Hydrobiologia (2016) 782:11–22 DOI 10.1007/s10750-016-2714-x

MEDITERRANEAN TEMPORARY PONDS Review Paper

How to survive and persist in temporary freshwater? Adaptive traits of sponges (Porifera: Spongillida): A review

Renata Manconi . Roberto Pronzato

Received: 19 October 2015 / Revised: 27 January 2016 / Accepted: 5 February 2016 / Published online: 21 March 2016 Ó Springer International Publishing Switzerland 2016

Abstract Spongillida (Porifera) colonized tempo- transforming the mother sponge functional body into rary freshwater bodies at the global level. To enhance gemmules (gemmulation) and vice versa (regenera- colonization, survival, long-term persistence, and tion of the active sponge). During dormancy, the dispersal, most continental sponges display crypto- majority of these sponges are represented only by biosis as dormancy of resting bodies, i.e. asexual gemmules adhering to hard substrata, floating at the gemmules, 0.25–1 mm in diameter, containing stami- water surface, resting in the silty/sandy bottoms, or nal cells protected by a collagenous theca usually dispersing by flooding, animal carriers, and wind. A armed by siliceous skeletal spicules. High plasticity of double functional role is performed by clonal gem- body plan, physiology, life cycle, and reproductive mules to persist in situ and for dispersal in discontin- modes are the key adaptive strategies of these sponges. uous continental water both in time and space. The life cycle rhythm is characterized by the alterna- tion of vegetative (active sponges) and cryptobiotic Keywords Life history Á Cryptobiosis by dormancy Á phases (dormant clones of gemmules). Hibernation or Morphofunctional traits of resting stages Á Phenotypic aestivation occurs cyclically according to the species plasticity Á Clonal strategy and the environmental constraints of local hydro- graphic and climatic regimes. Ontogenetic constraints, e.g. chronic morphogenesis and clonal strategy by staminal cells, support a metamorphic process Introduction

Sponges are over 8500 species (Van Soest et al., 2015) Guest editors: Simonetta Bagella, Dani Boix, Rossella but species richness value is only 250 (ca. 3%) for Filigheddu, Ste´phanie Gasco´n, Annalena Cogoni / Mediterranean Temporary Ponds sponges inhabiting inland water that belong to the order Spongillida (previous suborder Spongillina R. Manconi (&) Manconi & Pronzato, 2002, 2011, 2015;Ca´rdenas Dipartimento di Scienze della Natura e del Territorio et al., 2012; Morrow & Ca´rdenas, 2015). This (DIPNET), Universita` di Sassari, Via Muroni 25, 07100 Sassari, Italy monophyletic group of sponges (Manconi & Pronzato, e-mail: [email protected] 2002, 2015; Erpenbeck & Wo¨rheide, 2007;Ca´rdenas et al., 2012; Morrow & Ca´rdenas, 2015) colonized R. Pronzato continental water not later than the Triassic from a Dipartimento di Scienze della Terra, dell’Ambiente e della Vita (DISTAV), Universita` di Genova, hypothetical marine Haplosclerida ancestor (Pronzato 16032 Genoa, Italy & Manconi, 1994a; Manconi & Pronzato, 2002, 2014). 123 12 Hydrobiologia (2016) 782:11–22

Spongillida are widespread in all continents, species are able to produce different gemmular excluding Antarctica, and several species, probable morphs in the same sponge to perform different roles species complexes, show wide geographic range from dispersal to persistence (Manconi & Pronzato, (Manconi & Pronzato, 2007, 2008, 2014). Several 2007, 2014). records focus on extremely stressing conditions, e.g. The present paper aims to analyse the life history and temporary water (permafrost) in circumpolar northern the life cycle of model species in contrasting, also regions, temporary water in hot deserts, small tempo- extreme, environmental conditions. In particular, the rary ponds in sub arid–arid conditions, and tropical main focus is on the adaptive strategies of life cycle both hydrographic basins characterized by flooding and in the long and short term. Inversion of the life cycle extreme water level variations (Manconi & Pronzato, rhythm, persistence and dispersal processes, gemmula- 2008, 2014). tion and dormancy, clonation, and meta-populations are The abundance of sponges varies widely from considered as the key strategies for the persistence of the region to region, and in some cases sponge populations sponge fauna in temporary water. Temporary water with are so flourishing and dense to strongly impact on occurrence of icing and drying are compared versus human health or/and productive activities. In the perennial water in order to understand adaptive strate- Amazon basin, siliceous spicules of sponges are so gies for survival and persistence. abundant in the water column during the raining season to determine permanent eye damage (Volkmer- Ribeiro et al., 2006). In the lower Mekong basin Freshwater sponges’ life cycle (Thailand), large sponges with high biomass amount heavily colonize fishermen nets, damaging fishery and The life cycle of Spongillida appears to be synchro- aquaculture (Manconi et al., 2013). On the contrary, nized with the local long- or short-term seasonal sponges are very rare in some Mediterranean islands rhythm of the hydroperiod. Only few taxa show a (Manconi & Pronzato, 1994a) or absent as in the perennial long-term life cycle (without gemmules) Canary Archipelago and in the western Indian Ocean displaying only the active vegetative filter-feeder archipelagos (Manconi, 2008; Manconi & Pronzato, phase encompassing sexual reproduction (e.g. 2009). Lubomirskiidae). This matches only some taxa in a The key adaptive structures determining fluctua- few perennial water bodies, e.g. large ancient lakes. tions of their colonizing success are asexual resistant On the other hand, in most hydrographical condi- bodies as small collagen spherules, i.e. the gemmules tions the life cycle of Porifera is annual with four containing totipotent staminal cells able to perform phases: active filter-feeding and sexually reproducing cryptobiosis. Gemmules are also present in a few sponge, metamorphosis by gemmulation, dormancy as marine sponges from marine shallow water (Fell, gemmule carpet, and hatching of gemmules with 1974; Simpson & Fell, 1974; Marra et al., 2013). regeneration of the active sponge (Fig. 1). Active In the evolutionary history of Spongillida, a sponges perform sexual reproduction by internal notable radiation of gemmular morphotrait occurred fertilization and planktonic parenchymellae larvae in inland water worldwide involving over 210 species (Fig. 1). The active phase matches the favourable belonging to three families, viz. Spongillidae, Metani- season, whereas dormancy the most adverse one. Of idae, and Potamolepidae (Manconi & Pronzato, 2007, course, the ‘‘adverse seasons’’ are opposite if we 2014). A wide array of gemmule architecture ranges consider for example northern Canada and Siberia from a very simple structure, e.g. thin theca of permafrost lands vs. Australian billabongs, Saharan compact spongin such as genus Nudospongilla Annan- wadi, Namibian pans, and the Mediterranean insular dale, 1918, up to the complex multilayered theca with area. As a consequence, the widespread species spiny spicules and pneumatic layer from chambered to Ephydatia fluviatilis (Linnaeus, 1759) displays a fibrous, e.g. many species of Metaniidae Volkmer- hibernation phase in the cold latitudes and an aesti- Ribeiro, 1968 and Spongillidae Gray, 1867. The vation phase in the warm ones within an apparent combination of these traits in the various gemmular cosmopolitan range (Manconi & Pronzato, 1994b; morphs makes each species unique. Moreover, some Manconi, 2008).

