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 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 04WLYVHVra mH&C.Ka,Wihi 5 Weinheim KGaA, Co. & GmbH Verlag WILEY-VCH 2014 © Hydrobiology of Review International 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, Lake Fluctuating water levels Periodic droughts; washout Precipitation, rivers; Both A,H,D,S,Z Meerimajeel in drought potential low evaporation Marshes Wetlands that dry partly Usually predictable Varies greatly (months, Precipitation, flow, water Both A,H,D,S,Z or in drought decades); washout table; evaporation/ completely, gueltas potential low percolation Phytotelmata Pitcher plants, leaf axils, Spring into late summer Varies greatly: days to Precipitation, plant Detrital A, D, Z tree holes decades; washout fluids; evaporation/ potential high percolation

Seasonally Interdunal ponds, Varies: rare and Days, weeks, or months; Precipitation and water Both, varies A, D, S, Z 2014, flooded depressions playas, seasonal unpredictable to washout potential low table; evaporation/ on category pools, brackish predicable by season percolation 99 ponds, limestone ,3 turloughs –

Lotic systems Washes and intermittent Varies: rare and Weeks, months or longer; Precipitation; Both waters temporary of Rotifers A,H,D,S,Z 19 channelized seeps unpredictable to washout potential evaporation/ predicable by season seasonally high percolation Small aridland Rock pools (huecos, Often rare and Days, weeks, months; Precipitation; Both A, D, Z basins tinajas), aguelmans unpredictable washout potential high evaporation Cryogenic systems Cryoconite holes, melt Summer, but Days, weeks, or months; Melt water; flow or Grazing A, D water pools, ponds unpredictable washout potential low refreezing that freeze completely Artificial Anthropogenic Cattle tanks, Seasonal, Seasonal to long term; Precipitation; Both A,D,H,Z basins depressions from but varies washout potential evaporation/ warfare, fish ponds, with use seasonal (low to high) percolation quarries, rice paddies Small containers Birdbaths, cups, Seasonal Days, weeks, months; Precipitation; Grazing A, D, Z mesocosms, tires, washout potential high evaporation rain barrels and gutters Habitats associated Drainage ditches, tire Depends on local Days to weeks; washout Precipitation; Both A,D,S,Z with roads ruts and potholes, conditions potential moderate to evaporation/ foot/hoof prints low percolation

