Schmidtea mediterranea ( Benazzi, Baguñà, Ballester & Del Papa, 1975 ), Benazzi, Baguna, Ballester & Del Papa, 1975

Vila-Farré, Miquel, Sluys, Ronald, Almagro, Ío, Handberg-Thorsager, Mette & Romero, Rafael, 2011, Freshwater planarians (Platyhelminthes, Tricladida) from the Iberian Peninsula and Greece: diversity and notes on ecology, Zootaxa 2779, pp. 1-38 : 31-35

Schmidtea mediterranea ( Benazzi, Baguñà, Ballester & Del Papa, 1975)

( Fig. 1 )

Discussion of the Iberian populations. The Mediterranean species Schmidtea mediterranea has been reported in Barcelona, Girona ( Fig. 1 ), Menorca, Mallorca, Corsica, Sardinia, Sicily and Tunisia ( Benazzi et al. 1975; De Vries et al. 1984; Baguñà et al. 1999; Harrath et al. 2004). Spanish animals belong to an asexual strain that is only able to reproduce by means of fission, whereas members of other populations undergo sexual reproduction. In Barcelona, S. mediterranea is found only in the pond system of the Montjuïc Mountain, within the city’s perimeter. During recent sampling on Montjuïc, we only found the species in the “Viver dels Tres Pins”, a plant nursery with several ponds. We have not found specimens in Girona, although we searched on one occasion.

General remarks on diversity. The triclad fauna of Europe is mainly formed by three ecological groups of species. The first includes hypogean and groundwater species that are particularly speciose in France, central and eastern Europe, e.g. several dendrocoelids, Ph. vitta (which are also present in streams), Plagnolia vandeli De Beauchamp & Gourbault, 1964 , Polycelis benazzi De Beauchamp, 1955 , Crenobia alpina anophthalma (Mrázek, 1907) and Dugesia absoloni (Komárek, 1919) (see Dahm & Gourbault, 1978). Cave-dwelling species of this group are very scarce in Spain.

The second group is formed by spring- and cold stream-dwelling species. From that group, members of the genus Phagocata are considered to be typical inhabitants of springs (cf. Roca et al. 1992) and widely distributed in southern Europe. Crenobia alpina (Dana, 1766) and Polycelis felina , whose distributions are restricted to cold streams and springs, are well represented in European and Iberian waters, whereas Dugesia gonocephala (Dugès, 1830) , a stream-dwelling species, is absent from Spain.

The third group of species includes warm water species and is represented in central and northern Europe by lake-dwelling triclads that are also present in warm rivers. These central European species typically reproduce sexually and have been reported very rarely in Spain and Portugal (see Baguñà et al. 1981; García-Mas & Jiménez, 1984). Here, as well as in the rest of the Mediterranean area, the genus Dugesia Girard, 1850 is very abundant. In this region, populations of Dugesia with a triploid karyotype that reproduce by fissiparity are exceptionally abundant ( Lázaro et al. 2009) and outnumber diploid sexual populations, and triploid parthenogenetic populations in certain areas, such as the Iberian Peninsula. In general terms, the number of species that are capable of reproduction by fission increases from northern to southern Europe.

Nevertheless, this ecological classification is not absolute (cf. Reynoldson, 1974). In general terms, lake-dwelling species also inhabit quiet areas of rivers, while stream species may also be present in cold lakes ( Reynoldson, 1953). Dendrocoelum lacteum is a lake-dwelling triclad, but it has been found in rapid streams in southern Sweden, where it has taken the spatial niche of Crenobia alpina ( Herrmann, 1986) . In the Iberian Peninsula, the lake-dwelling species Schmidtea polychroa mainly occurs in rivers, as lowland natural lakes are rarely present in this area.

