Ecology of an Anchialine Cave in the Adriatic Sea with Special Reference

Marine Ecology. ISSN 0173-9565

ORIGINAL ARTICLE Ecology of an anchialine cave in the Adriatic Sea with special reference to its thermal regime Maja Novosel1, Branko Jalzˇic´2, And-elko Novosel3, Mira Pasaric´4, Antonieta Pozˇar-Domac1 & Ivan Radic´1

1 Department of Biology, Faculty of Science, University of Zagreb, Zagreb, Croatia 2 Zoological Department & Croatian Biospeleological Society, Croatian Natural History Museum, Demetrova, Zagreb, Croatia 3 Nerej Diving Film Tourism Ltd, Vojnovic´eva, Kasˇina, Croatia 4 Andrija Mohorovicˇic´ Geophysical Institute, Faculty of Science, University of Zagreb, Zagreb, Croatia

Keywords Abstract Adriatic Sea; Anchialine cave; hexactinellids; Hvar Island; Oopsacas minuta; polychaetes; This study examines the ecology and thermal regime in the Zˇ iva Voda anchi- sea temperature. aline cave on Hvar Island (Adriatic Sea, Croatia). The cave, which has no direct connections with the open sea, contains a dense population of the deep- Correspondence sea hexactinellid sponge Oopsacas minuta Topsent, 1927. Several species of Maja Novosel, Department of Biology, Faculty polychaetes, molluscs and crustaceans were also recorded. Two-year tempera- of Science, University of Zagreb, Rooseveltov ture data recorded simultaneously at two depths within the cave and at a trg 6, 10000 Zagreb, Croatia. E-mail: [email protected] nearby outside site provide information on thermal conditions in the system. The temperature oscillations within the cave are strongly dampened – varying from 14.6 C in winter to 17.9 C in summer – the annual range being four times smaller than in the adjoining sea. These data suggest that O. minuta can withstand higher temperatures than previously expected from deep-sea or cold- water cave occurrences, and that other environmental factors must be playing an important role.

of the water body (Sket 1986, 2005). This paper focuses Problem on the ecology and thermal regime of the Zˇ iva Voda an- Anchialine habitats are coastal water bodies flooded with chialine cave on Hvar Island (Adriatic Sea, Croatia), par- seawater which fluctuates with the tides, and with no ticularly because this is only the eighth locality in the obvious connection to the sea. Stock et al. (1986) defined world where hexactinellid sponges (glass sponges) are so anchialine as bodies of haline waters, usually with a shallow that they can be reached by SCUBA diving (Leys restricted exposure to open air, always with more or less & Lauzon 1998; Jalzˇic´ et al. 2005; Bakran-Petricioli et al. extensive subterranean connections to the sea, and show- 2007). ing noticeable marine as well as terrestrial influences. Along the eastern Adriatic coast, a several anchialine caves Material and Methods have been recorded. Rad-a (2000) was the first to record the presence of the hexactinellid sponge Oopsacas minuta The Zˇ iva Voda anchialine cave is situated on the island of Topsent, 1927, normally known from the deep-sea, in the Hvar, on the border between the central and southern Zˇ iva Voda anchialine cave. Ozimec & Jalzˇic´ (2002) then Adriatic (Fig. 1). As this cave has no direct connections provided a description of the same cave, while Krsˇinic´ with the open sea, both speleological and SCUBA diving (2005) described Speleohvarella gamulini, a new genus methods were necessary for this study. Both the land and species of calanoid copepod from this cave. Most and underwater parts of the cave have been mapped by other studies on anchialine caves in the Adriatic Sea were standard topographical methods used in speleology conducted on the surface, i.e. freshwater or brackish parts (Fig. 2). The land part was mapped using a compass,

Marine Ecology 2007, 28 (Suppl. 1), 3–9 ª 2007 Blackwell Publishing Ltd No claim to original US government works 3 Ecology of an anchialine cave in the Adriatic Sea Novosel, Jalzˇic´, Novosel, Pasaric´, Pozˇar-Domac & Radic´