123 Hydrobiologia (2016) 782:11–22 13

taxa display diverging life histories. Some species, such as Ephydatia fluviatilis with very large geo- graphic range, must face different climatic and hydrographic regimes (Pronzato & Manconi, 1991, 1994a, b; Pronzato et al., 1993; Corriero et al., 1994; Pronzato & Manconi, 1995; Manconi, 2008). Long-term studies, up to 5 years, were focused in particular on the Italian populations of E. fluviatilis considered as a model. Water bodies here considered as a model (Fig. 2) are widespread along a latitudinal cline from north to south of the Italian peninsula, from continental to insular water, from icing to drying, and flooding conditions, i.e. continental Liguria versus coastal Liguria vs. Sardinia Island vs. Sicily Island. (i) A torrent of North-Central Liguria (Torrente Scrivia) flowing North from the Apennines to the Po River basin with continental climate is characterized by perennial Fig. 1 Life cycle of gemmule-producing freshwater sponges hydroperiod, low winter temperatures, occasional icing, (Ephydatia fluviatilis). A Sexual life cycle. B Asexual life cycle. and with notable fluctuations in water level. (ii) A short a Active filter-feeder sponge; b planktonic larva parenchymella; stream of the East Ligurian Riviera (Rio San Francesco) c post-larval stage; d sponge degeneration and gemmulation; flowing from the Apennines to the Ligurian Sea is e carpet of cryptobiotic gemmules on the substrate; f gemmule architecture (cross section); and g gemmule hatching and characterized by perennial hydroperiod, temperate regeneration of active sponge climate, moderate air temperature fluctuations, and perennial hydroperiod with notable fluctuations in water From a different point of view, a carpet of dormant level. (iii) A short stream of North-West Sardinia (Rio gemmules can be considered a group of resistant Bunnari) flowing from the Balzo Hill and tributary to the bodies, displaying cryptobiosis up to the new favour- Rio Mascari is characterized by perennial hydroperiod, able season, and at the same time also an asexual Mediterranean climate, fluctuations in temperature, and dispersal system able to clone several meta-popula- notable fluctuations in water level up from flooding to a tions, both in the same habitat and far away from their short dry phase in some tracts (ca. 1 month). (iv)A place of origin (Pronzato & Manconi, 1994a). On the temporary canal (Canale Tagliavia, North-West Sicily, contrary, the sexual production of the planktonic Bosco di Ficuzza Natural Reserve) is characterized by parenchymella larvae does not allow the dispersal and dominant lentic conditions, Mediterranean climate, and colonization in a discontinuous-fragmented environ- notable fluctuations in water level with relatively long ment (Fig. 1). In this scenario, asexual reproductive dry phase (3–4 months) (Fig. 2). mode by resting bodies matches an r strategy, while The populations of E. fluviatilis inhabiting these sexual mode matches a K strategy. Continental four water bodies display a notable plasticity in sponges can utilize both these strategies, simultane- phenology along the latitudinal gradient with different ously or in alternative. timing of life cycle phases. A long period of winter dormancy with only carpets of gemmules on the substrate, lasting from mid- Aestivant versus hibernant sponge populations November to the end of June, characterizes the northern and life cycle inversion population of Scrivia. Gemmule hatching occurs in July and the active sponges feed, grow, and sexually Various biogeographic patterns characterize Spongill- reproduce during the next 3 months, up to the end of ida at species, genus, and family level according to October. Gemmulation is very fast and, during the first their natural history. Climates offer worldwide con- half of November, active sponges are completely trasting challenges to sponges’ survival and different transformed in overwintering gemmule (Fig. 2).