a) A, anemochory of dormant stages (diapausing embryos in monogononts and xerosomes in bdelloids); H, hydrochory of active or dormant animals from other populations; D, dormant stages produced by in situ population; S, active or dormant animals from surface runoff; Z, zoochory of dormant stages. E. J. Walsh et al. International Review of Hydrobiology 2014, 99,3–19 these basins fill by seasonal rain, a rise in the water table, rapid filling and potential washout from seasonal, but or snowmelt, with water disappearing by evaporation and/ sporadic, rains. Many small pools dry within a few days, but or percolation. larger ones may persist for much longer. Depending on Depressions between dunes can function as catch their location these basins are subject to both deflation and basins for seasonal rains, and upon filling can develop deposition of aeolian sediments and wide diel swings in robust communities. Several studies have been reported water temperature. Rotifers with unique life history on the numerous ephemeral dune ponds of Doñana adaptations [26], as well as cryptic species have been National Park (Spain). For example, Serrano and Fahd [59] recovered from rock basins: e.g., the Epiphanes senta found that species richness of both crustaceans and complex [71, 72]. rotifers was significantly correlated with the length of the hydroperiod. Accumulative species richness (A) and 3.7 Cryogenic systems mean, single collection species richness (M) varied as a function of hydroperiod: long (A ¼ 35, M ¼ 5.98); interme- Rotifers are found in ice habitats that span several scales. diate (A ¼ 41, M ¼ 5.09); short (A ¼ 24, M ¼ 5.62). This They are present in the interstitial film of water on the ice report indicates that sites with intermediate hydroperiods grains of algal patches on snowfields [73]. When a small are more speciose when the survey is accomplished over a mass of dust, rock, or organic debris on the surface of a longer timeframe, a fact that is missed by single samples: glacier is sufficiently warmed to melt water, a cryoconite see also [60–62]. Other complicating factors include hole will form; such holes or puddles can present differences in aquifer source, as well as the biotic and opportunities for colonization. Smagowicz [74] reports abiotic constituents [63]. Flooded areas following seasonal Keratella serrulata in temporary melt water puddles from a monsoons in a gypsum dune series in White Sands glacier on Mt. Turbacz (southern Poland). On a larger National Monument (New Mexico, USA) contain few scale, some shallow ponds in polar regions and alpine rotifers species (e.g., bdelloids, Hexarthra fennica, H. tundra freeze solid in the winter, yet rotifers are present polydonta), which is likely a function of the high sulfate even if the habitat is never completely ice-free [75]. concentrations of these habitats (EJW unpub. data). Everitt [76] reported presence of five bdelloids and five Other habitats that have not received adequate monogononts in Deep Lake Tarn, a pool that freezes attention include the Carolina Bays of the eastern solidly in the Antarctic winter. USA [64], wetland potholes of North American prairies [65], and tree tip ups. Tree tip ups are temporary pools that 3.8 Anthropogenic basins sometimes form when strong winds uproot a tree, creating a shallow depression that may fill with water long enough Systems of human origin that temporarily may hold water for a rotifer community to develop. are too multifarious for complete treatment here, but include cattle tanks, rice paddies, quarries, fish ponds, and 3.5 Lotic systems depressions associated with the actions of warfare [32]. Cattle (stock) tanks commonly are constructed by enlarg- Temporary streams and floodplain basins fill during ing an existing pool, damming a stream, or building a seasonal rains, sometimes very rapidly; others arise from walled tank. Because stock tanks typically are subject to seeps (intermittently flowing springs). These flow for heavy organic load from fecal material, these systems are varying distances, filling small basins along the often hypertrophic and are home to rotifers that are tolerant way [66–68]. Landscape use has an effect on the sediment to high nutrient concentrations (e.g., Euchlanis dilatata, E. egg bank of these habitats. For example, Frisch et al. [69] senta). Rice paddies usually are hypertrophic as well, and found differences in species composition when comparing contain numerous species [77–81]. For example, in their rotifers hatched from sediment taken from a temporary study of a rice paddy and an adjacent fish pond in Laos, stream flowing through agricultural lands as compared to Segers and Sanoamuang [78] recorded 135 species, with two reference zones. 41.5% present exclusively in the paddy.

3.6 Small aridland basins 3.9 Small containers

Rock pools are common in aridlands with exposed This category differs from the previous one by size and the impervious bedrock. Because these basins often occur original intent of use. Almost any type of receptacle that in clusters, they represent a metacommunity with the can hold water for more than a few days is a potential individual basins varying in size, spatial arrangement, and habitat for rotifers, including discarded cups and tires [82], potential for surface connectivity [15, 70]. Ranging in size birdbaths [83–85], cemetery vases, rain gutters [21], and from <1 to well over 1000 L, these habitats are subject to small tree hole analogs [86]. While it may be assumed that

6 © 2014 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim International Review of Hydrobiology 2014, 99,3–19 Rotifers of temporary waters any species is capable of colonizing these habitats, propagules from the sediments [93–96] or blowing bdelloids are commonly present: e.g., Abrochtha mesel- dust [97]. Samples should be taken from several sites, soni, Adineta vaga, and P. roseola. as the distribution of propagules may not be uniform. Sample preservation techniques depend on the 3.10 Habitats associated with roads ultimate fate of the material. As noted in Wallace and Snell [98], for taxonomic identification some species must When roadside drainage ditches and tire ruts or potholes be examined live, while others are best identified when become filled with water, they become temporary habitat for preserved in buffered formalin solution. Lugol’s iodine and rotifers. However, it appears that little research has been Rose Bengal stain can be used to enhance visibility for done on these sites beyond casual examination [87–91]. In counting purposes. Materials to be used for DNA analyses seasonal ponds that form in permanent road ruts in St. John, are better preserved in 95% EtOH. Thus, it is often US Virgin Islands, one of us (EJW) found high densities of advantageous to prepare both alcohol- and formalin- Asplanchna sieboldii, Brachionus angularis, and Filinia preserved material from field samples. novaezealandiae,aswellasDaphnia sp., Volvox sp., and a variety of ciliates. These habitats warrant further research. 5 Temporary waters: Contributions of rotifer research to ecological and 4 Sampling temporary waters evolutionary theory

