How do freshwater organisms cross the “dry ocean”? A review on passive dispersal and colonization processes with a special focus on temporary ponds Giulia Incagnone, Federico Marrone, Rossella Barone, Lavinia Robba & Luigi Naselli-Flores Hydrobiologia The International Journal of Aquatic Sciences ISSN 0018-8158 Volume 750 Number 1 Hydrobiologia (2015) 750:103-123 DOI 10.1007/s10750-014-2110-3 1 23 Your article is protected by copyright and all rights are held exclusively by Springer International Publishing Switzerland. This e- offprint is for personal use only and shall not be self-archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. 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A review on passive dispersal and colonization processes with a special focus on temporary ponds Giulia Incagnone • Federico Marrone • Rossella Barone • Lavinia Robba • Luigi Naselli-Flores Received: 15 July 2014 / Revised: 28 October 2014 / Accepted: 2 November 2014 / Published online: 13 November 2014 Ó Springer International Publishing Switzerland 2014 Abstract Lakes and ponds are scattered on Earth’s special emphasis to temporary ponds, which represent surface as islands in the ocean. The organisms inhab- ‘‘isolated’’ ecosystems both in space and in time, and iting these ecosystems have thus developed strategies to are characterized by high levels of biological diversity. pass the barrier represented by the surrounding land, to The existence of a sharp decoupling between ‘‘dispersal disperse and to colonize new environments. The potential’’ and ‘‘actual establishment rates’’ is stressed, evidences of a high potential for passive long-range thus urging a definitive overcome of the so-called dispersal of organisms producing resting stages ‘‘Everything is Everywhere’’hypothesis in order to gain inspired the idea that there were no real barriers to a proper understanding of the biogeography and their actual dispersal, and that their distribution was ecology of inland water organisms. only limited by the ecological characteristics of the available habitats. The development of genetic tech- Keywords Dispersal vectors Á Biogeography Á niques allowed to criticize this view and revealed the Dispersal-gene flow paradox Á Priority effect Á existence of a more complex and diverse biological Monopolization hypothesis Á Cosmopolitanism scenario governed by an assortment of historical and paradigm ecological factors. In this paper, we review the literature related to the passive dispersal of organisms producing resting stages among inland lentic ecosystems, with Introduction To explain the biosphere concept, Vladimir Vernad- Guest editor: Koen Martens / Emerging Trends in Aquatic skij described the surface of our Planet as covered by a Ecology continuous layer of a multitude of (micro)organisms G. Incagnone Á R. Barone Á L. Robba Á (Vernadsky, 1998). Although he was mainly interested L. Naselli-Flores (&) in the processes that these organisms perform in Dipartimento di Scienze e Tecnologie Biologiche, shaping and moulding the Earth’s surface, one ques- Chimiche e Farmaceutiche – Sezione di Botanica ed tion may arise from this perspective: how do the Ecologia Vegetale, Universita` di Palermo, Palermo, Italy e-mail: [email protected] organisms distribute and colonize the entire Planet’s surface? Since the mid-eighteenth century, Biogeog- F. Marrone raphy has been studying the patterns of species Dipartimento di Scienze e Tecnologie Biologiche, distribution across geographical areas and through Chimiche e Farmaceutiche – Sezione di Biologia Animale ed Antropologia Biologica, Universita` di Palermo, geological time. However, even if well-established Palermo, Italy hypotheses on the distribution patterns of species on 123 Author's personal copy 104 Hydrobiologia (2015) 750:103–123 Fig. 1 Ephippia of cladocerans coating the stranded aquatic vegetation and the shores of Lake Iseo (Northern Italy) in early spring (photos by Federico Marrone) continents exist, it is more difficult to explain these A high potential for long-range passive dispersal of patterns on geographical or biological islands, espe- these organisms is supported by the very high cially on the most remote and isolated ones (Whittaker population sizes which microorganisms can attain & Ferna´ndez-Palacios, 2007). In this frame, inland (up to an order of magnitude of 109 l-1) and by the lentic water bodies can be considered a special case of ‘‘astronomical numbers’’ of resting stages (Foissner, ‘‘biological islands’’ scattered across the land masses 2006) produced by the larger ones (Fig. 1). This (Ripley & Simovich, 2009), and the distribution potential is also supported (i) by the very fast patterns of their biota, depending on dispersal abilities colonization of newly formed water bodies (see and colonization successes, are not fully clarified yet Maguire, 1963; Jenkins & Buikema, 1998; De Meester (Shurin et al., 2009). et al., 2002; Audet et al., 2013, and references therein) The organisms inhabiting inland water ecosystems and historically (ii) by the rapid recolonization of the have developed diverse active and passive strategies to faunally depleted central and northern regions of the pass the barrier represented by the surrounding land, northern hemisphere after the last Pleistocene glacial disperse and colonize new environments. The most event, which is genetically mirrored by the ‘‘southern effective strategy to achieve dispersal is the produc- richness vs. northern purity paradigm’’ of the Holarc- tion of resting stages. These (also called akinetes, tic biota (Hewitt, 2000; Marrone et al., 2010). cysts, ephippia, statoblasts, spores, seeds in different Such evidences for a long time inspired the idea that group of organisms) are dehydrated dormant stages of there were no real barriers to the dispersal of resting the cell or of the embryo that show no measurable stage producing aquatic organisms. Their distribution metabolism and are enveloped in a highly protective (i.e. the actual presence of a given taxon in a given cover (Wells et al., 1997; Dumont & Negrea, 2002). site) should therefore only be limited by the ecological Prokaryotes, unicellular eukaryotes, and small multi- characteristics of the available habitats themselves. cellular organisms less than 2 mm in length (micro- Accordingly, the differences observed in the biota organisms sensu Fontaneto & Brodie, 2011) have been could be explained by the selective pressures operated generally considered to have a cosmopolitan distribu- by the environment only (see Martiny et al., 2006). tion because of their minute sizes and their ability to This idea, known as the ‘‘Everything is Everywhere form resting stages which facilitate dispersal by wind (EiE) hypothesis’’, was already sustained by Darwin and migrating animals. In this review, the passive (1859), and then formally defined at the beginning of dispersal mechanisms of microorganisms and of larger the twentieth century; it can be efficaciously summa- ones (e.g. some calanoid copepods, large branchio- rized by the renowned statement of the Dutch micro- pods, stoneworts, mosses, quillworts, vascular plants) biologist L.G.M. Baas Becking: ‘‘Everything is producing resting stages in the same size range everywhere, but the environment selects’’ (see Wil- (100–600 lm) of microorganisms will be discussed. liams, 2011 for a review). 123 Author's personal copy Hydrobiologia (2015) 750:103–123 105 From a genetic perspective, according to the ‘‘EiE significant, may remain undetected (Bilton et al., hypothesis’’, an extensive gene flow among popula- 2001). Moreover, dispersal often occurs through tions should grant the genetic homogeneity of the multiple processes and vectors (Higgins et al., 2003). species throughout their whole extensive distribution In this review, we will put a special focus on temporary ranges, actually preventing the occurrence of allopat- water bodies, since these ecosystems represent biodi- ric differentiation among populations and, eventually, versity hotspots (Williams et al., 2001; Zacharias et al., of allopatric speciation. Therefore, freshwater micro- 2007) and their functioning and conservation strictly organisms should belong to a few, widely spread (i.e. depends on the dispersal and colonization abilities of subcosmopolitan to cosmopolitan) species, and these their biota (Sahuquillo & Miracle, 2013; Marrone et al., should be characterized by the absence of genetic 2013; Korn et al., 2013). Moreover, temporary ponds, structuring throughout their whole wide distribution alternating flooded and dry phases, add the duration of areas, each of them actually acting as a single, their ponding phase as a further temporal dimension to immense, potentially panmittic population (‘‘Cosmo- their ‘‘insular features’’ (Ebert & Balko, 1987; Naselli- politanism Paradigm’’). Flores & Barone, 2012). In addition, these ecosystems However,