WINTER ACTIVITY OF TERRESTRIAL ISOPODS FROM THERMAL HABITATS IN WESTERN ROMANIA

Terrestrial isopods from warm shores neighboring the thermal waters from western Romania remain active in the winter. This phenomenon is registered in 35 habitats, affecting 12 species (Hyloniscus transsilvanicus, H. riparius, Haplophthalmus danicus, Trichoniscus sp., Androniscus roseus, Cylisticus convexus, Protracheoniscus politus, Trachelipus nodulosus, T. rathkii, Porcellio dilatatus, Armadillidium vulgare, A. versicolor), the most common being T. nodulosus. Females with a marsupium were observed in the cold season in the case of some small-sized species that are present in the immediate vicinity of the shores of thermal waters (A. roseus, H. riparius and H. transsilvanicus). The high temperatures of the thermal waters warm the surrounding terrestrial environment, affecting the life cycle of the terrestrial isopods.


INTRODUCTION
Terrestrial isopods hibernate during the winter in temperate areas (Gupta, 1963), a situation also valid in Romania (Radu andTomescu, 1981, Tomescu et al., 1995).Thus, their life cycle implies the alternation of a hibernation period and a period of activity.However, there are some indirect clues concerning a continuation of activity over winter of terrestrial isopods near the thermal waters from western Romania.And while it is expected that terrestrial isopods hibernate in the cold periods, amphibians have been found that consume them during the winter (Covaciu-Marcov et al., 2006, Bogdan et al., 2012).Recently, active amphibians were recorded during the winter in the thermal waters of western Romania (Covaciu-Marcov et al., 2006, 2010, 2011, Sas et al., 2007, 2012, Bogdan et al., 2011).This observation raises the hypothesis that terrestrial organisms living on the warm shores of the thermal waters, such as terrestrial isopods, also remain active in the winter.The fact that active amphibians from thermal waters consumed terrestrial isopods suggests that these were also active in winter.Consequently, we studied whether terrestrial isopods from the thermal habitats of western Romania remain active in the cold season, in order to observe the possible modifications of their biology and ecology induced by the conditions from these habitats.

MATERIALS AND METHODS
The field study was realized between December and February of two consecutive winters (2010/2011 and 2011/2012).The terrestrial isopods were captured by hand from under different natural (rocks, logs) or artificial (domestic waste) shelters, as well as from under the grassy vegetation and from the soil surface.The species were determined in the laboratory, according to Radu (1983Radu ( , 1985)), and the current nomenclature (Schmalfuss, 2003).Overall, we investigated 58 thermal habitats from western Romania.Most of them are artificial, but there are also natural ones, such as the thermal lake of 1 Mai Spa and the thermal springs of Călan Spa (Table 1).Thermal canals originating from drill holes or swimming pools represent the artificial habitats, as in the case of winter active amphibians (e.g.Bogdan et al., 2011, Covaciu-Marcov et al., 2006, 2010, 2011, Sas et al., 2012).These canals are linear, with usually abrupt shores, the water level being lower than their margins.Most thermal habitats are surrounded by degraded surfaces, covered only with grassy vegetation.Răbăgani, Bobâlna and Moneasa are the only thermal habitats linked to forests.

RESULTS
Winter active terrestrial isopods were present in 35 of the 58 investigated thermal habitats (Table 1).Terrestrial isopods populate the areas near water, where the soil does not freeze.The length of the warm shore varies according to the habitat type and the volume or temperature of the thermal water.There are thermal habitats with water temperatures of 70ºC, which warm a long length of the canal and a wide surface of the shore.In the habitats in which terrestrial isopods are not active during winter, the shores are without shelters, vegetation, and are often directly exposed to cold air, which causes freezing in close proximity to the water.There are also habitats in which the flow or water temperatures are too low to sufficiently warm the shore.
We identified 12 terrestrial isopod species that were active in winter (Hyloniscus transsilvanicus, H. riparius, Haplophthalmus danicus, Trichoniscus sp., Androniscus roseus, Cylisticus convexus, Protracheoniscus politus, Trachelipus nodulosus, T. rathkii, Porcellio dilatatus, Armadillidium vulgare, A. versicolor).The highest number of species was recorded in the larger, relatively natural habitats, which are also the oldest, such as the Călan Spa and Răbăgani (Table 1).We identified 313 terrestrial isopod individuals of which 161 were females, 89 were males and 63 were juveniles.The most common species during the winter in the areas neighboring the thermal waters was T. nodulosus.This species was also the most frequent in the habitats (Table 2).
Together with the disappearance of hibernation, some isopod species from certain habitats also present a modification of the reproductive period induced by the thermal regime.Females with marsupium with eggs were identified in February at 1 Mai Spa, Călan Spa and Tărian.The modification of the reproductive period was observed in three species: A. roseus, H. riparius and H. transsilvanicus.This phenomenon was observed in 14 females, of which 10 belonged to the species H. riparius (observed at 1 Mai Spa and Tarian), three to H. transsilvanicus and one to A. roseus (observed at Calan Spa).