123 14 Hydrobiologia (2016) 782:11–22

123 Hydrobiologia (2016) 782:11–22 15 b Fig. 2 Ephydatia fluviatilis. Life cycle inversion is shown rainfall in the Ligurian Riviera (San Francesco), and along a north–south climatic cline in four model sites (white dots 15.8°C MAAT and 651 mm of rainfall in the south- on the background geographic map) of continental and insular Italy (North Liguria vs. coastal Liguria vs. Sardinia Island vs. westernmost site (Bunnari). Sicily Island). Seasonal phases of the life cycle around the year (clockwise pie charts) are indicated for Scrivia, San Francesco, Bunnari, and Tagliavia water courses. Dark grey = dormancy Long-term drying phase (carpet of gemmules). Light grey = gemmulation phase and hatching phase (coexistence of dormant gemmules and active sponges). White = active sponge phase (filter-feeding Among the model sites of temperate climate, the only and sexually reproducing specimens). Climate diagram with air one characterized by temporary water is Tagliavia temperature and rainfall (right) with a hydroperiod of up to 7 months between inundation and desiccation. Here gemmules stay in the dry phase for up to 5 months during the long-term A contrasting behaviour is displayed by the San south Mediterranean summertime, exposed to UV Francesco population. Sponges are active around the radiation and desiccation (MAAT of dry period ca. 25 year producing gemmules during the entire annual to over 45°C). cycle with a variable percentage of specimens from As for sponges inhabiting the shallow water 3% in winter to 30% in summer. As a consequence, temporary ponds of Mediterranean islands, we recently gemmules are present all around the year. A total confirmed (data unpublished), nearly 40 years after the dormancy of the population does not occur and first record, the long-term persistence of sponge gemmule production in this condition can be consid- populations inhabiting the temporary ponds (paulis) ered a strategy to face potential stressing conditions. of the Giara di Gesturi basaltic highland (ca. 550 m asl, This behaviour is in contrast with the classic phases of South-central Sardinia). Ephydatia fluviatilis the life cycle rhythm: active sponge, sexual reproduc- (Spongillidae) was reported in both summer and winter tion, gemmulation, dormancy, hatching, and regener- (1978) by Margaf & Maas (1982) in the microhabitat ation of active sponge (Fig. 2). represented by the lower surface of boulders scattered The life cycle rhythm inversion is evident when in paulis at water depth ranging from few centimetres comparing the aestivant Sardinian population versus to 1 m. These populations are capable to adapt their life the hibernant Scrivia population. Dormancy, exclu- style and physiological rhythms to ephemeral notably sively as gemmule carpets, occurs in the former site fragmented-discontinuous habitats of small size in a (August–September) according to very low water meso-Mediterranean climate with a hydroperiod of level (a few cm of depth). Gemmule hatching is 7–8 months and dry period lasting from mid-May to completed in October and the population is active for a late September. Air temperature ranges from 32.7°C successive long hydroperiod of 8.5 months, from (July–August) to 4.6°C (February) with rare snowfall autumn to the early summer, up to mid-July. Gem- on the plateau, and an annual rainfall of ca. 750 mm mulation is completed during the second half of July (winter maxima ca. 100 mm/month; summer minima (Fig. 2). ca. 10–15 mm/month). Despite contrasting microcli- The southern Sicilian population is aestivating too matic conditions among model water bodies, the but the dormancy, as dehydrated gemmule carpets, circum-Mediterranean climate is almost classified as lasts a longer period of 4 months (July–October). CSU (hot-summer Mediterranean climate) or Cf Hatching occurs in November. Active phase is short (maritime oceanic climate) in the Koppel climate (December–April). Gemmulation occurs in May classification (Peel et al., 2007). As a consequence, (Fig. 2). these conditions cannot be considered extreme but, Climate differences are conspicuous along the nonetheless, their variations constrain the sponges’ latitudinal cline. At the southernmost site (Sicily), physiological rhythm year round up to the inversion of the mean annual air temperature (MAAT) is 18.4°C life cycle phases inhabiting different geographic areas. and 606 mm of rainfall, whereas the northernmost site But freshwater sponges are able to live also in hot (Scrivia) shows 11.7°C MAAT and 1088 mm of desert climate (BWh). Ephemeral water bodies in rainfall. The in-between sites show intermediate strictly arid conditions harbour sponges in extremely conditions, i.e. 14.5°C MAAT and 1002 mm of isolated areas of the Sahara and the Kalahari–Namib 123 16 Hydrobiologia (2016) 782:11–22

