The biodiversity of the terrestrial malacofauna of Turkey – status and perspectives

Th e status of knowledge of the terrestrial malacofauna of Turkey is briefl y reviewed, and the perspectives for studies on the malacofauna of the country are discussed.


Introduction
Situated on the gateway between Europe and Asia, Turkey represents an important study area for biogeographical research (Demirsoy 1999).On its territory, several important biogeographic zones overlap, and thus species with close relationships to the European, Caucasian, Turanian, and Eremial malacocoenoses can be found.Additionally, the country is very rich in endemic taxa as well.Th e rich array of geomorphological structures supports a high rate of speciation and variation due to geographic isolation.Th e remarkable degree of climatological variation ranging from extremely humid subtropical to almost desert-like conditions off er a multitude of niches for terrestrial molluscs.Additionally, geological substrates considerably infl uence absence or presence of mollusc species, and also may have an impact on the size of living populations.
(rainfall throughout the year with more than 2000 mm precipitation).Th ese diff ering climatological types are mirrored by the potential vegetation of Turkey, which is composed by dense humid forests in the north and the Amanos Mountains, dry steppe forests in the center (embracing true steppes around Tuz Lake), supramediterranean dry forests in the Taurus Mountains, and a variety of Mediterranean dry forests in the west and the southern coast (Mayer andAksoy 1986, Hütteroth andHöhfeld 2002).
Th e transition of human society from rambling hunters to sessile farmers and shepherds took place in southeastern Turkey in the contact zone to the Fertile Crescent some 12.000 yrs ago (Schmidt 2006).Th e impact on the potential vegetation caused by these human activities and several minor climatic changes throughout this period formed the fragmented vegetation we encounter in Turkey today.
Terrestrial molluscs in general are capable to adapt to almost all types of landscapes.Th us, a country like Turkey with a high relief energie and diversifi ed climate and vegetation supports a similarly rich and diversifi ed malacofauna.Consequently, changes of landuse and climate as described above immediately impact the malacofauna causing areal shifts following the changing environmental conditions, including depletion or even complete loss of populations.Increasing pasture farming leads to a loss of forest vegetation, and thus to a loss of molluscan species adapted to forest conditions.Th e recent rise of average summer temperature due to Global Warming may particularly aff ect the Mediterranean species.During a fi eld survey in May/June 2006 (Gümüş, Gosteli and Neubert) we visited the coastal area between Fethiye and Kas and observed a considerable decrease in numbers of dead shells, and living specimens were extremely rare.Th is observation is confi rmed by many colleagues working in the eastmediterranean area, but a quantitative (and causal connective) analysis of the phenomenon is missing.However, it can be speculated that both, the average length of the dry summer period and the absolute temperature is rising, and that the aestivation period of species adapted to the Mediterranean type of drought is too long now.Th e animals die from starvation or desiccation, and several species or subspecies may already approach the verge of extinction.

Some historical aspects
Th e fi rst species from the Turkish terrestrial malacofauna were described by Guillaume-Antoine Olivier (1756Olivier ( -1814)), who, amongst others, collected natural history objects in the Middle East.For example he named the following species (Figs 1-3): Multidentula ovularis (Olivier, 1801) and Bulgarica denticulata (Olivier, 1801) from "Ghemlek" [= Gemlik in the Bay of Mudanya] or Assyriella guttata (Olivier, 1804) from Urfa (for more information on Olivier and his famous collection we refer to Tillier and Mordan 1983).After Olivier, the area was visited by the German J. R. Roth and his party (Roth 1839), and then was target of other scientists, naturalists and collectors like Bellardi, Boissier, Dubois de Montpereux, Frivaldsky, Huet de Pavillon, Parreyss, Schläfl i, Sievers and others.Th eir collections went to the most prolifi c malacologists interested in the area like Bourguignat, Charpentier, Küster, Mousson, L. Pfeiff er and Rossmässler.In the second half of the 19 th century, the famous German malacologists O. Boettger and W. Kobelt from the Senckenberg Museum in Frankfurt intensifi ed the malacological research in Turkey, with contributions by Nägele, Retowski and Westerlund.After Kobelt's death in 1916, the "Golden Age" of malacology was fi nished except for some contributions by P. Hesse, Lindholm and O. von Rosen.After almost 50 years of scientifi c silence, it was the "Netherlands biological expedition to Turkey 1959", which again shifted the focus of malacologists to Turkey (Anonymous 1963).Since then, the malacological science received an enormous boost and stimulated both international as well as Turkish scientists to deepen the knowledge of theTurkish malacofauna.During this period, which now lasts about 50 years, one third of the number of taxa accepted today as valid has been added!Some of the most active contributors to this success should be mentioned here (in alphabetic order of the surnames): Bank, R.A., Falkner, G., Forcart, L., Gittenberger, E., Gümüs, B.A., Hausdorf, B., Hudec, V., Menkhorst, H.P.M.G., Neubert, E., Nordsieck, H., Rähle, W., Riedel, A., Schütt, H., Şeşen, R., Szekeres, M.I., Wiktor, A. and Yıldırım, M.Z.

