Rotifers of Temporary Waters

International Review of Hydrobiology 2014, 99,3–19 DOI 10.1002/iroh.201301700 REVIEW ARTICLE Rotifers of temporary waters Elizabeth J. Walsh 1, Hilary A. Smith 2 and Robert L. Wallace 3 1 Department of Biological Sciences, University of Texas at El Paso, El Paso, TX, USA 2 Department of Biological Sciences, University of Notre Dame, Notre Dame, IN, USA 3 Department of Biology, Ripon College, Ripon, WI, USA While ubiquitous, temporary waters vary greatly in geographic distribution, origin, size, Received: January 30, 2013 connectivity, hydroperiod, and biological composition. However, all terminate as active Revised: September 4, 2013 habitats, transitioning into either dryness or ice, only to be restored when conditions improve. Accepted: September 19, 2013 Hydroperiod in some temporary habitats is cyclical and predictable, while in others it is sporadic. Although the rotifer communities of temporary waters are subjected to unique selective pressures within their habitats, species share many of the same adaptive responses. Here, we review temporary waters and their rotiferan inhabitants, examining community composition, life history, and evolutionary strategies that allow rotifers to flourish in these fluctuating environments. Keywords: Astatic waters / Biodiversity / Diapause / Ephemeral ponds / Life history adaptations 1 Introduction most monogononts undergo a true, endogenously regu- lated diapause [6] in the form of diapausing embryos Temporary waters, also termed astatic, ephemeral, (resting eggs). As adults, monogononts possess little intermittent, vernal, seasonal, or periodic, are those in capacity to withstand freezing [7] unless extraordinary which the entire habitat alternates between the presence of methods are employed [8]. However, the subitaneous liquid water and its absence. Water loss can occur via embryos of Brachionus plicatilis are capable of surviving direct drainage, percolation, evaporation, or freezing, with freezing using cryopreservation techniques [9]. Regard- fluctuations in hydroperiod (wet phase duration) being less of the dormancy mechanism, survivors are poised to daily, seasonally, annually, or longer [1, 2]. Accordingly, life repopulate the habitat when liquid water returns. In in temporary waters is adapted to a duel existence, addition, community dynamics are affected because rotifer flourishing when the habitat contains liquid water, but dormant stages can undergo passive dispersal. As a result migrating or enduring its absence. For rotifers, which are temporary waters are useful systems to test ecological incapable of active migration to another habitat, occupancy theory [10–13], including metacommunity theory [14, 15], of temporary habitats is linked to tolerance mechanisms dispersal theory [16, 17], the effects of fragmentation on and/or passive dispersal. The two main subclasses of food web networks [18], and ecosystem processes in rotifers, bdelloids, and monogononts, use different strate- disturbed habitats [19, 20]. gies to survive in a dormant ametabolic state. Bdelloids The first account of the rotifers of temporary waters undergo quiescence, marked by a change in metabolism appears to be Van Leeuwenhoek’s description of rotifers in progressing into the anhydrobiotic state of the xero- rain gutters [21]. Since then there have been numerous some [3]. Adult bdelloids as well as their eggs can survive reports of rotifers in ephemeral habitats, but most of these repeated cycles of freezing and thawing [4, 5]. In contrast deal with habitats that dry, all but ignoring cryogenic systems. While some studies merely report species’ presence, others provide more detailed analyses [22, 23] or combine observational and experimental data [24– 26]. Here, we review the rotifers of temporary waters by Correspondence: Dr. Elizabeth J. Walsh, Department of Biological Sciences, University of Texas at El Paso, El Paso, TX, USA describing types of temporary habitats, examining various E-mail: [email protected] methods of sampling, and exploring their life history and Fax: 915-747-5808 evolutionary strategies. For additional discussion of the © 2014 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim 3 E. J. Walsh et al. International Review of Hydrobiology 2014, 99,3–19 distribution of rotifers across environment types, including and in drought years may burn. Once considered marginal permanent systems, consult Pejler [22] and references land, many marshes were drained; however, upon cited therein. Rotifers that live in the thin film of water of the restoration they quickly become good habitat for zoo- limnoterrestrial (which also may alternate between liquid plankton [40]. Some non-tidal salt marshes also are and dry/frozen) are not covered in this review: these temporary, with a hydroperiod that alternates between habitats