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Ancient Lake Ohrid: biodiversity and evolution

  • SPECIATION IN ANCIENT LAKES
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Abstract

Worldwide ancient lakes have been a major focal point of geological, biological, and ecological research, and key concepts in, for example, evolutionary biology are partly based on ancient lake studies. Ancient lakes can be found on most continents and climate zones with most actual or putative ancient lakes in Europe being restricted to the Balkan Region. The arguably most outstanding of them is the oligotrophic and karstic Lake Ohrid, a steep-sided graben of rift formation origin situated in the central Balkans. Here, an attempt is made to summarize current knowledge of the geological, limnological, and faunal history of Lake Ohrid. Additionally, existing data on biodiversity and endemism in Lake Ohrid are updated and evaluated, and patterns and processes of speciation are reviewed in the context of the Ohrid watershed, including its sister lake, Lake Prespa. Whereas the geological history of the Ohrid Graben is relatively well studied, there is little knowledge about the limnological and biotic history of the actual lake (e.g., the age of the extant lake or from where the lake first received its water, along with its first biota). Most workers agree on a time frame of origin for Lake Ohrid of 2–5 million years ago (Mya). However, until now, the exact limnological origin and the origin of faunal or floral elements of Lake Ohrid remain uncertain. Two largely contrasting opinions either favour the theory of de novo formation of Lake Ohrid in a dry polje with a spring or river hydrography or a palaeogeographical connection of Lake Ohrid to brackish waters on the Balkan Peninsula. Whereas neither theory can be rejected at this point, the data summarized in the current review support the de novo hypothesis. An assessment of the fauna and flora of Lake Ohrid confirms that the lake harbours an incredible endemic biodiversity. Despite the fact that some biotic groups are poorly studied or not studied at all, approximately 1,200 native species are known from the lake, including 586 animals, and at least 212 species are endemic, including 182 animals. The adjusted rate of endemicity is estimated at 36% for all taxa and 34% for Animalia. In terms of endemic biodiversity, Lake Ohrid is with these 212 known endemic species and a surface area of 358 km2 probably the most diverse lake in the world, taking surface area into account. Preliminary phylogeographical analyses of endemic Lake Ohrid taxa indicate that the vast majority of respective sister taxa occurs in the Balkans and that therefore the most recent common ancestors of Ohrid- and non-Ohrid species likely resided in the region when Lake Ohrid came into existence. These data also indicate that there is relatively little faunal exchange and overlap between Lake Ohrid and its sister lake, Lake Prespa, despite the fact that the latter lake is a major water supplier for Lake Ohrid. Studies on selected species flocks and scatters, mostly in molluscs, point towards the assumption that only few lineages originally colonized Lake Ohrid from the Balkans and that the majority of endemic species seen today probably started to evolve within the lake during the early Pleistocene. Within the Ohrid watershed, endemism occurs at different spatial and taxonomic scales, ranging from species endemic to certain parts of Lake Ohrid to species endemic to the whole watershed and from subspecies to genus level and possibly beyond. Modes of speciation in the Ohrid watershed are largely affected by its degree of isolation. Observational evidence points towards both allopatric (peripatric) and parapatric speciation. Though sympatric speciation within a habitat is conceivable, so far there are no known examples. Today, the lake suffers from increasing anthropogenic pressure and a “creeping biodiversity crisis”. Some endemic species presumably have already gone extinct, and there are also indications of invasive species penetrating Lake Ohrid. The comparatively small size of Lake Ohrid and the extremely small range of many endemic species, together with increasing human pressure make its fauna particularly vulnerable. It is thus hoped that this review will encourage future research on the ecology and evolutionary biology of the lake’s taxa, the knowledge of which would ultimately help protecting this unique European biodiversity hot spot.

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Acknowledgements

We are extremely grateful to our colleagues from the Hydrobiological Institute Ohrid (HBI) for their immense support and hospitality and for encouraging our work. Without the continuous help from our dear friends, particularly from the institutes’ director, Goce Kostoski, and the benthos expert, Sasho Trajanovski, our work would have been impossible. Sonja Trajanovska, Biljana Budzakoska, and Bruno Streit took part in some field trips and/or provided valuable logistic support. Dimce Georgiev was always a very experienced scout and Zoran Brdarovski a safe skipper of the HBI research vessel. Both also helped a lot with sampling. Over the years, many graduate students took part in field trips, contributed to sampling efforts, and generated valuable data. They are gratefully acknowledged here. Kirstin Schreiber digitized the maps shown in Fig. 6; Anne-Kathrin Hauswald provided the photographs of Valvata spp. shown in Fig. 8; and Andreas Kubicek took the two underwater photographs shown in Fig. 11. We thank Mathias Harzhauser, Oleg Mandic, Andreas Matzinger, Sebastian Krastel, Jerzy Sell, and Bernd Wagner for valuable comments on an earlier version of the manuscript and for the fruitful discussions on Lake Ohrid issues. We are also very grateful to Thomas von Rintelen and Matthias Glaubrecht for reviewing the manuscript. Our work has been greatly inspired by the outstanding scientific contributions of the world authority on the evolution of Lake Ohrid—Sinisa Stankovic (1892–1974).