Sampling of benthic fauna inside Zˇ iva Voda cave was carried out on 11–12 April 2003 and 2–3 April 2005. Sampling was undertaken on the cave walls and on bottom rocks and sediment. Samples were taken individu- ally or by scraping from the walls, and were preserved in 70% ethyl alcohol. Temperature conditions within the cave and at a nearby open sea site were surveyed during 2 years using small Onset StowAway TidbiT data loggers ﬁxed on rocks. The data were measured from 12 April 2003 to 16 February 2005, with ±0.2 C accuracy, and a 30-min sampling interval. Three loggers were deployed at 12 and 24 m depths in the right channel of the cave and at 22 m depth in the nearby open sea (Fig. 1). The obtained 2-year time series of 30-min temperature values were ana- lysed together with corresponding smoothed time series, Fig. 1. The Eastern Adriatic Sea with a detailed map of the study formed respectively by 24-hour and 30-day moving aver- location (O ¼ Zˇ iva Voda cave). ages (e.g. Emery & Thomson 1998). In order to examine in more detail the seasonal temperature cycle, harmonic clinometer and measuring tape, while underwater parts analysis was performed by ﬁtting the smoothed time ser- were surveyed using the compass, the depth gauge and ies to a sum of an annual and semi-annual sine function the measured guideline. The open sea water surface level (e.g. Emery & Thomson 1998). The analysis of amplitudes and the water surface level in both cave lakes were and phases reveals the relationship between heating and measured using a geodetic level. cooling within the cave and in the nearby sea.

Fig. 2. Proﬁle and ground plan with sections of the Zˇ iva Voda cave.

4 Marine Ecology 2007, 28 (Suppl. 1), 3–9 ª 2007 Blackwell Publishing Ltd No claim to original US government works Novosel, Jalzˇic´, Novosel, Pasaric´, Pozˇar-Domac & Radic´ Ecology of an anchialine cave in the Adriatic Sea

Results

Geologic and hydrographic setting

Zˇ iva Voda cave is located on the E-SE slope of Kozja Cove, on the southern coast of the island of Hvar (Fig. 1). The cave entrance is 31 m above sea level. Morphologically, Zˇ iva Voda cave is a ramified system developed by corrosion and erosion following bedding planes within Upper Creta- ceous (Senonian) beds (Borovic´ et al. 1977). Cave channels clearly follow inclination of layers, from 45 to 50, and dip towards the S-SE. These layers are the southern part of an anticline whose axis extends along the island of Hvar in an E-W direction. Along Kozja Cove numerous breccias were observed, implying the presence of multiple transversal faults on the eastern part of the island (Fig. 2). The entrance passage is lens-shaped in profile and des- cends at an angle of 45 towards a large chamber and to the left (east) towards a narrower channel. The large cham- Fig. 3. Time series of water temperature, recorded with a 30-minute ber bends towards the west and has a small pool of sampling interval at two depths in Zˇ iva Voda cave (top) and at a nearby 1 · 1.5 m at its lowest point. Underwater, this right chan- open-sea location (bottom), between April 2003 and 16 February 2005. nel reaches a maximum depth of 38 m. In the left channel, temperatures varied from 12 C in winter to around after 30 m of dry passage, there is a 5 · 3 m pool with sub- 22 C in early autumn (Fig. 3). The abrupt warming of merged passage extending to a maximum depth of 26 m. seawater by more than 5 C within several days in early Both channels have a thick layer of mud on the floor. At the surface of both pools, there is a brackish layer approximately 3 m deep. The water surface in both lakes is on average 50 cm above sea level, probably due to the lagging capillary water exchange between the open sea and the cave as well as the constant input of freshwater into the cave. Although the limestone bedrock has a high secondary permeability, there is no (or only extremely weak) circulation between the left and right channels. The left channel contained no macrofauna, whose absence here may be due to the configuration of the cave – the left channel extends under the island, while the right channel trends towards the sea.

