Adaptive Traits of Sponges (Porifera: Spongillida): a Review
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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