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  1. Department of Animal Ecology and Systematics, Justus Liebig University Giessen, Heinrich-Buff-Ring 26-32 (IFZ), 35392, Giessen, Germany

    Christian Albrecht & Thomas Wilke

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  1. Christian Albrecht
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Correspondence to Thomas Wilke.

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Guest editors: T. Wilke, R. Väinölä & F. Riedel

Patterns and Processes of Speciation in Ancient Lakes: Proceedings of the Fourth Symposium on Speciation in Ancient Lakes, Berlin, Germany, September 4–8, 2006

Glossary

Allopatric speciation

Evolution of reproductive barriers in populations that are prevented from exchanging genes at more than a negligible rate by a geographic barrier (Futyuma, 2005).

Anagenesis

Directional evolutionary change of various characteristics within a lineage (Futyuma, 2005).

Ancient lake

Extant lake that has existed since before the last glacial maximum. There is controversy as to the minimum age of an ancient lake. Whereas Gorthner (1994) proposed an age of at least 0.1 My, other workers suggest a considerably older minimum age.

Ancient sister lake

Ancient sister lakes are ancient lakes lying in close geographic proximity, sharing a related origin and significant time of co-existence, usually having hydrological connection as well as a balanced degree of faunal overlap and distinctness (Albrecht et al., 2008).

Aquifer

A formation, group of formations, or part of a formation that contains sufficient saturated permeable material yielding water to wells and springs (Field, 2002).

Cladogenesis

Branching of a lineage into two or more descendant lines (Futyuma, 2005).

Convergence

Similarities which have arisen independently in two or more organisms that do not share a common ancestry.

Endemic

Pertaining to a taxon that is restricted to the geographic area specified (Lomolino et al., 2006).

Intralacustrine

Within a lake.

Karst

A terrane, generally underlain by limestone or dolomite, in which the topography is chiefly formed by the dissolving of rock and which may be characterized by sinkholes, sinking streams, closed depressions, subterranean drainages, and caves (Field, 2002).

Lake proper

Actual continuous lake body excluding peripheral water bodies or effluents/affluents.

Long-lived lake

A lake of long existence that can be extant (ancient lake) or fossil (palaeolake) (Gorthner, 1994; Martens, 1997).

Palaeolake

A fossil ancient lake that existed in the past when hydrological conditions were different (Cohen, 2003).

Parapatric speciation

Divergence of neighbouring populations, between which there is modest gene flow, with subsequent reproductive isolation (Futyuma, 2005).

Peripatric speciation

Divergence of a small population from a widely distributed ancestral form (Futyuma, 2005).

Polje

A large, flat floored depression in karst limestone (Slavic polje: field) whose long axis is developed parallel to major structural trends (Field, 2002).

Ponor

Hole or opening (Slavic ponor: swallow hole) in the bottom or side of a depression where a surface stream or lake flows either partially or completely underground into the karst groundwater system (Field, 2002).

Proto-lake

The term “proto-lake” is sometimes used synonymously with the term “palaeolake”. Here, the term is used in association with pre-lake settings.

Radiation

Event of rapid cladogeneses.

Relict

Surviving taxon of a previous geological period or of ancient faunas and floras, whose close relatives have disappeared (e.g., Stankovic, 1960).

Short-lived lake

Mostly post-glacial lakes that go through a normal cycle of lake succession (see also ancient or long-lived lake).

Speciation

Evolutionary process leading to new species.

Species flock

In ancient lakes, monophyletic group of at least three species that are endemic to the lake but which may include taxa that today occur outside the lake (Greenwood, 1984; Schön & Martens, 2004).

Species scatter

A group of closely related taxa that are characterized by the criteria speciosity and endemicity but which do not represent a monophyletic entity (Hauswald et al., 2008).

Sympatric speciation

Evolution of reproductive barriers within a single, initially randomly mating population (Futyuma, 2005).

Thalassoid

Marine-like (Greek thalassa: sea). It refers to taxa that resemble marine taxa without necessarily having a marine origin. In ancient lake research, the term “thalassoid” is most often used to describe morphological or structural features of shells and other external body parts that are usually known from marine taxa (i.e., ribs, spines).

Watershed

Catchment area of a drainage basin.

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Albrecht, C., Wilke, T. Ancient Lake Ohrid: biodiversity and evolution. Hydrobiologia 615, 103–140 (2008). https://doi.org/10.1007/s10750-008-9558-y

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