Temperature proﬁles Water temperatures within the right channel at 12 and 24 m depth were very steady, equalling 16.6 ± 1.0 and 16.3 ± 0.8 C, respectively. Winter values did not fall below 14.6 C, while maximum values at the same depths were 17.9 and 17.5 C, respectively, in late summer and early autumn (Fig. 3). During the warm part of the year the water column was weakly stratiﬁed – the temperature difference at the two depths never exceeded 2 C. On the daily time scale, the cave temperature was extremely stable (Fig. 4), all deviations being within the precision of the instrument. These temperature conditions are remarkably different Fig. 4. Departures of 30-min temperature values from corresponding from those in the nearby open sea, where (at 22 m depth) daily means.

Marine Ecology 2007, 28 (Suppl. 1), 3–9 ª 2007 Blackwell Publishing Ltd No claim to original US government works 5 Ecology of an anchialine cave in the Adriatic Sea Novosel, Jalzˇic´, Novosel, Pasaric´, Pozˇar-Domac & Radic´

September – which resulted in increased sea temperatures 24 m depth, while the minimum in the open sea occurs throughout autumn – was completely absent in the cave. earlier (19 February). Similarly, the maximum temperature Beyond this wide annual range in temperature, the open in the cave at 24 m (2 October) displays a 1-month lag sea exhibited pronounced short-period oscillations during compared with the peak at 12 m (9 September), but occurs the warm season. On occasions, the temperature changed almost simultaneously with the maximum at the same by more than 6 C within several hours (Fig. 4). Such depth in the open sea (12 October). oscillations are related to internal waves induced in the region of the thermocline and have been observed in Benthos features other parts of the Adriatic (Novosel et al. 2004). Seasonal temperature variations are represented by time The cave contained a dense population of the hexactinel- series of 30-day moving averages (Fig. 5). The ‘monthly’ lid sponge Oopsacas minuta Topsent, 1927 along the cave values of temperature in the cave formed a symmetric roof and vertical and overhanging walls (Fig. 6). Their annual oscillation. A sine function with a period of 1 year highest abundance was between 15 and 35 m depth, described 92–94% of the temperature variability in the cave where approximately 15 individuals grew per m2.At at 12–24 m depth, respectively. The seasonal cycle in the shallower depths (6–15 m) the abundance was 1–2 open sea, however, is much more asymmetric and is more individual s ⁄ m2, while deeper (35–37 m) the abundance adequately described (92%) by a sum of the annual and was low again (2–3 individual) s ⁄ m2. semi-annual harmonics. The amplitudes and phases of the The second most abundant organisms inside the cave harmonic constituents reveal the relationship between the were polychaetes. Three species of serpulid polychaetes seasonal temperature changes in the cave and in the open were found. Live specimens of Metavermilia multicristata sea. The temperature ranges in the cave (2.7 and 2.1 C) at (Philippi, 1844) and Semivermilia crenata (O.G. Costa, 12 and 24 m, respectively, are quite similar, but are signiﬁ- 1861) were identiﬁed. Metavermilia multicristata, observed cantly lower than the annual range in the nearby open sea growing on the cave walls, was the most numerous of the (8.1 C). The temperature minimum in the cave is reached three. The discovery of S. crenata in this cave represents in early March at 12 m, but only 1 month later (8 April) at the second record for the species in the Adriatic Sea. The third species, Protula sp. sensu (Bianchi 1981), was represented only by fragile, relatively large (12 mm in diameter) empty tubes. Tubes were collected from the cave wall and sediment on the bottom of the cave. Furthermore, skeletal remains of two bivalves, the mussel Pododesmus patelliformis (Linne´, 1761) and the shipworm Teredo navalis (Linne´, 1758), and of one decapod, the spider crab Herbs- tia condyliata (Fabricius, 1787), were found as well.