Desert (e.g. Nama Pan and Etosha Pan) (Manconi, 2008; Manconi & Pronzato, 2009). In the Algerian Sahara, sponges inhabit small, isolated, extremely harsh freshwater bodies of Tassili N’Ajjer (Tuzet, 1953; Manconi & Pronzato, 2009) where rainfalls are less than 100 mm/year, and air temperature over- comes 40°C for almost four months during summer. As for sponge life cycle in the wet tropics, a contrasting seasonal dormancy was reported by Annan- dale (1911) in the western Deccan (Mumbai area, Western India) for Corvospongilla lapidosa (Annan- dale, 1908) and Stratospongilla bombayensis (Carter, 1882). The two species display a contrasting life cycle rhythm although sharing the same growth form in the same microhabitat (lower surface of stones). C. lapidosa was in full vegetative phase in November (beginning of ‘cold weather’, the coolest and driest season of the year). At the same time and space, S. bombayensis was in the dormant phase with body represented exclusively by a Fig. 3 a Arboreal sponges (red circles) dry on the branches of mass of gemmules capable to hatch and display a rainforest canopy along the Rio Negro (Brazil) during the dry flourishing active phase only during the ‘rains’. season. b Closeup of a specimen (box, detail of a) (Clint Robertson courtesy) On the other hand, the life cycle of other species from West India, i.e. Eunapius carteri (Bowerbank, 1863), Radiospongilla cerebellata (Bowerbank, Effectively, these enormous and spectacular floods 1863), and Dosilia plumosa (Carter, 1849), is con- are a model of special ‘‘temporary water’’ that, when strained by the monsoon climate in a small temporary retired, leave sponges dry for a long term with hot pond (Pune, West India) with hydroperiod from late lapse (4–6 months at ca. 30°C). It is possible to June–early July till late March when most of the area hypothesize that this apparently non-sense situation dries up (Kulkarni et al., 2015). could be favourable for successful species dispersal In the Neotropical Region, the particularly unex- and increase of population abundance. Drulia and pected phenomenon of ‘‘arboreal sponges’’ (Fig. 3)was Metania are massive, gemmule-producing, species reported (Archibold, 1995) during extremely dry con- with a stout and robust multi-spicular fibrous skeletal dition in the Rio Negro River (Brazilian Amazonia) and network. Gemmules, trapped in the sponge skeleton in the Gran Pantanal (Paraguay Basin). The Igapo` meshes, have no many chances to be released and tropical rainforest surrounding rivers is partially sub- spread around in a perennial water submersion. On the merged with a hydroperiod of 6–8 months during the contrary, arboreal sponge specimens (Fig. 3) could be raining season. The maximum rainfall level is from advantaged. For example, the Drulia species normally March to April, exceeding 200 mm/month. On the settle on submerged vegetable substrata (Fig. 4), and contrary, from July to December virtually no rain occurs as a consequence it is not an extraordinary event to lower than 20 mm/month. During the wet period, some settle on temporary submerged fronds of the arboreal species belonging to the genera Drulia Gray, 1867 and canopy. The gemmules of these species are scattered Metania Gray, 1867 are able to settle on the submerged in the skeletal network just under the sponge surface tree branches (Fig. 3) just under the maximum water (Fig. 4) protected by a loose cage of spicules. Under level. As for the systematics of the latter genera although dry conditions, gemmules can be dispersed by wind, recently Drulia was proposed as junior synonym of flying insects, or birds. A potential periodically Metania (Castello-Branco et al., 2015), we disagree occurring of unfavourable stressing condition acts as with this decision on the basis of key diagnostic traits of a promoter of species dispersal opportunity. The the gemmular architecture and its spicular armature (see widely fluctuating water level, speed, and turbulence Manconi et al., 2015). in the cyclic alternation of the rainy and dry seasons in 123 Hydrobiologia (2016) 782:11–22 17

Fig. 4 Drulia cf. browni. a Dry specimen settled on the branch cage armed by a few spicules encasing the gemmular theca of a tree; b sponge surface showing the superficial, light (SEM); and d three gemmules within skeletal ectosomal meshes coloured, rounded gemmules (close up of a); c fragile spicular (SEM closeup of b) the tropical and equatorial area seem to favour the match this definition. The nickname ‘‘white desert’’ of presence of sponges. Ultimately, dry condition is Antarctica is due to the absence of the liquid phase of tolerable for several freshwater sponges. water; in fact, none of the freshwater sponge species This is true also in cold-temperate climates of the were found until now on this continent. On the Nearctic and North-Western Palaearctic regions where contrary, its submerged coast hosts a very rich marine Spongilla lacustris (Linnaeus, 1759) produces two sponge fauna under the ice level (see Fig. 1 in morphs of resting bodies, i.e. gemmules with thin theca McClintock et al., 2005). and gemmule with thick theca (Simpson & Gilbert, Surprisingly at the North Polar Circle latitudes the 1973; Gilbert & Simpson, 1976; Frost et al., 1982; permafrost ponds of North Europe, Greenland, Simpson, 1984; Fell & Levasseur, 1991;Fell,1993;De Alaska, Northern Canada, and Siberia host a few Santo & Fell, 1996; Manconi & Desqueiroux-Faundez, pioneer sponge species (Annandale, 1915; Holmquist, 1999). The two morphs display different physiological 1973; Ricciardi & Reiswig, 1993; Økland & Økland, performances and functional roles in the same speci- 1996; Manconi & Pronzato, 2002; Reiswig et al., men. The yellow–green gemmular morph with thin 2010) which aberrant life cycle has a drastically theca produced in autumn is overwintering with a high reduced active phase and a drastically prolonged degree of cold hardiness and able to tolerate being dormancy hibernation. In some extreme cases, pop- frozen in ice down to -20°C, but are not desiccation ulations of Spongilla lacustris and Ephydatia muelleri tolerant (Fell & Levasseur, 1991). The brown gemmular (Lieberku¨hn, 1856) are reported over the 70th parallel morph with thick theca produced in midsummer is in the Tundra permafrost (Økland & Økland, 1996) desiccation tolerant able to survive severe drying for with winter air temperature constantly under -40°C. long term (De Santo & Fell, 1996). There are very few reports about this extreme adaptation to temporary water in cold climate, while Extreme icing the reverse situation, i.e. prolonged dry conditions, is quite common for sponge populations in temperate and If temporary water is generally considered those tropical latitudes. This indicates a notable capability of undergoing complete drying, also icing habitats may adaptation in warm-hot climates than in cold ones. 123 18 Hydrobiologia (2016) 782:11–22

