Torsten Hauffe

Mollusc Biodiversity and Endemism in the Potential Ancient Lake Trichonis, Greece

ABSTRACT Ancient lakes are hotspots of biodiversity, often harboring a large number of endemic species that make them prime model systems for evolutionary biologists. Besides such well-recognized ancient or long-lived lakes as Baikal, Biwa, Ohrid, and Tanganyika, there are other potentially old and biodiverse lakes in the world with poorly specified ages and under-studied faunas. We here report on the mollusc fauna of one such lake, Lake Trichonis in continental Greece. This graben lake is situated in a highly tectonized area, characterized by karst features and probably of middle to late Pliocene origin. Lake Trichonis is deep, oligotrophic, and rich in such specific habitat types as macrophyte meadows, rocky shores and sublacustrine spring systems. Moreover, it is a hotspot of freshwater biodiversity in Greece, particularly in molluscs. After reviewing newly collected material and the published mollusc records, we found that at least 33 mollusc species occur in Lake Trichonis, with 24 gastropod and 9 bivalve species currently being recognized. This is 24% of the total freshwater mollusc diversity of Greece; 21% of the gastropods (five species) are endemic to Lake Trichonis. If the whole Trichonis Basin is considered, which also includes neighboring Lake Lysimachia, eight species (33%) of the total fauna appear to be endemic. Taking lake surface areas into account, the index of gastropod endemism of 0.442 (log Nendemic species/log Asurface area) for the Lake Trichonis Basin resembles on a world-wide scale values known for Lake Baikal, Russia, and Lake Biwa, Japan, and is only exceeded by Lake Ohrid, Macedonia/Albania, and ancient lakes of Sulawesi, Indonesia. Despite the limited knowledge about the lakes evolutionary history, the suggested age of origin, the palaeogeographical characteristics, and the potential timing of phylogenetic events reviewed here support the presumed status of Lake Trichonis as an ancient lake. From a conservational standpoint, more research, management and conservation efforts are necessary because ancient lakes are among the most vulnerable and threatened ecosystems on earth. Effects of human-induced environmental change are already noticeable in Lake Trichonis. Recognition of Lake Trichonis as a unique system with an unusually high biodiversity may help promoting conservation efforts.

The role of barriers and gradients in differentiation processes of pyrgulinid microgastropods of Lake Ohrid

Ancient Lake Ohrid is characterized by vertical (bathymetrical) zones within the lake, presumably promoting allopatric speciation due to barriers or parapatric speciation along gradients. Examples within the lake include the belt of Chara algae as well as the shell zone, both presumably impeding migrations of benthic invertebrates. Three potential cases of vertical differentiation leading to distinct depth forms have been reported for the gastropod subfamily Pyrgulinae (Caenogastropoda: Hydrobiidae): Ginaia munda ssp., Macedopyrgula spp. and Ochridopyrgulamacedonica ssp. Based on DNA data of the COI gene from a total of 145 specimens, this article aims at investigating the vertical differentiation within these depth forms and thus patterns of speciation in Lake Ohrid. An initial morphometric analysis showed a clear correlation of shell shape and collecting depth for Ginaia munda ssp. and Macedopyrgula spp. This morphological trend is largely reflected in the genetic structure of the respective taxa. The data presented here indicate the existence of strong gradients of abiotic and biotic factors in Lake Ohrid rather than distinct barriers. Therefore, parapatric speciation may be the predominant form of differentiation of benthic invertebrates in the lake. Incomplete lineage sorting, hybridization and phenotypic plasticity possibly caused by epigenetic mechanisms are discussed as possible reasons for the incongruence between geno- and phenotype observed in few specimens of Ginaia munda ssp. and Macedopyrgula spp. For the third taxon, Ochridopyrgulamacedonica ssp., morphometric and genetic analyses revealed only weak support for the previously proposed depth forms. However, a horizontal differentiation of lake and spring populations was revealed instead, and parapatric and allopatric differentiations are discussed in this taxon.

Invaders versus endemics: alien gastropod species in ancient Lake Ohrid

Species invasions into ancient lakes are an important but little understood phenomenon. At ancient Lake Ohrid, a systematic assessment of invasive mollusc species using morphological and genetic data was conducted from 2003 to 2012. Two globally invasive gastropod species, Physa acuta and Ferrissia fragilis, have recently been discovered at 4 out of 386 sites. These sites are anthropogenically impacted. The invasive species co-occur with endemics. Phylogenetic analyses of populations from native and invaded ranges of both species confirmed their identities and provided insights into their invasion histories. Accordingly, P. acuta is genetically more diverse than F. fragilis. Both species are currently present in a considerable number of lakes on the Balkan Peninsula. Possible future trends in Lake Ohrid and the Balkans are discussed and further spread of both species is likely. Given the ongoing environmental change in Lake Ohrid, the number of observations of non-indigenous or other widespread species will probably rise in the coming years and such species and their impact on native species should be carefully monitored. Moreover, ancient lakes with recurrent invasions of alien species might serve as interesting model systems for the study of important topics of invasion biology.