Strategies for sampling temporary waters depend on the In the following section, we present specific examples of volume of the basin, but in practice these are usually no how studies of temporary waters have informed our different than those used in permanent systems (Table 2). understanding of ecological and evolutionary concepts. The ultimate goal of sampling a water body of any size is to obtain a truly representative sample of the biota present. 5.1 Biodiversity Given the naturally heterogeneous nature of many temporary waters both spatially and temporally, one must Traditionally, estimates of aquatic biodiversity have be particularly cognizant of the site, time, and frequency of focused on lakes, rivers, and other permanent water sampling. Depending on the goal of the study, sampling sources. However, it is becoming increasingly clear that may be qualitative or quantitative. Qualitative sampling temporary waters can make significant contributions to often involves collecting plankton tows from various points rotifer species richness (Table 3). It is not surprising that in a water body, while quantitative sampling strives to the number of rotifer genera and species recorded varies determine species abundance in a given volume of water. depending on habitat. Several rotifer species were first Methods for sampling the open water are more well recorded from temporary waters (Table 4). A few developed and a variety of devices (e.g., Van Dorn grab examples illustrating species diversity and endemism of samplers, composite samplers) are available that are rotifers in temporary habitats, and the effect of neglecting suitable for sampling larger temporary waters. For smaller these sites in regional surveys of species richness, are or more fragile systems, specialized methods are often given below. needed. For example, Yanoviak and Fincke [92] have Temporary waters in Australian floodplain basins described sampling methods for tree holes and other develop substantial communities [99, 100]. In a survey phytotelmata; these may be adapted for sampling other of >100 ephemeral pools along the River Murray, Shiel habitats with small volumes. Yet, the potential for temporal et al. [101] reported over 250 rotifer species; however, the fluctuations in active/dormant communities should be mean diversity of these sites was low and very variable: considered; samples taken immediately after inundation S ¼ 10.9, with 43% singletons. Further, such temporary may not reflect community dynamics toward the middle or waters harbor high levels of endemism. For example, Shiel end of the wet phase. In addition, application of traditional and his colleagues (pers. com.) compiled a list of described sampling techniques in small basins or those in the last endemics from Australia; 43% of these were found in stages of drying may result in serious alteration to ephemeral habitats or their sediments. community composition: i.e., the act of sampling can In a study of habitats on the island of Minorca, De influence the trajectory of community development. Manuel [102] found that of 45 monogonont taxa, 51% were Moreover, in deserts and other fragile systems where found only in permanent habitats, 18% only in temporary water is limited and/or a critical resource for animals, care habitats, and 31% in both. The richness of the permanent should be taken so as not to damage the resource. sites was 37 species, and that of temporary waters was 23. Another method of ascertaining the species present in a Thus, nearly 1/5th of the rotifer diversity on this island habitat, even one that is dry, is to revive dormant would have been missed if only permanent habitats were

Table 2. Examples of sampling methods employed in temporary habitats

Habitat Collection methodsa) Refs.b)