Discussion

Thermal conditions inside the Zˇ iva Voda cave The cave is characterized by a very stable water temperature of around 16.5 C (which is equal to mean annual air temperature at Hvar; Penzar et al. 2001), with all temperature variability being related to a small-amplitude, symmetric annual cycle. Such conditions reﬂect the fact that air and water within the cave are sheltered from direct solar radiation and mechanical perturbations by wind, and that there are noticeable water currents on a macroscopic scale. The water in the cave is very still with no visible motion. Therefore, a number of processes that control the distribution of temperature at sea are absent here. In general, seawater is heated by the absorption of Fig. 5. Time series of water temperature, smoothed with a 30-day solar radiation and by the conduction of sensible heat moving average (black line). Also shown are the ﬁtted annual har- from the atmosphere; it is cooled by back radiation, monic (grey full line) and the sum of an annual and semi-annual har- conduction of sensible heat to the atmosphere and by monic (grey dashed line).

6 Marine Ecology 2007, 28 (Suppl. 1), 3–9 ª 2007 Blackwell Publishing Ltd No claim to original US government works Novosel, Jalzˇic´, Novosel, Pasaric´, Pozˇar-Domac & Radic´ Ecology of an anchialine cave in the Adriatic Sea

Fig. 6. Hexactinellid Oopsacas minuta on a wall in the Zˇ iva Voda cave. evaporation. This exchange is limited to a very thin surface after a long heating season, usually the gusty NE Bora layer. Heat is transported to deeper layers by small-scale wind, when intense mechanical mixing drives warm sur- turbulent eddies (i.e. eddy diffusivity) – the process being face water to deeper layers. However, the fact that this several orders of magnitude stronger than molecular dif- long-lasting temperature increase is not registered in the fusion – by horizontal and vertical fluid flow, and by cave leads us to speculate on how the cave is connected wind-induced mechanical mixing (Bowden 1983). In the to the open sea. There are two possibilities: either the Zˇ iva Voda cave, however, heating, cooling and the trans- connection is at a much greater depth where wind mixing port of heat are all greatly diminished. First, only the plays no role, or, more likely, the seawater penetrates the scattered part of solar radiation is available for absorp- cave very slowly, through a system of small crevices, fil- tion. Secondly, evaporation and sensible heat flux strongly tering out all variability at time scales shorter than several depend on wind velocity and thus are also significantly months. In any case, the aquatic system within the cave is reduced. Thirdly, in the absence of turbulent motion, the apparently very isolated from the nearby sea. Note also diffusion of heat across the air/sea interface and within that, if this is the case, the convective overturning set up the water is restricted to molecular motion, with molecu- by autumn cooling could be the most important process lar diffusivity being several orders of magnitude smaller for renewing oxygen in the deeper layers of the cave. than eddy diffusivity (Bowden 1983). During summer, heat slowly diffuses to deeper layers. However, during Benthos winter cooling, a layer of denser water is formed at the top and starts to sink, setting up thermal convective cur- Anchialine taxa include organisms with widely disjunct dis- rents. This asymmetry in heating/cooling is readily tributions and some with affinities to bathyal species (Iliffe observed in our data in spring as a 2-month lag between 1992). Anchialine stygobites are almost exclusively of mar- temperatures at the two depths, and in autumn as an ine origin and consist primarily of crustaceans. The reason almost simultaneous temperature drop (Fig. 3). why crustaceans make up 80–90% of anchialine stygobites The most pronounced feature observed in our series of is not clear. Perhaps they can better adapt to such limiting open sea temperatures is the abrupt warming in early factors in the anchialine environment as lack of light, low September. This reflects the first episode of strong wind levels of dissolved oxygen, and limited food supply. Only

