nutrient levels fluctuate over time, one possibly relevant mechanism is coexistence between specialists on low and specialists on high nutrient levels. The relevance of this process is supported by the observations of coexistence in the laboratory, and by simple models, which show that negative frequency dependence of two such specialists can stabilize coexistence. However, as microbial populations are often large and fast growing, they evolve rapidly. Our aim is to determine what happens when species can evolve; whether evolutionary branching can create diversity or whether evolution will destabilize coexistence. We derive an analytical expression of the invasion fitness in fluctuating environments and use adaptive dynamics techniques to find that evolutionarily stable coexistence requires a special type of trade-off between growth at low and high nutrients. We do not find support for the necessary evolutionary trade-off in data available for the bacterium Escherichia coli and the yeast Saccharomyces cerevisiae on glucose. However, this type of data is scarce and might exist for other species or in different conditions. Moreover, we do find evidence for evolutionarily stable coexistence of the two species together. Since we find this coexistence in the scarce data that are available, we predict that specialization on resource level is a relevant mechanism for species diversity in microbial communities in fluctuating environments in natural settings.     

Fish introductions reveal the temperature dependence of species interactions

A major area of current research is to understand how climate change will impact species interactions and ultimately biodiversity. A variety of environmental conditions are rapidly changing owing to climate warming, and these conditions often affect both the strength and outcome of species interactions. We used fish distributions and replicated fish introductions to investigate environmental conditions influencing the coexistence of two fishes in Swedish lakes: brown trout (Salmo trutta) and pike (Esox lucius). A logistic regression model of brown trout and pike coexistence showed that these species coexist in large lakes (more than 4.5 km²), but not in small, warm lakes (annual air temperature more than 0.9–1.5°C). We then explored how climate change will alter coexistence by substituting climate scenarios for 2091–2100 into our model. The model predicts that brown trout will be extirpated from approximately half of the lakes where they presently coexist with pike and from nearly all 9100 lakes where pike are predicted to invade. Context dependency was critical for understanding pike–brown trout interactions, and, given the widespread occurrence of context-dependent species interactions, this aspect will probably be critical for accurately predicting climate impacts on biodiversity.     

Distribution of rotifers in North Island,New Zealand,and their potential use as bioindicators of lake trophic state

The distribution and ecology of planktonic rotifers was investigated in 33 lakes in the North Island, New Zealand, between 1997 and 1999. A total of 79 species of monogonont rotifer were identified, with an average of 21 species per lake, a diversity which is high in comparison with many previous New Zealand studies. Most species recorded were cosmopolitan taxa, and were widespread in their distribution over the North Island. Multivariate analyses (Multi-Dimensional Scaling and Canonical Correspondence Analysis) did not distinguish distinct lake groupings based on rotifer communities, but rather gradients in assemblages, which were most highly associated with lake trophic state. Based on these responses, the development of potential rotifer bioindicator schemes for lake trophic state is described and discussed.