Tropical Tank bromeliads Pipettes (5 mL), filtered with 150 mm mesh net and then [1] (French Guiana) preserved Tree holes (Panama) All water removed, examined and returned; rotifers identified to [2] subclass Temperate Pitcher plants Whole leaves excised, returned to the lab and the entire [3] (Sarracenia purpurea) contents examined; (Newfoundland; Eastern seaboard, USA) Pipettes (15 mL), water removed from each leaf and examined [4] Small astatic ponds Planktonic: net bolting sieve mesh No. 25 [5] (Mikołajki, Poland) Aridland Billabong (Albury, Australia) Planktonic: 50 mm mesh net and small volumes taken by [6] syringe and filtered Billabongs (Victoria, Australia) Rehydrated dry sediments [7] Semiarid stream (Doñana, Spain) [8] Playa-cattle tank Planktonic: water tube (10 L) 53 mm mesh net [9] (Doña Ana Mnts, NM, USA) Desert systems: reservoirs, Planktonic: 63 mm mesh net; plant squeeze; sediment cores [10] cattle tanks, small rock and benthic material; hydrophyte surfaces pools, small springs, artificial ponds (Big Bend National Park, USA) Temporary ponds (50–104 m2) Planktonic: 30 mm mesh net; rinsing plants and algae into net; [11] (semiarid, NW Iran) sugar floatation extraction of diapausing embryos Temporary ponds, 0.1 to Planktonic: 63 mm mesh net [12] 5.0 ha (Southwest Spain) Cold Cryoconite holes Hand pump [13] (Arctic and Antarctic Stir water and grab sample [14] glaciers; Spitsbergen) Moss samples in shallow Plant squeeze method [15] ponds that freeze from the bottom up (Devon Island, NWT, Canada) a)Using a mesh size of 63 mm can underestimate rotifer density and biomass by 2–3 orders of magnitude [168]; biodiversity estimates also may be suspect. b)1, Brouard et al. [169]; 2, Yanoviak [57]; 3, Bateman [52]; 4, Petersen et al. [50]; 5, Klimowicz [170]; 6, Pontin and Shiel [100]; 7, Segers and Shiel [171]; 8, Frisch et al. [69]; 9, MacKay et al. [24]; 10, Wallace et al. [67], Walsh et al. [62], Wallace et al. [110]; Walsh (pers. obs.); 11, Viayeh and Špoljar [172]; 12, Fahd et al. [60], Serrano and Fahd [59], Fahd et al. [61]; 13, Mueller et al. [173]; 14, De Smet and Van Rompu [133]; 15, De Smet and Beyens [174].

examined. In a survey of >160 Chihuahuan Desert aquatic 5.2 Dispersal habitats (96 permanent; 67 temporary), we (EJW and RLW, unpubl. obs.) identiﬁed over 250 rotifer species (ca. Investigation of dispersal and colonization dynamics of 12% of all known monogononts). Species richness varied temporary habitats has led to the development and testing dramatically between permanent habitats (1–48) and of the Bass Becking Principle and the Monopolization temporary habitats (1–33), with 10% of species only Hypothesis. The Bass Becking principle of “everything is found in temporary habitats. everywhere, but nature selects” [103–106] has been

Table 3. Examples of the rotifer biodiversity of temporary habitats

Diversitya)

Geographic locations Site description Genera Species Refs.b)

Tropical Lake Chilwa, Malawi Periodic drought lake 4 6 [1] Temperate Asperg, Germany Ephemeral ditches and pools 10 32 [2] Mikołajki, Poland Small astatic ponds (n ¼ 8) 19 78 [3] Aridland Chihuahuan Desert (TX, USA) Ephemeral playa 21 35 [4] Chihuahuan Desert (TX, USA) Tinajas (n 10) series of cascading pools 5 15 [4] River Murray, Australia Isolated billabongs (n ¼ 13) 18 52 [5] West Azarbaijan, Iran Temporary ponds (n ¼ 3) 11 29 [6] Cold Arctic and Antarctic Temporary ponds that freeze completely (n 10) 61 330 [7] Devon Island (NWT, Canada) Solitary pools (n ¼ 8) that freeze from the bottom up 13 66 [8] Hyrnebeen Glacier (Spitsbergen) Cryoconite holes (n ¼ 8) 3 5 [9] a)Bdelloids not included. b)References: 1, Kalk [37]; 2, Klement [175]; 3, Klimowicz [170]; 4, Walsh, unpubl. obs.; 5, Shiel, per. commun.; 6, Viayeh and Špoljar [172]; 7, Species list, De Smet, per. commun.; 8, De Smet and Beyens [174]; 9, De Smet and Van Rompu [133]. attributed quite regularly to not only bacteria but also An important model of regional patterns of species zooplankton, especially rotifers [107]. While many zoo- distribution and gene ﬂow is the monopolization hypothesis plankton species are reported to be cosmopolitan, this (MPH). Based on the idea of persistent founder effects and feature has been rejected as a characteristic of these taxa; rapid local adaptation [112, 113], the MPH argues that rotifers have a biogeography [108–111]. historical colonization events of aquatic systems play

Table 4. Examples of rotifers that were ﬁrst recorded from temporary waters

Speciesa) Habitat Location Refs.b)