DISCUSSION
Regardless of the air temperature, terrestrial isopods remain active throughout the entire winter period.They behave normally, trying to shelter when surprised.T. nodulosus frequently hides under domestic waste (cardboard, old rags etc.), which is present near the thermal waters.The finding of isopods that are active during winter confirms the fact that temperature triggers hibernation, as in the case of the amphibians from thermal waters (e.g.Covaciu-Marcov et al., 2006, 2011).The winter-active terrestrial isopods occupy an area of variable width on the shores of the thermal water.Species connected to humid areas, such as H. riparius and H. transsilvanicus (Radu, 1983, Tomescu et al., 2005), are found close to the water.Species related to drier areas, like T. nodulosus and A. vulgare, are found at a certain distance from the water, even as far as areas with frozen soil.However, T. nodulosus, a xerophilous species (Farkas, 2010) is the most common in the thermal habitats.
Modification of the reproductive period has been observed in three isopod species from three thermal habitats.We encountered H. riparius and H. transsilvanicus females with marsupium at the beginning of February, in conditions in which H. riparius reproduces between May and July (Tomescu et al., 2002) and H. transsilvanicus between May and August (Tomescu, 1976).However, it cannot be stated that isopods have a continuous reproduction, as do some frogs from the thermal waters (Covaciu- Marcov et al., 2006), or that an additional or an early reproduction occurs, as we did not monitor these populations throughout the whole year.In the case of Răbăgani (BH) Thermal lake X X X X X 5 Săcuieni I (BH) Inundate grassy area X X X 3 Călan -small basin (HD) Old abandoned swimming pools X X X X 4 Călan -roman spoon (HD) X X 2 an Amphipod species from Iceland, the influence of thermal water determined the start of the breeding season, bringing it 2-3 months forward (Ingólfsson et al., 2007).This could be the situation in terrestrial isopods from the northwestern Romania's thermal habitats, which breed approximately 3 months earlier than normally.Isopods from temperate areas have a seasonal reproduction, displayed during the summer in a relatively short interval (e.g.Tomescu, 1972, Tomescu et al., 1992).However, there are species that have a continuous reproduction in tropical areas (Dangerfield and Telford, 1990).In the case of terrestrial isopod species, temperature is considered to be a factor determining the periodicity of reproduction (McQueen, 1976), warmer conditions determining earlier breeding (Hornung and Warburg, 1993).Reproduction is energetically costly for terrestrial isopod females; the presence of the marsupium reduces the females' mobility and exposes them to predators (Lardies et al., 2004).However, to remain active during winter is a reproductive advantage as some predators are absent and food is sufficient.Because terrestrial isopods are detritivores (Hassall et al., 1987), they can normally feed during the winter, thus remaining active does not disadvantage them.
The terrestrial isopods that reproduce in winter belong to small-sized species connected to moist ar-eas.Being present close to the water, they are little influenced by air temperature.Therefore, they are most susceptible to the appearance of modifications in the reproduction biology.Two of the three habitats with isopods that reproduce during winter are natural and old habitats (1 Mai Spa and Călan Spa).In these habitats, continuous reproduction has also been recorded in amphibians (e.g.Covaciu-Marcov et al., 2006, Sas et al., 2010).
The low number of isopod species from most thermal habitats is probably a consequence of anthropogenic disturbance.Near the majority of the thermal canals, there are only degraded terrains.The species connected to moist areas appear only in less affected habitats where there are wet areas with vegetation on the shores.Other species, such as P. politus, are rare in the thermal habitats, because the habitats that correspond to them are also rare.This is a sylvan species (Tomescu et al., 2011), and was encountered only at Răbăgani, a habitat surrounded by an oak forest.
Beside the ecological aspects, our results have a faunistic importance.To our best knowledge, until now A. roseus was known in western Romania only from four localities (Radu, 1983, Ferenti et al., 2012a), now being encountered in another five.The species' presence in non-thermal habitats (Ferenti et al., 2012a) can indicate that they have a wider distribution range in western Romania.However, the relatively high frequency of A. roseus in thermal habitats can indicate a link between them.It is possible that this endogenous species (Radu, 1983) is advantaged by the warm soil near the thermal water.P. dilatatus was mentioned in the past in only one locality from the country (Radu, 1985).It seems that the species is connected to warmer, artificial areas, being previously observed in the botanic garden of Cluj-Napoca (Radu, 1985).Although it has been encountered in colder areas (Spuņgis, 2008), it appears to be a rare presence in the Pannonian Basin (Vilisics and Hornung, 2010).The presence of H. transsilvanicus at only 103 m altitude at Săcuieni seems unusual, as this species has been considered in the past to be characteristic for hills and mountains in Romania (Tomes-  , 2011).However, H. transsilvanicus was found on the plains of Hungary (Kontschán, 2003, Vilisics andHornung, 2010), and recently identified in northwestern Romania, in Carei Plain (Ferentti et al., 2012b).However, the presence of this species at Săcuieni, south of the Carei Plain, suggests that the low altitude populations have a larger distribution range in northwestern Romania.The presence of H. transsilvanicus in the lower areas of northwestern Romania and the neighboring sectors of Hungary is possible due to the existence of marshes, where other mountainous species also appear at low altitudes (Covaciu-Marcov et al., 2008, 2009).

Table 2 .
The number of the individuals (No.), relative abundance (A %) and frequency (f %) of the species