Persistence, dispersal, and reproductive strategies contrary, sexual reproduction or gemmule dispersal within a single isolate habitat promotes local mutations, In general, gemmules play a double role of resistant bottlenecks, and genetic drift ending in possible and passive dispersal bodies. Most species belonging speciation events (Pronzato & Manconi, 1994a). to Spongillida produce gemmules of a single morph Contrary to what might be assumed freshwater mainly at the sponge basal portion (Fig. 1e) or less sponges are pre-adapted to live in temporary water. frequently also scattered in the meshes of the Indeed, less than 20% of the known Spongillida choanosomal fibrous skeleton (see Fig. 4). species does not produce gemmules. The absence of Continental water is an extremely fragmented- these key dispersal propagules automatically confines discontinuous environment, as a consequence the populations to restricted geographic areas and water widely distributed sponge species, e.g. Eunapius frag- bodies. This irreversible reduction of the potential ilis (Leidy, 1851) and Spongilla alba Carter, 1849, must geographic range has de facto turned them into face desiccation during dispersal by biological carriers endemic species. This is the case of the family and/or physical vectors, e.g. mammals and birds Lubomirskiidae (4 genera, 15 species) endemic to (zoochory), or wind (anemochory). The latter possibil- the Baikal Lake (Siberia) and of Ochridospongia ity is easier for aestivant populations subjected to rotunda Arndt, 1937 (Fig. 6), one of the four species desiccation of water bodies. Dry gemmules protect endemic to the Ohrid Lake (Macedonian–Albanian staminal cells by a pneumatic layer and can hook the fur border) (Manconi & Pronzato, 2002). or feathers of animals by means of their protruding If the Baikal sponge fauna seems well diversified spiny spicules (siliceous gemmuloscleres). The resting and, apparently, not exposed to risks, the Ohrid sponge gemmules can hatch at the rising of water level during fauna is highly threatened (Kostoski et al., 2010). The the raining season originating active sponges in situ. small dimensions of the water body, the dense human Two gemmular morphs in the same specimen settlement along its coasts, and fishery activities have (Manconi & Pronzato, 2004) with contrasting weight substantially reduced the population of the endemic O. (heavy vs. light), architecture (thin theca with a few rotunda that should be kept under strict control. In spicules vs. stout theca armed by abundant spicules), particular, these sponges were largely subjected to and topographic distribution within the massive intensive bycatch in fishing nets since long time sponge body (sessile heavy gemmules in basal carpet (Fig. 6) (Pronzato & Manconi, 2001). vs. free light gemmules in the skeletal network) are The majority of Spongillida species produce gem- typical of Corvospongilla mesopotamica (Manconi & mules. Almost all species produce very complex Pronzato, 2004). Summarizing, when the sponge gemmules with pneumatic layer armed by spiny habitat dry up, the mother sponge degenerates, the gemmuloscleres in the cosmopolitan family Spongill- sessile gemmular morph persists on the substratum, idae (Manconi & Pronzato, 2004) the most speciose of and the free morph is dispersed. In a second time, the order with 22 genera and 155 species (Fig. 7). The persistent gemmules regenerate a sponge in the same double role (persistence and dispersal) of gemmules is position, while the dispersed propagules colonize new the key to Spongillida evolutionary success in colo- substrata and/or new habitats (Fig. 5). nization and persistence of freshwater. Gemmules are able to carry the sponge populations through periods of harsh environmental conditions. A potential decline Conclusive remarks in taxonomic richness and diversity of freshwater sponges and their several associated organisms must From an evolutionary standpoint, ‘‘super-tramp’’ spe- be considered as a result of non-sustainable land-use cies of freshwater sponges that have an apparent activities (i.e. habitat modification/destruction, agri- cosmopolitan biogeographic pattern potentially benefit cultural/silvicultural methods, urban development, from the overland dispersal. The populations and meta- pollution/siltation, and aquifer overexploitation) not populations of a freshwater sponge species, dispersed in only in developing countries. a discontinuous habitat, can maintain inter-fertility only Conservation plans together with the red lists of through panmixis, redistributed randomly on large species exposed to risks does not include any species geographical scale by gemmule dispersal. On the of these not charismatic basal metazoans as well as 123 Hydrobiologia (2016) 782:11–22 19

Fig. 5 Persistence versus dispersal processes in the life cycle of strictly adhering to the substratum. c Degeneration of the mother Corvospongilla mesopotamica as a sponge model. Diverging sponge and dormancy with dispersal of free light gemmules. morphofunctional role of the two gemmular morph. a Active Sessile heavy gemmules persist on the substratum. d Hatching sponge. b Production by the active sponge of two gemmular of sessile heavy gemmules and in situ regeneration of the mother morphs as free light gemmules (black circles) in the skeletal sponge. Modified from Manconi & Pronzato (2004) meshwork versus sessile heavy gemmules (black triangles)