Tropical Abrochtha carnivora Seasonal wetland Barbados [1] Temperate Lecane herzigi Roadside pool Strahan, Tasmania [2] Trichotria buchneri Aridland Brachionus pinneenaus Creek bed Cue, Western Australia [3] Cephalodella sp. nov. Rehydrated, dry sediments River Murray, Victoria, Australia [4] Hexarthra sp. nov. Rock pools (huecos) Chihuahuan Desert, TX, USA [5] Floscularia wallacei Rehydrated, dry sediments Bonegilla, Victoria, Australia [6] Pentatrocha gigantea Cold Rhinoglena kutikovae Shallow lake, freezes to the bottom Bunger Hills, East Antarctica [7] Lecane piepelsi Shallow tundra pools (moss) Barentsøya, Svalbard [8] Lepadella deridderae deridderae Temporary pond De Panne, Belgium [9] Lepadella d. alaskae Tundra polygon trench Point Barrow, Alaska Lepadella beyensi Puddle of submerged moss Cambridge Bay, Victoria Island, [10] NWT, Canada a)Species have been standardized for validity according to Segers [176], but an exhaustive examination of the literature has not been done to determine whether these species have been recorded elsewhere since their original publication. b)Refs.: 1, Ricci et al. [131]; 2, Koste et al. [177]; 3, Koste et al. [178]; 4, Langley et al. [118]; 5, Schröder et al. [26]; 6, Segers and Shiel [171]; 7, De Smet and Gibson [179]; 8, De Smet [180]; 9, Segers et al. [181]; 10, De Smet [182].

© 2014 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim 9 E. J. Walsh et al. International Review of Hydrobiology 2014, 99,3–19 predominant roles in determining genetic structure of collected from snapshot sampling of active communities of present day populations, establishing prioritization effects either ephemeral or permanent habitats [127]. More and thus minimizing potential for new colonists to impact recently Frisch et al. [17] investigated colonization success genetic diversity. The MPH attempts to explain the paradox of zooplankton in 48 newly constructed ponds in Doñana that despite evidence for high dispersal capacity in National Park. While these researchers reported that zooplankton, gene flow often is restricted among pop- copepod and cladoceran success was positively correlat- ulations. However, some workers argue that there is little ed with relative position, connectivity, and surface area, no evidence showing wide and frequent dispersal and that significant features were found for rotifer colonists. founder effects may confound estimates of gene flow [114, 115]. Thus, Bohonak and Jenkins [115] argue that 5.3 Dormant communities dispersal and colonization are two separate processes. Both ideas were developed based on the assumptions that Depending on the system, sediments may hold a large aquatic habitats are somewhat temporary over geologic reserve of propagules (i.e., an egg bank), which is critical in time and that connectivity among sites can be high [116, re-establishing the rotifer community after drought [121, 117]. 127, 128]. Langley et al. [118] compared the rotifer Rotifers may disperse among temporary waters by communities that developed in mesocosms to which either water, wind, and/or animals. Supporting the idea of high sterilized or un-sterilized sediment had been added. Of dispersal capacity, communities become quickly estab- some 54 species observed in their mesocosms after lished in experimental mesocosms whether they are 35 days of filling, 22% had not been recorded in active supplemented with sediments containing dormant prop- water bodies in the area and four were new to science. In agules [118, 119], or not (EJW, per. obs.). One of us (EJW) another study, Walsh and her colleagues (per. obs.) found established six, 67 L mesocosms in the Chihuahuan that rehydrated sediments from 11 temporary habitats in Desert and followed zooplankton colonization patterns the Chihuahuan Desert yielded 32 species, seven of which over 9 weeks. All mesocosms were colonized by algae and had not been found in surveys of the active habitats. ciliates (week 1) and rotifers (week 2); 10 rotifer species The factors affecting survival of dormant rotifers in dry were found by week 7. No microcrustaceans were found. sediments include salinity, temperature, and UV light; These results rival those of Holland and Jenkins [120], who however, in damp sediments, humidity, microbial activity, report 10 rotifers and two microcrustaceans over 25 weeks. and predators also are important and need to be assessed Of the rotifers in the Chihuahuan Desert mesocosms, six in greater detail. Both bdelloid xerosomes [129] and were found in nearby natural habitats and six were hatched monogonont diapausing embryos [42] deteriorate over in a separate study of dried sediments taken from the study time, although in bdelloids desiccation actually may site. improve individual fitness up to a point [130]. One of us Flooding connects habitats that had been cut off by (HAS) found variation in hatching rates of diapausing drought, redistributing diapausing embryos among these embryos obtained from a series of ponds that differ in isolated sites [121]. Thus, large, permanent water bodies hydroperiod, and different rates of production and lipid can resupply smaller basins that do dry with active animals content of diapausing embryos made in the laboratory by (e.g., [122–126]). Interestingly, greater rotifer biodiversity brachionids from these ponds (Table 5). Potentially, can be obtained by rehydrating dry sediments than can be hydroperiod may influence the quality and thus viability