Traditionally, the Iberian Peninsula was considered to be relatively poor in triclad species. However, the new data in this paper suggest that the low species richness of the Iberian Peninsula is due to a collector’s artefact, and that our knowledge of the number of species and of their distribution is far from complete. However, our samples confirm that lake-dwelling species are scarce in this area. These ecological trends are described in more detail below, albeit with the caveat that major areas of the Iberian Peninsula (e.g. Central and Southern Spain) remain to be explored.

Hypogean and groundwater species in Spain. Most of the dendrocoelids from central and western Europe occur in hypogean habitats and have a very small distribution range, as far as is known. Dendrocoelum lacteum is the only epigean species that is widely distributed in Europe and is present in both lakes and rivers. We have only found two new populations of dendrocoelids, which are probably inhabitants of hypogean waters. Species of this group are rarely observed in surface waters and this could be why D. inexspectatum was only found on one occasion, even though we visited the same station several times. Hypogean species are hard to find. We suspect that they occur in many other areas of the Iberian Peninsula, but will only be found after intensive sampling efforts that include caves. The northern Pyrenees are rich in hypogean dendrocoelids ( Gourbault, 1972) and the southern slopes of these mountains will probably yield greater diversity after detailed study.

Phagocata vitta , a white planarian that is widely distributed in Europe, occurs in springs, seasonal waters and brooks ( Gourbault, 1972; Ball & Reynoldson, 1981). In Spain, a white hypogean planarian similar to Ph. vitta is treated here as Phagocata sp. and has been found at fifteen localities (about eleven during our sampling; Fig. 1 ). Its distribution seems to be discontinuous when only surface waters are considered, but the species may be widespread, as it mainly occurs in groundwater. At several localities, the species has only been observed after rainy periods when groundwater emerges on the surface. In addition, the hypogean habit means that traps frequently need to be used to catch specimens, which are only sporadically present in surface waters. Phagocata vitta is the only European member of the genus that has colonized the northernmost areas of the continent and the British Isles. However, the taxonomic status of this wide-ranging species is uncertain, due to the presence of different karyological races in Europe (see Roca et al. 1992 and references therein).

Currently, it is not possible to determine whether the Iberian populations of this white Phagocata represent a new species or one of the known species, as we have not collected sexually reproductive specimens. Therefore, we have followed a conservative approach to taxonomy and refer to these animals as Phagocata sp.

Diversity of the genus Phagocata in Spain. Balkan species of the genus Phagocata form an anatomically homogeneous group of planarians with characteristic histology of the copulatory apparatus (cf. Kenk, 1978). They form a spermatophore that is used in the transfer of sperm to the copulatory bursa of the partner. All members of this Balkan group are white, with the exception of Ph. maculata . However, the pigmentation of the latter is usually reduced to some spots and its internal anatomy conforms closely to that of the rest of the Balkan Phagocata .

The analysis of the anatomy and distribution of Phagocata species in Spain reveals the presence of a heterogeneous group whose only distinctive characteristic is its pigmentation. The species presents diverse histology of the copulatory apparatus from which no common morphological feature can be extracted, except for the presence of a weak penis bulb and the absence of a spermatophore. The histological organization of the ejaculatory duct is very diverse, in contrast with the homogeneous structure of the ejaculatory duct in the Balkan species.

Four out of the five Iberian epigean species are restricted to only a few freshwater springs and adjacent streams. This suggests that the morphological diversity may partly be the result of springs functioning as isolating barriers in speciation ( Nielsen, 1950, 1951; Hubbs, 1961; Roca et al. 1992) and genetic differentiation ( Brändle et al. 2005). For example, studies of spring populations of Crenobia alpina in Germany ( Brändle et al. 2005) show that this species forms rather isolated populations with little dispersal between springs. Furthermore, it is suggested that the genetic differentiation between populations does not reflect the present geography of drainage systems, but the geography of the ancestral drainage system of the area ( Brändle et al. 2005). Similarly, the geological history of the Iberian Peninsula, where the Mediterranean rivers have been isolated for long periods of time, may have led to species differentiation in the genus Phagocata in the same way as was suggested for other Iberian groups with poor dispersal ability, such as fish and hydrobid snails ( Arconada & Ramos, 2003).