Fig. 6 Ochridaspongia rotunda endemic to the Ohrid Lake. specimens from the Ohrid Lake (historical photograph dating a Typical growth form of the species (local common name: back to the fifties, modified from Hadzische, 1953) Turkish cake); b Fishery bycatch by nets of a huge amount of

123 20 Hydrobiologia (2016) 782:11–22

Fig. 7 Morphotraits of gemmules (resting stages) of Spongill- with theca surface strongly armed by distal rotules of radial ida (SEM). a Spongilla lacustris, unarmed light gemmule with gemmuloscleres; f Stratospongilla bombayensis, hemispherical thin theca; b Metania reticulata, cage of tangential megascleres sessile gemmule with theca armed by tangential gemmuloscle- encasing the gemmule; c M. reticulata, ovoid gemmule res; g Radiospongilla crateriformis, gemmular theca with radial (removed from the cage, see b) with birotules gemmuloscleres gemmuloscleres (cross section, closeup of d); h Umborotula radially arranged in the theca; d Radiospongilla crateriformis, bogorensis, gemmule surface with distal rotules of gemmu- gemmular theca (cross section) with radially arranged pseudo- loscleres (closeup of e); i Oncosclera rousseleti, gemmule with birotules gemmuloscleres; e Umborotula bogorensis, gemmule tangential gemmuloscleres (detail of cross section) many species of other freshwater invertebrates and focusing on the poor knowledge of this fauna with 31 plants with rare exceptions, e.g. in Brazil. The threats species only known from the type locality and never could be particularly severe in water bodies scattered found again, out of 58 recorded species. Moreover, the in arid land. To protect and possibly increase abun- number of studies on African freshwater sponges from dance of Spongillida by biotechnology (i.e. sponge the seventies to today (45 years) are less than 15, culture in water enriched of organic matter) would without papers from 1980 to 1990 (Manconi & represent a sustainable approach to maintaining bio- Pronzato, 2009). diversity and improving the rational management of As for apparently well-known areas, i.e. Tennessee freshwater ecosystems and their natural resources (USA), recent investigation supported by international (Manconi & Pronzato, 2007, 2008, 2009, 2014). cooperation on taxonomic research resulted in the new A dramatic status of African inland sponges was finding of a Spongillida family never recorded before recently highlighted (Manconi & Pronzato, 2009) from the Nearctic Region, i.e. Potamolepidae with the 123 Hydrobiologia (2016) 782:11–22 21 new genus Cherokeesia Copeland, Pronzato & Manconi, Frost, T. M., G. S. Denagy & J. J. Gilbert, 1982. Population 2015 in the Appalachian area (Copeland et al., 2015). dynamics and standing biomass of the freshwater sponge, Spongilla lacustris. Ecology 63: 1203–1210. Unfortunately, freshwater sponges are a neglected Gilbert, J. J. & T. L. Simpson, 1976. Gemmule polymorphism in elitist field of study and the major risk of extinction is the freshwater sponge Spongilla lacustris. Archive fu¨r the extinction of experts in their taxonomy and natural Hydrobiologie 78: 268–277. history. Hadzische, S., 1953. Beitragzur Kenntnis der Spongillidenfauna der groben Mazedonischen Seen (Dojran-, Prespa- und Ohridsee). Recueil des Travaux Station Hydrobiologique Acknowledgements We thank the financial support by the Ohrid 3: 73–103. Regione Autonoma della Sardegna (RAS/L. 7-CRP-60215- Holmquist, C., 1973. Spongilla lacustris (L.) (Porifera) from 2012), the Fondazione Banco di Sardegna, INTERREG EU, and Northern Alaska and Northwestern Canada. Zoologische the Italian Ministero dell’Universita` e della Ricerca Scientifica e Anzeiger 191(5/6): 300-309. - Tecnologica (MIUR PRIN). Kostoski, G., C. Albrecht, S. Trajanovski & T. Wilke, 2010. A freshwater biodiversity hotspot under pressure – assessing threats and identifying conservation needs for ancient Lake References Ohrid. Biogeosciences 7: 3999–4015. Kulkarni, M. R., S. Padhye, A. I. Vanjare, S. S. Jakhalekar, Y. Annandale, N., 1911. Freshwater sponges, hydroids and poly- S. Shinde, S. V. Paripatyadar, S. D. Sheth, S. Kulkarni, S. zoa. Porifera. In