include the edaphon of terrestrial [27] and bog being flooded with marine and/or freshwater inputs, and soils [28, 29], and water films on damp mosses and dryness [41]. In a similar fashion, coastal ponds can lichens [30]. dry [42, 43], but may be subjected to inundations of fresh- or brackish waters. Such sites offer an opportunity to study osmoregulatory ability in rotifers from habitats with 2 Characterizing temporary waters fluctuating salinities (see below) and have been the focus of several studies on adaptation and evolution of rotifers in The processes that produce the basins in which temporary temporary waters [44, 45]. waters arise are diverse. Like lakes, which are grouped into lake districts [31], temporary waters also have 3.3 Phytotelmata localized distributions [13, 32]. Perhaps due to this diversity, temporary waters defy a simple, consistent Plant hollows that hold water are natural microcosms, and classification. Several features may be important to our may be short-lived (e.g., leaf axils) or endure for decades understanding of the dynamics of temporary waters. These (e.g., tree holes; [16]). The volume entrained within these include the following: basin composition (edaphic con- systems varies from a few mLs in leaf axils, to a few L in ditions); water source; predictability of filling/thawing; tank bromeliads, to >5 L in tree holes [46]. seasonal timing and absolute duration of the hydrologic Traps of pitcher plants (e.g., Sarracenia) possess cycle; surface connectivity; and composition of biotic rotifers, but most research on these systems focuses on components. As a result several ways of categorizing the dynamics of the mosquito-inquiline community [47, temporary waters have been promoted [2, 25, 33–36]. 48]. Rotifers in these phytotelmata are limited mostly to Alternatively, Örstan [23] suggested a novel categorization bdelloids (Habrotrocha rosa and Philodina roseola), based on likelihood of drying as a function of number of which are consumed by dipteran larvae [49–51]. rotifer generations. According to the study of Petersen et al. [50] 70% of Sarracenia purpurea traps contain H. rosa, but Bate- man [52] reported a higher rate (ca. 95%). In a 3 Categories of temporary waters comprehensive survey of S. purpurea in three states in the northeastern USA, Błędzki and Ellison [28] report five Accounts of rotifers in temporary waters are numerous and other species in addition to H. rosa: Cephalodella widely scattered in the literature, but many times these anebodica, Keratella mixta, Lecane lunaris, Notholca reports are only anecdotal with the main emphasis being acuminata, and Polyarthra vulgaris. By excreting nitro- on microcrustaceans and/or insects. Here, we review 10 gen and phosphorous, rotifers are important in the general categories of temporary waters (Table 1), with the mineral nutrition of these communities [53]. Presumably, caveat that there is some overlap among these groups. rotifers live as inquilines in other pitcher plants, but no systematic surveys have been done. 3.1 Drought lakes Rotifers also have been reported in the leaf axils of certain plants (e.g., Dipsacus, Scirpus), tank bromeliads, and other Most lakes are viewed as being permanent, but in water-filled cavities of plants [54, 55]. Although they can be aridlands they can dry completely. For example, Lake quite abundant in forests, tree holes have been relatively Chilwa, a shallow lake in southeastern Malawi (Africa), neglected as a habitat for study [56, 57]. A common tree hole undergoes periodic drought [37] and the rotifer community inhabitant, Habrotrocha thienemanni, is capable of achieving À is reset after a drought/filling cycle. In an inland saline lake dense populations of >56 000 inds. L 1 [58]. in Argentina, rotifer species diversity was low but stable over two consecutive filling cycles, and was likely 3.4 Seasonally flooded basins and depressions constrained by high conductivity [38]. Depressions in the landscape include interdunal ponds, 3.2 Marshes playas (pans, vleys), pools in forests and shrublands (including Carolina Bays), prairie potholes, gueltas in Freshwater marshes are composed of both flowing and desert regions, brackish coastal ponds, tree tip ups, and stagnant waters, but some are inundated seasonally [39] limestone turloughs. Depending on the local conditions, 4 © 2014 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim © 2014 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim 5 International Review of Hydrobiology Table 1. Categories of temporary waters ordered by general hydroperiod characteristics Inundation Hydroperiod Hydrology Food web Likely population Category Examples frequency (duration; washout) (filling; discharge) (grazing or detrital) sourcesa) Natural Drought lakes Lake Chilwa,

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