We have never observed reproduction by fission in this group of epigean species. On one occasion, we collected only asexual specimens of Ph. gallaeciae from Ourense (river Miño, Galicia). The population was abundant at that time, but no sexual specimen could be found. This suggests that the species may become asexual for part of the year, although this needs to be analysed in more detail.

Phagocata gallaeciae inhabits the Miño, a river with a large effluence. This is a very unusual habitat, as members of this genus are usually restricted to springs and creeks associated with cold microhabitats ( Reynoldson, 1965 and references therein). However, we have never found Phagocata species in springs in this area or on the Cantabrian coast, where wells are inhabited by Polycelis felina or, more rarely, by Dugesia sp.

In 1918 at the Quelle de la Figuereta spring (Lleida, northeastern Spain), Arndt (1926) collected two immature or asexual specimens of an unidentified brown planarian. He suggested that these specimens, classified as Planaria sp., could belong to the species Planaria lugubris ( Schmidtea lugubris (Schmidt, 1861) , but note that at that time S. lugubris and S. polychroa were frequently confused). We visited the site and observed brown individuals of Phagocata that were externally identical to Phagocata pyrenaica . Two sexual specimens were sectioned (V.Pl.6877.1, V.Pl.6877.2). An examination of their copulatory apparatuses confirmed their identity as members of Ph. pyrenaica . In addition, this locality is only about 10 km from the type locality of this species (populated by transparent specimens) and about 16 km from the other known locality (near Basturs, which is populated by brown specimens). Therefore, we believe that Arndt (1926) collected immature specimens of the brown form of Phagocata pyrenaica . Despite the fact that he collected “ Planaria lugubris ” in the river nearby, springs are not a suitable habitat for this lake-dwelling species ( Ball & Reynoldson, 1981) or for its close relative Schmidtea polychroa .

Apparent scarcity of lake-dwelling species in the Iberian Peninsula. Central European lake-dwelling triclads with sexual reproduction that also occur in warm rivers are very rare in the Iberian Peninsula. Three of these species, Schmidtea lugubris , Planaria torva (Müller, 1774) and Polycelis tenuis , have been reported in Spain and Portugal on several occasions, but their presence is very doubtful as the records are usually based on external morphology only. Polycelis nigra and Dendrocoelum lacteum are known in only a few localities. Schmidtea polychroa is the only member of this group that is widely distributed in Spain ( Fig. 1 ). Baguñà et al. (1981) proposed that the significant absence of lake-dwelling species is partially due to the scarcity of natural lakes at low altitude. However, these species also occur in rivers. Therefore, shortage of lakes alone cannot explain their rarity. Historical factors apparently have not prevented the occurrence of some of the species of this group, as D. lacteum and P. nigra are present in the Iberian Peninsula. Regarding ecological factors, temperature and oxygen concentration in Iberian rivers most likely do not constrain their distribution. An alternative explanation is that the characteristic highly seasonal discharge pattern of the Mediterranean rivers, with periodical torrential floods and severe droughts ( Bonada et al. 2007), favours the predominance of species with asexual reproduction. In particular, it favours species of the genus Dugesia , which is dominant in the Mediterranean sector of Spain. Four factors may promote the success of asexual species or populations. First, this reproductive trait allows rapid colonization of recently disturbed areas, even under conditions of very low population density ( Lázaro et al. 2009). Second, the size of a Dugesia specimen that originates from the tail of a fissiparous individual (the equivalent of a hatchling emerging from an egg capsule) is bigger than hatchlings of any of these European species (pers. obs.), which increases its chances of survival. Third, the embryonic development of the egg capsules lasts on average about 20 days at 20 ºC, while complete regeneration of a tail piece of Dugesia takes only about five days under similar thermal conditions. This suggests that the fissiparous species can more rapidly adapt to changing environmental conditions. Fourth, egg-laying species are better competitors in areas with high levels of resources ( Reynoldson, 1961; Calow et al. 1979), which is probably not the case in disturbed areas, such as Mediterranean rivers just after long periods of floods or drought. The fact that several Spanish freshwater planarians may encapsulate in a thin cocoon of mucus under unfavourable environmental conditions (Ribas, 1990) or in the laboratory (present work) suggests that this is an adaptation to the irregular water levels in Mediterranean rivers. Ribas (1990) found that Schmidtea polychroa encysted inside mucous capsules in artificial canals that are frequently dry. Similarly, Ribas (1990) also observed specimens of Dugesia sicula Lepori, 1948 enclosed in pieces of humid mud. Our finding that P. nigra also encysts when starved suggests that European species living at the borders of their distribution range, in presumably non-optimal habitats, are able to use a survival strategy that has not been observed in other areas with more suitable environments.