Status of knowledge
Calculation of the absolute number of taxa is somewhat arbitrary, because this number strongly correlates to the species concept favoured by the particular researcher.Traditionally, molluscs are an overdescribed group, at least on the species-level, and for Turkey an average of two to three additional synonym names for each taxon are available.Th is opens a large fi eld for lumpers and splitters and explains partly diff ering numbers.Th e calculation presented here off ers a balanced view over the majority of opinions regarding taxa numbers in particular groups published so far, and scrutinized by our own experience.
According to our fi les, the Turkish malacofauna currently comprises 730 valid species and subspecies of terrestrial snails belonging to 36 families.Th e degree of endemism for the area of Turkey is about 65 %.An analysis of the increase of species numbers since 1950 is presented in Table 1.It illustrates the enormous increase of taxonomical knowledge which was achieved during this relatively short period.
Still, the census of the malacobiodiversity of Turkey has to be continued, and large areas in the country remain white spots.Some of them, like the inneranatolian steppe areas, will not contribute essentially because of their relatively unsuitable habitats.However, the malacofauna of many of the densely forested mountain ranges are unsatisfactorily or almost completely unknown.Records of species new to science can be expected, and the knowledge about the ranges of already known taxa will be increased.Another increase in taxa numbers may be caused by the recovery of cryptic species with the help of DNA sequencing methods, the Barcoding Project and other related activities.We conclude that there are more species waiting to be recovered and described, and estimate the total number of species (including subspecies) will reach and probably surmount 1.000 taxa.It should be noted that Turkey also has a very rich freshwater malacofauna with an enormous degree of endemic species.Unfortunately, the scientifi c exploration of this interesting group still is in a quite unsatisfactory state, and reliable numbers for the content of species-and genus-level taxa are hardly to obtain.According to our unpublished catalogues, we estimate that Turkey is inhabited by 300 species of freshwater molluscs, at least.
Th e degree of endemism on species level is relatively high and is comparable to that of Greece, which houses the highest number of terrestrial snail taxa in Europe with a similarily high value of endemism (cf.CLECOM database).Th ese eastmediterranean landscapes with their specialised types of vegetation have been inhabited by particularly prolifi c malacocoenoses, which could develop there without any major interruption since the Pliocene.Th is is a major diff erence to Central Europe, where sequences of long-lasting glaciations were interrupted by warmer ice-free periods causing a permanent destruction and re-settlement by molluscs.Th is may be one of the reasons for the high endemism on species-and genus-level in the eastmediterranean and Middle East region.In Turkey, several pulmonate families reach a maximum of biodiversity (Table 2, Fig. 4).Th e prevalence of a few families was also reported by Cook (1997), who evaluated taxonomic and geographic patterns, endemism, and the relationship between shell dimensions, habitat requirements, niche occupancies and the competition bet- ween sympatric species.He concluded that the Turkish malacofauna is not that well balanced as that of (continental) Europe, and thus is more similar to that of island groups like for example the Madeiran Archipelago.He also suggested that the Turkish fauna still shows evidence of external penetration with some local radiation, and that Turkey has not been a major centre of evolutionary novelty.However, the study of Cook is based on the synopsis of Schütt (1993) using 336 species with several of them being wrongly identifi ed.Th e considerable increase of our knowledge since 1993 with description of new endemic taxa, the large number of new records for species outside Schütt's "zones"and the presumed backlog of not yet discovered species surely would nowadays yield a diff ering result and cast the "similarity" with Madeira into some doubt.