Marine Ecology 2007, 28 (Suppl. 1), 3–9 ª 2007 Blackwell Publishing Ltd No claim to original US government works 7 Ecology of an anchialine cave in the Adriatic Sea Novosel, Jalzˇic´, Novosel, Pasaric´, Pozˇar-Domac & Radic´ four strictly anchialine species of sponges and 10 species of species were found near shallow-water hydrothermal vents annelids have been recorded so far (Iliffe 2005). in the Aegean Sea (Bianchi & Morri 2000). Protula sp. (sensu Hexactinellid sponges typically live in deep oceans (500– Bianchi) has a worldwide distribution. It is common in the 3000 m) world wide. Exceptionally, they have been found coralligenous biocoenosis, Posidonia oceanica meadows, and at such shallow depths that they can be reached by SCUBA the biocoenosis of coastal detritic bottoms, but also in mar- diving. These eight places in the world include: two sub- ine caves and in the bathyal down to 900 m (Bianchi 1981). marine caves off southern France, three island caves in the Only the skeletal remains of two bivalves and one deca- Adriatic Sea, along the coast of British Columbia and pod species were found inside the cave. One left valve of Alaska, in Antarctica and southern New Zealand (Leys & the mussel Pododesmus patelliformis was found in the Lauzon 1998; Jalzˇic´ et al. 2005; Bakran-Petricioli et al. examined material. Pododesmus patelliformis is a relatively 2007). Based on the assumption that propagules of O. mi- rare species with wide distribution found attached on dif- nuta have a short planktonic life-span, Bakran-Petricioli ferent hard substrata. It was reported to a depth of 1400 m et al. (2007) hypothesize that suitable ‘stepping-stone’ hab- and has an Atlantic–Mediterranean distribution (Parenzan itats (still to be located) exist between the southern Adriatic 1974). The skeletal remains of several valves and numerous deep basin and the distant colonized island caves. tubes found on the muddy bottom recorded the presence Oopsacas minuta is the only hexactinellid from which of the bivalve shipworm Teredo navalis. The decapod spider live larvae have been observed thanks to its occurrence in crab Herbstia condyliata was identified based on one cara- shallow-water caves (Boury-Esnault & Vacelet 1994). pace. This species is generally found in dark places, almost Although it reproduces throughout the year, not much is exclusively in the innermost parts of caves, where it is active known about its recruitment or population dynamics even during the day. Herbstia condyliata is distributed because of the difficulties encountered in accessing its cave along the eastern coast of the Atlantic and throughout the habitat (Boury-Esnault et al. 1999). The feeding strategy Mediterranean (Tu¨rkay 2001). of hexactinellids differs notably from that of other spon- As Humphreys et al. (1999) demonstrated, conven- ges. These sponges rely on the great volume of their aqui- tional open circuit diving methods significantly influence ferous cavities coupled with an extreme thinness of the environmental conditions in anchialine habitats. Exhalent living tissue. Furthermore, anucleate choanocytes of the bubbles from conventional SCUBA disrupt the physico- hexactinellid are mostly used to circulate water and do not chemical environment and destroy the fragile anchialine trap and digest particles, unlike other groups of sponges fauna. Individuals of O. minuta are weakly attached to such as Demospongiae and Calcarea (Vacelet 1996). substrata. Therefore, conventional SCUBA divers dislodge Until now, O. minuta – also known from the deep sea many individuals from the cave roof with their air bub- (Vacelet 1996; Bakran-Petricioli et al. 2007) – was found in bles. Even a careless diver’s fin thrust can easily detach environments where the sea temperature is always colder them from their substrata. Consequently, for future than that recorded in Zˇ iva Voda cave. Vacelet (1996) exploration of Zˇ iva Voda and all other anchialine caves, reported temperatures between 13.0 and 14.7 Cin‘3PP only rebreathers should be used. cave’ on the French coast. The temperature in Zˇ iva Voda cave ranges from 14.6 C in winter to 17.9 C in summer, Summary which is significantly higher than the 13 C homothermy of the deep Mediterranean. O. minuta therefore apparently Temperature conditions within the Zˇ iva Voda anchialine withstands dampened seasonal temperature fluctuations in cave and at a nearby open sea site were surveyed during still water and completely dark environments. 2 years, from 12 April 2003 to 16 February 2005, at a 30- None of the polychaete species found in Zˇ iva Voda cave min sampling interval. Water temperatures within the 12 are strictly anchialine: all have been reported either in the and 24 m depth were very steady, equalling 16.6 ± 1.0 and bathyal zone, in marine caves or sites with reduced salinity, 16.3 ± 0.8 C, respectively. Winter values never fell below and have an Atlantic–Mediterranean or cosmopolitan distri- 14.6 C, while maximum values at the same depths bution. Serpulid polychaetes dominate the cave in terms of were 17.9 and 17.5 C, respectively, in late summer and species diversity. Metavermilia multicristata is common in early autumn. Inside the cave, a dense population of the the bathyal zone and one of the most abundant serpulid ‘deep-sea’ hexactinellid sponge Oopsacas minuta was worms at depths down to 1000 m (Bianchi 1981). This spe- found. Their highest abundance was between 15 and 35 m cies was also reported to settle in some marine caves subjec- depth, where approximately 15 individuals grew per m2. ted to freshwater input (Zibrowius 1968). Semivermilia The second most abundant organisms observed inside the crenata is common in the bathyal and in the dark parts of cave were polychaetes. The aquatic system within the cave submarine caves. It is rare on infralittoral and circalittoral is very isolated from the nearby sea. Until now, O. minuta concretions and on detritic bottoms (Bianchi 1981). Both has been found in environments where the sea tempera-