Shipley A. E. (ed), Fauna of British India, K. Phuge, K. Bhakare, A. S. Kulkarni, K. Pai & H. Including Ceylon and Burma. Taylor & Francis, London: V. Ghate, 2015. Documenting the fauna of a small tem- 27–126, 241–245. porary pond from Pune, Maharashtra, India. Journal of Annandale, N., 1915. Description of a freshwater sponge from Threatened Taxa 7(6): 7196–7210. the N.W. of Siberia. Me´moires de l’Acade´mie Impe´rial des Manconi, R., 2008. The genus Ephydatia (Spongillina: Spongill- Sciences de St. Petersbourg 27: 1–3. idae) in Africa: a case of Mediterranean vs Southern Africa Archibold, O. W., 1995. Ecology of World Vegetation. Springer disjunct distribution. Biogeographia 29: 19–28. business media, Dordrecht. Manconi, R. & R. Desqueiroux-Faundez, 1999. Freshwater Ca´rdenas, P., T. Pe´rez & N. Boury-Esnault, 2012. Sponge sys- sponges (Porifera, Spongillidae) from the Lake of Geneva, tematics facing new challenges. Advances in Marine Switzerland. Revue Suisse de Zoologie 106: 539–553. Biology 61: 79–209. Manconi, R. & R. Pronzato, 1994a. Spongillids of Mediter- Castello-Branco, C., A. R. Calor & C. Menegola, 2015. ranean Islands. In Van Soest, R. W. M., Th M G Van Microscleres and gemmoscleres as phylogenetic signals in Kempen & J. C. Braekman (eds), Sponges in time and Spongillida: phylogeny and biogeography of the genus space. Balkema, Rotterdam: 333–340. Metania Gray, 1867 (Porifera, Metaniidae). Invertebrate Manconi, R. & R. Pronzato, 1994b. Conquiste evolutive e Systematics 29(4): 369–385. adattamenti dei Poriferi per la vita nelle acque interne. Copeland, J., R. Pronzato & R. Manconi, 2015. Discovery of Bollettino dei Musei e degli Istituti Biologici living Potamolepidae (Porifera: Spongillina) from Nearctic dell’Universita` di Genova 58–59: 77–96. freshwater with description of a new genus. Zootaxa Manconi, R. & R. Pronzato, 2002. Spongillina n. subord., 3957(1): 37–48. Lubomirskiidae, Malawispongiidae n. fam., Metaniidae, Corriero, G., R. Manconi, P. Vaccaro & R. Pronzato, 1994. Life Metschnikowiidae, Palaeospongillidae, Potamolepiidae, strategies of Ephydatia fluviatilis in two different envi- Spongillidae. In Hooper, J. N. A. & R. W. M. Van Soest ronments. In Van Soest R. W. M., Van Kempen Th. M. G. (eds), Systema Porifera: a Guide to the Classification of & J. C. Braekman (eds), Sponges in time and space. sponges, Vol. I. Kluwer Academic/Plenum Publishers, Balkema, Rotterdam: 321–326. New York: 921–1019. De Santo, E. M. & P. E. Fell, 1996. Distribution and ecology of Manconi, R. & R. Pronzato, 2004. The genus Corvospongilla freshwater sponges in Connecticut. Hydrobiologia 341: Annandale (Haplosclerida, Spongillina, Spongillidae) with 81–89. description of a new species from eastern Mesopotamia, Erpenbeck, D. & G. Wo¨rheide, 2007. On the molecular phy- Iraq. Archiv fu¨r Hydrobiologie, Supplement, Monographic logeny of sponges (Porifera). Zootaxa 1668: 107–126. Studies 151(1–2): 161–189. Fell, P. E., 1974. Diapause in the gemmule of the marine sponge Manconi, R. & R. Pronzato, 2007. Gemmules as a key structure Haliclona loosanoffi, with a note on the gemmule of Hal- for the adaptive radiation of freshwater sponges: A mor- iclona oculata. Biological Bulletin, Marine Biological pho–functional and biogeographical study. In Custo´dio, Laboratory, Woods Hole 147: 333–351. M. R., G. Loˆbo-Hajdu, E. Hajdu & M. Muricy (eds), Fell, P. E., 1993. In Adiyodi K. G. & R. G. Adiyodi (eds), Porifera Research: Biodiversity, Innovation, Sustain- Porifera. Reproductive Biology of Invertebrates VI, A, ability, Serie Livros 28. Museu Nacional, Rio de Janeiro: Asexual Propagation and Reproductive Strategies. Oxford 61–77. & IBH Publishing Co., New Delhi: 1–44. Manconi, R. & R. Pronzato, 2008. Global diversity of sponges Fell, P. E. & E. D. Levasseur, 1991. Cold hardiness of the green (Porifera: Spongillina) in freshwater. In Balian E. V., gemmules of Spongilla lacustris L. (Porifera: Spongilli- Le´veˆque C., Segers H. & K. Martens (eds), Freshwater dae). Hydrobiologia 218: 107–112. animal diversity assessment. Hydrobiologia 595: 27–33.