Mollusc biodiversity in a European ancient lake system: lakes Prespa and Mikri Prespa in the Balkans

The spatial distribution of (endemic) biodiversity in ancient and potentially ancient lakes in Europe is poorly understood. Examples include Lakes Prespa and Mikri Prespa in the Central Balkans. Utilizing information of the most species-rich taxon in these lakes, the Mollusca, we therefore attempt to statistically assess and visualize the spatial distribution of biodiversity, to analyse biogeographical patterns, and to carry out a conservation assessment. We estimate that at least 40 (sub)species (29 gastropod and 11 bivalve taxa) occur in the lakes. For both lakes combined, 37.5% of the mollusc taxa are endemic. In general, the mollusc richness in Lake Mikri Prespa is lower than in Lake Prespa and less heterogeneously distributed. The highest species richness can be seen on the western and south eastern shores of Lake Prespa. Based on the presence/absence of genera, a minimum spanning tree analysis supports the sister lake relationship of both lakes, which, in turn, are most closely related to lakes in the western Balkans and not to nearby Lake Ohrid. The IUCN red list assessment revealed (A) a tendency towards mollusc faunal change, (B) a contemporary decline and potential loss of mollusc diversity, and (C) that all endemic species are of conservation concern.

A new approach for dating introduction events of the quagga mussel (Dreissena rostriformis bugensis)

Determining the temporal or spatial origin of an invasive population is a challenging task as first detections are often made only after the respective species is established. In this study we propose an indirect method for dating introduction events. It is based on the characteristic competition dynamics of two invasive freshwater taxa in Western Europe: the established invader Dreissena polymorpha (zebra mussel) and the recent invader Dreissena rostriformis bugensis (quagga mussel). The underlying assumption is that in sympatric populations, the quagga mussel outcompetes the zebra mussel over time. Thus, relative abundance of the quagga mussel might correlate with time since introduction. On a European scale, we tested this assumption with a combination of data from field samplings and the literature. The correlation analysis confirmed the assumption of a time depended displacement of the zebra mussel by the quagga mussel. In a second step, we calculated the specific rates of displacement based on a regular monitoring of four selected sites in the western part of Europe. These time-series studies revealed an increase of relative abundance of the quagga mussel of 36% per year. We then tested our novel tool by using three case studies, showing that our estimations of quagga mussel introduction events are in concordance with data from independent studies. We propose that our method provides a useful tool to estimate the age of a given quagga mussel population within few years after introduction.

Spatially explicit modeling of Schistosomiasis risk in eastern China based on a synthesis of epidemiological, environmental, and intermediate host genetic data

Schistosomiasis japonica is a major parasitic disease threatening millions of people in China. Though overall prevalence was greatly reduced during the second half of the past century, continued persistence in some areas and cases of re-emergence in others remain major concerns. As many regions in China are approaching disease elimination, obtaining quantitative data on Schistosoma japonicum parasites is increasingly difficult. This study examines the distribution of schistosomiasis in eastern China, taking advantage of the fact that the single intermediate host serves as a major transmission bottleneck. Epidemiological, population-genetic and high-resolution ecological data are combined to construct a predictive model capable of estimating the probability that schistosomiasis occurs in a target area (“spatially explicit schistosomiasis risk”). Results show that intermediate host genetic parameters are correlated with the distribution of endemic disease areas, and that five explanatory variables—altitude, minimum temperature, annual precipitation, genetic distance, and haplotype diversity—discriminate between endemic and non-endemic zones. Model predictions are correlated with human infection rates observed at the county level. Visualization of the model indicates that the highest risks of disease occur in the Dongting and Poyang lake regions, as expected, as well as in some floodplain areas of the Yangtze River. High risk areas are interconnected, suggesting the complex hydrological interplay of Dongting and Poyang lakes with the Yangtze River may be important for maintaining schistosomiasis in eastern China. Results demonstrate the value of genetic parameters for risk modeling, and particularly for reducing model prediction error. The findings have important consequences both for understanding the determinants of the current distribution of S. japonicum infections, and for designing future schistosomiasis surveillance and control strategies. The results also highlight how genetic information on taxa that constitute bottlenecks to disease transmission can be of value for risk modeling.

Benthic primary production in an upwelling-influenced coral reef, Colombian Caribbean

In Tayrona National Natural Park (Colombian Caribbean), abiotic factors such as light intensity, water temperature, and nutrient availability are subjected to high temporal variability due to seasonal coastal upwelling. These factors are the major drivers controlling coral reef primary production as one of the key ecosystem services. This offers the opportunity to assess the effects of abiotic factors on reef productivity. We therefore quantified primary net (Pn) and gross production (Pg) of the dominant local primary producers (scleractinian corals, macroalgae, algal turfs, crustose coralline algae, and microphytobenthos) at a water current/wave-exposed and-sheltered site in an exemplary bay of Tayrona National Natural Park. A series of short-term incubations was conducted to quantify O2 fluxes of the different primary producers during non-upwelling and the upwelling event 2011/2012, and generalized linear models were used to analyze group-specific O2 production, their contribution to benthic O2 fluxes, and total daily benthic O2 production. At the organism level, scleractinian corals showed highest Pn and Pg rates during non-upwelling (16 and 19 mmol O2 m−2 specimen area h−1), and corals and algal turfs dominated the primary production during upwelling (12 and 19 mmol O2 m−2 specimen area h−1, respectively). At the ecosystem level, corals contributed most to total Pn and Pg during non-upwelling, while during upwelling, corals contributed most to Pn and Pg only at the exposed site and macroalgae at the sheltered site, respectively. Despite the significant spatial and temporal differences in individual productivity of the investigated groups and their different contribution to reef productivity, differences for daily ecosystem productivity were only present for Pg at exposed with higher O2 fluxes during non-upwelling compared to upwelling. Our findings therefore indicate that total benthic primary productivity of local autotrophic reef communities is relatively stable despite the pronounced fluctuations of environmental key parameters. This may result in higher resilience against anthropogenic disturbances and climate change and Tayrona National Natural Park should therefore be considered as a conservation priority area.