Encystment in a mucous cyst has been reported in several other planarian species. It forms part of their asexual reproductive cycle in the following species: Phagocata velata and Ph. fawcetti from North America and several species of the genus Atrioplanaria De Beauchamp, 1932 . In Ph. velata and Ph. fawcetti , an animal may fragment into multiple pieces and each fragment is encased in mucous. In this condition, the fragment may survive dry periods in its vernal habitat (Ball et al. 1981). The European species Ph. vitta (Dugès, 1830) may also reproduce asexually by fragmentation ( Ball & Reynoldson 1981). In this species, specimens may encyst and thus survive in temporary springs ( Stankoviċ & Komárek, 1927).

Species of Atrioplanaria may also reproduce by fission or fragmentation. For several species of this genus, either entire animals or fragments may become enveloped in a mucous covering, viz. A. prosorchis (Kenk, 1937) , A. notadena ( De Beauchamp, 1937) , A. aquabellae Bromley, 1983 , A. sp. (cf. Bromley 1983 and references therein). Specimens of A. notadena may survive complete drying up of cave pools by being enclosed in clay whose hygroscopic properties provide a sufficient degree of humidity for the dormant individual ( Ginet & Puglisi, 1964).

The marine triclad Procerodes lobatus (Schmidt, 1861) may also encapsulate in a thin, transparent and elastic capsule. As the animals may encapsulate under otherwise favourable environmental conditions and the capsules cannot totally prevent desiccation, researchers have been unable to provide a satisfactory explanation for this behaviour (cf. Sluys, 1989 and references therein). The same may apply to the egg capsules with a mucous layer in P. n i g r a or the encystment of adults, i.e. that these mucous capsules are probably not sufficient to prevent desiccation in case of total absence of water. However, these structures probably enhance the probability of survival if some water remains in the river. Similarly Child (1913) observed that encapsulated pieces of Phagocata velata were not able to resist total desiccation. However, the species was able to survive in “ditches and pools partly filled with dead leaves where even though the water disappears, the bottom under the thick layer of leaves is always more or less wet and the encysted pieces are not subjected to drying” ( Child 1913, p. 182). Encysted adult specimens of P. n i g r a are apparently totally inactive (no movement was observed), which may be a way to reduce energy consumption under starvation, a condition that promotes encystment of the animals, at least under laboratory conditions.

Notes on the ecology of Girardia tigrina . The great ability of G. t i g r i n a to colonize new environments is the result of several factors. First, it is able to use artificial channels for dispersal ( Wright, 1987). Second, dispersal through human activity facilitates the colonization of new water bodies ( Wright, 1987). Third, it is an opportunistic feeder that can exploit blooms of suitable prey ( Pickavance, 1971), and it can also prey on other triclads, at least under laboratory conditions ( Young & Reynoldson, 1999). Fourth, one animal is potentially able to establish a new population due to its great capacity of asexual reproduction ( Young & Reynoldson, 1999). Fifth, observations by Young & Reynoldson (1999 and references therein) and by the authors of the present work suggest that G. t i g r i n a adheres to surfaces (e.g. stones and vegetation) better than any other triclad species found in British and Iberian freshwaters, which may have contributed to its great success. Finally, G. t i g r i n a can tolerate very eutrophic habitats, brackish environments ( Wright, 1987) and warm waters ( Russier & Lascombe, 1970; Wright, 1987). The morphological variation observed between Iberian populations strongly suggests that independent introductions from its native area have recently occurred ( Ribas et al. 1989). Sluys et al. (2005) extensively discussed the morphological variation observed in various populations of G. tigrina from its native area as well as from regions in which it was introduced.