Future research perspectives
Th e extinction of species is a worldwide process with an increasing anthropogenous contribution.On a global scale, terrestrial molluscs belong to the most vulnerable taxa (Lydeard et al. 2004).Next to the already well documented threats, Global Warming will heavily aff ect terrestrial malacocoenoses by increasing desertifi cation of landscapes, aggradation of lakes, and decrease of water volumina available for wildlife.National and international strategies have to be developed to abate these eff ects as much as possible, but all eff orts will fail if we do not understand the system which is the target for protection.For this reason, science has to provide the basic data to achive sustained success for the protection of natural resources, which, last but not least, will protect mankind as well.
Th us, the fi rst step must be a complete survey of the species of molluscs living in Turkey, because only a species known by us can be protected!Th e hitherto malacological research and the revison of major groups of terrestrial snails resulted in a very detailed picture of the Turkish malacofauna.However, the potential backlog of 250 taxa (or even more) requires enormous eff orts for the future research.For this reason, the authors are about to launch some short-term projects which will focus on the investigation of the malacofauna of smaller areas which have been ommitted so far.For the long-term perspective, the following research topics should be addressed: 1) A nationwide survey with a parallel documentation of habitats, possible threats, etc. has to be conducted.Th is should follow a small-scaled itinery to make sure that each habitat is de facto covered.Th ese surveys should serve as a major source of specimens for all subsequent types of research.
2) Molecular studies on diff erent terrestrial and freshwater gastropods are increasingly used to revise the systematic position of taxa.However, for Turkey, there is only one molecular study concerning the family Clausiliidae of the Aegean and the Mediterranean regions (Uit de Weerd and Gittenberger 2004).We think that using DNA-Sequenzing in parallel to morphological work will recover more cryptic taxa in Turkey.It will support the research on phylogeny, evolutionary trends, speed of speciation, and many other interesting details of the Turkish malacofauna.
3) Preparation of a Red Data List of endangeroued species for Turkey.Prerequisit for such an enterprise is an extraordinarily good knowledge of the malacofauna, but also a broad understanding of the biology of the species, particularly of their specific niches and habitat requirements.Th is scientific branch, the aut-, dem-and synecology, is widely ignored in malacology, although here enormous advances of knowledge can be expected.Th ese data, once obtained, should be compiled and can be presented to the global community via organisations like IUCN and others.4) Snails are excellent indicator organisms for any kind of environmental research, because I) they colonise almost every habitat, II) the group is speciose, but not in too great numbers like insects, III) they are highly sensitive against short, medium or longscaled change of the environment, IV) they can be easily identified (once the survey is accomplished!),V) some species can be used as Flagship Species to raise public awareness for the protection of nature and the implementation of Nature Reserves.
5) A nation-wide independent institution like a Museum of Natural History is urgently needed to built up collections on the Turkish wildlife, to be used for comparison and to support further studies.Ideally, such an institution is accessible for anyone, who has a decided interest in snails, i.e. professionals as well as laymen.Today, Turkish malacologists keep their specimens in their private mollusk collections, and exchange of thoughts and specimens is cumbersome and ineff ective.A Museum of Natural History presents a perfect platform capable to satisfy all these requirements as exemplifi ed by many such museums in other countries.
6) Molluscs are one of the few groups that are well preserved in the fossil record, and for sure the most species-rich entity in excavations.Archaeomalacology -the study of molluscs in archaeological contexts -is a relatively new archaeological discipline.Th e field derived from archaeozoology, the study of animal remains from archaeological sites (Bar-Yosef Mayer 2008).Recently, archaeomalacology in Turkey has attracted the senior author and other Turkish colleagues like Dr. C. Çakırlar (Gümüş 2005(Gümüş , 2006;;Mienis and Gümüş 2007).Th ey have started to study recent and the subfossil shells from excavations in early human settlements like in Çatalhöyük (Çumra, Konya, in collaboration with Dr D. E. Bar-Yosef Mayer from Israel), in Şapinuva (Ortaköy, Çorum), and Troia (Çanakkale) (Çakırlar 2008).Subfossil shells have been collected from the walls of the archaeological sites (Fig. 5).An unusual fi nding of terrestrial snails in an Bronce-aged ship-wreck was recently recorded by Welter-Schultes (2001).Interestingly, snails have been used for various purposes by humans, and some of the species were identifi ed as having served as ornaments or probably were used as food (Fig. 6) (Bar-Yosef Mayer and Gümüş 2008).
Next to these human-related fields, the taxonomic composition of these findings can be used as indicators for the prevailing climatic conditions at the time when these  places have been settled by humans.Standardised comparisons with the recent malacofauna of the area may help to understand shifts in micro-and macroclimate.

Figure 4 .
Figure 4. Histogram showing the relative species richness of selected pulmonate families from Turkey in comparison to Europe (partly after CLECOM or own investigation).

Figure 5 .
Figure 5. Th e edge of a house wall where the freshwater and the terrestrial gastropods were collected from the excavation area in Catalhöyük archaeological site (Bar-Yosef Mayer and Gümüş 2008).

Figure 6 .
Figure 6.An assemblage of native pulmonate species found at Çatalhüyük (ca.10.000 y bp).Note the holes in the shells of a small terrestrial snail species on the bottom.Th ey probably were used as a necklace (Bar-Yosef Mayer and Gümüş 2008; Catalhoyuk Research Project Archives, Photographed by Burçin Aşkım Gümüş).

Table 1 .
Increase of newly described taxa within the last 30 years*.*Numbers do not count taxa exclusively described as new from Turkey.Th is is particularly true for genera.

Table 2 .
Comparison of species richness of important families between Turkey and Europe (based on Fauna Europaea).
Helicinae(high value for European Helicinae is caused by genus Murella from Sicily with > 100 taxa (to be merged to a single polymorphic species according to DNA-studies(Giusti and Manganelli, pers.comm.2007))52 283