8 Marine Ecology 2007, 28 (Suppl. 1), 3–9 ª 2007 Blackwell Publishing Ltd No claim to original US government works Novosel, Jalzˇic´, Novosel, Pasaric´, Pozˇar-Domac & Radic´ Ecology of an anchialine cave in the Adriatic Sea ture is always colder than that recorded in Zˇ iva Voda cave. Range, Western Australia. Journal of the Royal Society of Oopsacas minuta, therefore, withstands dampened seasonal Western Australia, 82, 88–108. temperature fluctuations in still water and complete dark- Iliffe T.M. (1992) Anchialine cave biology. In: Camacho A.I. ness. As conventional SCUBA can destroy fragile individu- (Ed.), The Natural History of Biospeleology. Museo Nacional als of O. minuta, for future exploration of Zˇ iva Voda we de Ciencias Naturales, Madrid: 617–636. suggest that only rebreathers should be used. Iliffe T.M. (2005) Biodiversity in anchialine caves. In: Culver D.C., White W.B. (Eds), Encyclopedia of Caves. Elsevier Aca- demic Press, London: 24–30. Acknowledgements Jalzˇic´ B., Grubelic´ I., Jalzˇic´ V., Miculinic´ K., Radic´ I. (2005) New Natural History Research of Medvjedstrok daˇ spilja (The We wish to thank V. Jalzˇic´ and D. Lovretic´ for their help Bear Cave) on the Island of Losˇinj (Croatia). 40th European during the speleological and diving work. T. Sˇiletic´ Marine Biology Symposium, Vienna, Austria; August 21–25, assisted with the bivalve and B. Kljajo with the decapod 2005; Abstracts: 74–75. identification. We are very grateful to Dr Frank K. Krsˇinic´ F. (2005) Speleohvarella gamulini, gen. et sp. nov., a new McKinney and two anonymous reviewers for their useful copepod (Calanoida, Stephidae) from an anchialine cave in suggestions on the manuscript. The support of the Minis- the Adriatic Sea. Journal of Plankton Research, 27, 607–615. try of Science, Education and Sport of the Republic of Leys S.P., Lauzon N.R.J. 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