123 22 Hydrobiologia (2016) 782:11–22

Manconi, R., R. Pronzato, 2009. Atlas of African freshwater Pronzato, R. & R. Manconi, 1994a. Adaptive strategies of sponges. Studies in Afrotropical Zoology, Royal Museum sponges in inland waters. Bollettino di Zoologia 61(4): for Central Africa, Tervuren, vol. 295: 214 pp. 395–401. Manconi, R. & R. Pronzato, 2011. Suborder Spongillina Pronzato, R. & R. Manconi, 1994b. Life history of Ephydatia (freshwater sponges). In Pansini M., R. Manconi & R. fluviatilis: a model for adaptive strategies in discontinuous Pronzato (eds), Porifera I. Calcarea, Demospongiae (par- habitats. In van Soest R. W. M., van Kempen Th. M. G. & J. tim), Hexactinellida, Homoscleromorpha. Fauna d’Italia, C. Braekman (eds), Sponges in Time and Space. Balkema, vol. XLVI, Calderini-Il Sole24Ore, Bologna, 341–366. Rotterdam: 327–331. Manconi, R. & R. Pronzato, 2014. Chapter 8 Phylum Porifera. In Pronzato, R. & R. Manconi, 1995. Long–term dynamics of a fresh- Thorp J. & D. C. Rogers (eds), Ecology and General water sponge population. Freshwater Biology 33: 485–495. Biology: Thorp and Covich’s Freshwater Invertebrates. 4th Pronzato, R. & R. Manconi, 2001. Atlas of European freshwater Edition, Vol. I. Academic Press, Elzevier, London, sponges. Annali del Museo Civico di Storia Naturale di 133–157. Ferrara 4: 3–64. Manconi, R. & R. Pronzato, 2015. Chapter 3 Phylum Porifera. In Pronzato, R., R. Manconi & G. Corriero, 1993. Biorhythm and Thorp J. & D. C. Rogers (eds), Keys to Nearctic Fauna: environmental control in the life history of Ephydatia flu- Thorp and Covich’s Freshwater Invertebrates. 4th Edition, viatilis (Demospongiae, Spongillidae). Bollettino di Vol. II. Academic Press, Elzevier, San Diego, 39–83. Zoologia 60: 63–67. Manconi, R., N. Ruengsawang, V. Vannachak, C. Hanjavanit, Ricciardi, A. & H. M. Reiswig, 1993. Freshwater sponges (Por- N. Sangpradub & R. Pronzato, 2013. Biodiversity in South ifera, Spongillidae) of eastern Canada: taxonomy, distribu- East Asia: an overview of freshwater sponges (Porifera: tion, and ecology. Canadian Journal of Zoology 71: 665–682. Demospongiae: Spongillina). Journal of Limnology Reiswig, H.M., T.M. Frost & A. Ricciardi. 2010. In Porifera. 72(s2): 313–326. Thorp J. H. & A. P. Covich (eds), Ecology and Classifi- Manconi, R., B. Cadeddu & R. Pronzato, 2015. Adaptive mor- cation of North American Freshwater Invertebrates, vol. 4, pho-traits, taxonomy and biogeography of the genus Me- Elsevier Inc., New York: 91–123. tania Gray, 1867 (Porifera: Spongillina: Metaniidae) with Simpson, T. L., 1984. The Cell Biology of Sponges. Springer, the description of a new species from Madagascar. Zootaxa New York: 662. 3918(1): 39–56. Simpson, T. L. & J. J. Gilbert, 1973. Gemmulation, gemmule Margaf, J. & B. Maas, 1982. Zur Oko¨logie der temporaren hatching, and sexual reproduction in fresh-water sponges I. Su¨swasserflachsen des Tafelbergs ‘‘Giara di Gesturi’’ auf The life cycle of Spongilla lacustris and Tubella pennsyl- Sardinien. Spixiana 5: 69–99. vanica Transactions of the American Microscopical Soci- Marra, M. V., B. Cadeddu, S. Giacobbe & R. Manconi, 2013. ety 92: 422–433. Porifera of Lake Faro (Sicily): gemmules of a sponge Simpson, T. L. & P. E. Fell, 1974. Dormancy among the Por- epibiont on Mytilus galloprovincialis. Biologia Marina ifera: gemmule formation and germination in fresh–water Mediterranea 20(1): 140–141. and marine sponges. Transactions of the American McClintock, J. B., C. D. Amsler, B. J. Baker & R. W. M. Van Microscopical Society 93: 544–577. Soest, 2005. Ecology of Antarctic marine sponges: an Tuzet, O., 1953. Spongilla carteri Bow., subsp. saharensis. overview. Integrative and Comparative Biology 45(2): Eponge du Tassili des Ajjer. Mission scientifique Tassili 359–368. des Ajjer (1949). Institut de Recherches Saharienne, Morrow, C. & P. Ca´rdenas, 2015. Proposal for a revised clas- Universite` de Alger 1 (Recherches Zoologique et medi- sification of the Demospongiae (Porifera). Frontiers in cales): 49–59. Zoology 12: 7. VanSoest,R.W.M.,N.Boury–Esnault,J.N.A.Hooper,K.Ru¨t- Økland, K. A. & J. Økland, 1996. Freshwater sponges (Porifera: zler, N. J. de Voogd, B. Alvarez de Glasby, E. Hajdu, A. Spongillidae) of Norway: distribution and ecology. B. Pisera, R. Manconi, C. Schoenberg, D. Janussen, K. Hydrobiologia 330: 1–30. R. Tabachnick, M. Klautau, B. Picton, M. Kelly, J. Vacelet, M. Peel, M. C., B. L. Finlayson & T. A. McMahon, 2007. Updated Dohrmann, M. C. Dı´az, P. Ca´rdenas, 2015. World Porifera world map of the Ko¨ppen-Geiger climate classification. database. Accessed at http://www.marinespecies.org/porifera. Hydrology and Earth System Sciences 11: 1633–1644. Volkmer-Ribeiro, C., H. L. Lenzi, F. Ore´fice, M. Pelajo- Pronzato, R. & R. Manconi, 1991. Colonization, life cycle and Machado, L. M. de Alencar, C. F. Fonseca, T. C. A. Batista, competition in a freshwater sponge association. In Reitner, P. P. A. Manso, J. Coelho & M. Machado, 2006. Fresh- J. & H. Keup (eds), Fossil and Recent Sponges. Springer, water sponge spicules: a new agent of ocular pathology. Berlin: 432–443. Memo´rias do Instituto Oswaldo Cruz 101(8): 899–903.

123