The species has been able to colonize several locations in the Iberian Mediterranean area due to the large network of agricultural irrigation channels. Although it is scarcely recorded in artificial water reservoirs, it is the only triclad that is present in these habitats, with the exception of one record of Dugesia sp. in the reservoir Pantà de Ulldecona (province of Castelló; northeastern Spain).

Girardia tigrina has been observed to coexist with all other known Spanish freshwater planarians, except Dendrocoelum spatiosum and the members of the genus Phagocata that are restricted to springs. This suggests that its partly opportunistic diet allows the species to successfully establish new populations at localities previously only inhabited by autochthonous Iberian planarians.

G. tigrina is restricted to nine sites in the Cantabrian Mountains and along the Cantabrian coast, where the relatively low temperature and frequently high velocity of the rivers running from the slopes of the mountains are not suitable for the species, as it is better adapted to warmer waters.

Schmidtea mediterranea in decline in the Iberian Peninsula. The species S. mediterranea has recently acquired new scientific relevance due to its appropriate physiological characteristics in relation to its regeneration abilities ( Kiefer, 2006). Furthermore it is an important model organism in developmental studies, which has resulted in the sequencing of its genome ( Robb et al. 2008). This provides additional reasons for the conservation of this natural population.

The asexual strain of S. mediterranea , which reproduces only by fission, is restricted in Spain to (1) a few sites on Montjuïc mountain, within Barcelona’s limits, (2) Girona and (3) the Balearic Islands. However, during recent sampling in Barcelona we observed a marked reduction in the number of populations. S. mediterranea disappeared from two ponds after they were reformed or cleaned. A third pond system, a plant nursery known as “Viver dels Tres Pins”, was successfully invaded by Schmidtea polychoa , whose external morphology is almost identical to that of S. mediterranea . We recorded S. polychroa from Montjuïc in 2007 and have observed its presence and reproduction up to the present time. S. polychroa is easily transported with aquatic plants and it is therefore able to colonize new habitats, as we have observed in an artificial pond recently constructed in Girona. Despite the fact that the possible interaction between S. polychroa and S. mediterranea is uncertain, there is some cause for concern as it has been shown that the introduction of alien planarians may result in the drastic decline of autochthonous species ( Reynoldson, 1985).

In the fourth pond on Montjuïc Mountain in which S. mediterranea was found, “Pantà de la Fuxarda”, we observed an abundant population of the introduced crayfish Procambarus clarkii (Girard, 1852) . Its introduction is known to cause dramatic changes in native plant and animal communities ( Gutiérrez-Yurrita & Montes, 1999). In addition, S. mediterranea was usually observed under the leaves of water lilies, which have disappeared (Emili Saló, personal communication). Finally, the size of the pond has been substantially reduced.

The second Iberian population of S. mediterranea is located in Girona, northeastern Spain. On a visit to the area we could not find any specimens. As we visited only one of the several possible habitats in that region, a more intensive sampling effort is needed to evaluate the situation of the species in this area.

Figures

FIGURE 1. Distributional records of the genera Schmidtea, Ph. sp. and Ph. cf. vitta in the Iberian Peninsula. Data from Arndt, 1926; Baguñà et al. 1980, 81; Ribas, 1990; Altaba et al. 1991; unpublished records, this study.