Phenotypic diversity, population structure and stress protein-based capacitoring in populations of Xeropicta derbentina, a heat-tolerant land snail species

The shell colour of many pulmonate land snail species is highly diverse. Besides a genetic basis, environmentally triggered epigenetic mechanisms including stress proteins as evolutionary capacitors are thought to influence such phenotypic diversity. In this study, we investigated the relationship of stress protein (Hsp70) levels with temperature stress tolerance, population structure and phenotypic diversity within and among different populations of a xerophilic Mediterranean snail species (Xeropicta derbentina). Hsp70 levels varied considerably among populations, and were significantly associated with shell colour diversity: individuals in populations exhibiting low diversity expressed higher Hsp70 levels both constitutively and under heat stress than those of phenotypically diverse populations. In contrast, population structure (cytochrome c oxidase subunit I gene) did not correlate with phenotypic diversity. However, genetic parameters (both within and among population differences) were able to explain variation in Hsp70 induction at elevated but non-pathologic temperatures. Our observation that (1) population structure had a high explanatory potential for Hsp70 induction and that (2) Hsp70 levels, in turn, correlated with phenotypic diversity while (3) population structure and phenotypic diversity failed to correlate provides empirical evidence for Hsp70 to act as a mediator between genotypic variation and phenotype and thus for chaperone-driven evolutionary capacitance in natural populations.

Multi-scale processes drive benthic community structure in upwelling-affected coral reefs

Environmental processes acting at multiple spatial scales control benthic community structures in coral reefs. However, the contribution of local factors (e.g., substrate availability and water clarity) vs. non-local oceanographic processes (e.g. upwelling events) in these highly complex systems is poorly understood. We therefore investigated the relative contribution of local and non-local environmental factors on the structure of benthic groups and specifically on coral assemblages in the upwelling-affected Tayrona National Natural Park (TNNP, Colombian Caribbean). Coral-dominated communities were monitored along with key environmental parameters at water current-exposed and -sheltered sites in four consecutive bays. Regression tree analyses revealed that environmental parameters explained 59.1% of the variation within the major benthic groups and 36.1% within coral assemblages. Findings also showed recurring patterns in community structures at sites with similar exposure across bays. We suggest that benthic community composition in TNNP is primarily driven by 1) wave exposure, followed by 2) temporal changes in nutrient availability governing the structure of benthic groups, and 3) local bay-specific differences controlling the zonation of benthic groups and coral assemblages. This study highlights the existence of complex hierarchical levels of local and non-local environmental factors acting on reef communities and stresses the importance of considering processes operating at multiple spatial scales in future studies on coral reef community structure and resilience.

Environmental heterogeneity predicts species richness of freshwater mollusks in sub-Saharan Africa

Species diversity and how it is structured on a continental scale is influenced by stochastic, ecological, and evolutionary driving forces, but hypotheses on determining factors have been mainly examined for terrestrial and marine organisms. The extant diversity of African freshwater mollusks is in general well assessed to facilitate conservation strategies and because of the medical importance of several taxa as intermediate hosts for tropical parasites. This historical accumulation of knowledge has, however, not resulted in substantial macroecological studies on the spatial distribution of freshwater mollusks. Here, we use continental distribution data and a recently developed method of random and cohesive allocation of species distribution ranges to test the relative importance of various factors in shaping species richness of Bivalvia and Gastropoda. We show that the mid-domain effect, that is, a hump-shaped richness gradient in a geographically bounded system despite the absence of environmental gradients, plays a minor role in determining species richness of freshwater mollusks in sub-Saharan Africa. The western branch of the East African Rift System was included as dispersal barrier in richness models, but these simulation results did not fit observed diversity patterns significantly better than models where this effect was not included, which suggests that the rift has played a more complex role in generating diversity patterns. Present-day precipitation and temperature explain richness patterns better than Eemian climatic condition. Therefore, the availability of water and energy for primary productivity during the past does not influence current species richness patterns much, and observed diversity patterns appear to be in equilibrium with contemporary climate. The availability of surface waters was the best predictor of bivalve and gastropod richness. Our data indicate that habitat diversity causes the observed species–area relationship, and hence, that environmental heterogeneity is a principal driver of freshwater mollusk richness on a continental scale.