Table 5. Spearman rank partial correlation coefﬁcients (rho) of traits with hydroperiod for Iberian ponds, controlling for salinity

Rotifer trait BSA CVF HOY TIR TON TOS SAL Rho p-Value

Diapausing embryo hatching (%) 62 47 36 84 17 10 20 0.795 0.006 Diapausing embryo production 207 22 133 159 452 857 38 0.291 0.004 (total embryos) (76) (9) (46) (45) (75) (174) (13) Diapausing embryo lipids 3.9 16.0 11.9 7.6 29.0 4.7 19.4 0.265 0.005 (pixel intensity) (0.9) (1.5) (2.8) (1.9) (4.8) (1.3) (1.9)

Mean values are shown per pond, with standard error in parentheses. BSA, Balsa de Santed; CVF, Laguna del Camino de Villafranca; HOY, Hoya Rasa; TIR, Laguna de Tírez; TON, Poza Norte, Cabanes-Torreblanca Marsh; TOS, Poza Sur, Cabanes-Torreblanca Marsh; SAL, Salobrejo. Hydroperiod categories were taken from [42]. Lipids were quantified by first decapsulating (permeabilizing) diapausing embryos as in [183], then staining with Nile Red as in [184]. Significant partial correlations (two-tailed).

10 © 2014 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim International Review of Hydrobiology 2014, 99,3–19 Rotifers of temporary waters of diapausing embryos (e.g., by selecting for more/less extremely saline (>12 000 mScm1). Active zooplankton maternal investment). populations declined and, of course, disappeared when the lake dried completely. When the lake refilled the 5.4 Species interactions zooplankton community was dominated by K. tropica, which comprised some 50–80% of zooplankton abun- Rotifer communities of temporary waters have provided dance. In the post-filling phase (1969), rotifer diversity model systems in which to characterize types and increased to include four additional species: Asplanchna strengths of species interactions. In particular, temporary brightwellii, F. opoliensis, Filinia sp., and Testudinella wetlands, as well as cryoconitic and phytotelmatic habitats patina. Nonetheless, population levels declined, presum- provide simple communities that can be easily sampled, ably from intense predation by cyclopoid copepods. On the manipulated, and followed. other hand, near the end of a drying event in Lake Abrochtha carnivora rehydrated from sediments col- Meerimajeel (Australia) when the water was very turbid lected from a seasonal wetland in Barbados [131] presents and quite warm (40°C), B. calyciflorus and A. sieboldii an example of a unique type of species interaction that was dominated the zooplankton, achieving densities >3700 first characterized in a temporary habitat – carnivory in a inds. L1 [135]. However, upon rewetting the zooplankton bdelloid rotifer. All other bdelloids feed on bacteria, algae, community recovered slowly, but with a suite of uncommon and detritus. Carnivory in this species may be an zooplankton, including Brachionus dichotomus. Thus, both adaptation to ensure adequate energy acquisition before of these lakes seem to exhibit at least a limited hysteresis entering diapause of an unknown duration. in the pattern of rotifer species loss and restoration. Cryoconitic habitats are subject to diel freeze–thaw Playas have been the subject of ecological studies that cycles in summer and completely freeze during winter. follow the population dynamics of the community [24], These sites contain communities composed of ciliates, assess influence of contaminants [39], and discover new insects, nematodes, rotifers, and tardigrades that function species: e.g., Macrotrachela sonorensis [136]. Two as part of a simple food web along with green algae, extensive studies on species in seasonally flooded diatoms, and heterotrophic bacteria and fungi [132]. Rotifer depressions have been reported. In South Africa Hutch- species found in cryoconite holes on a glacier in inson et al. [137] provide a comprehensive survey of the Spitsbergen include both bdelloids (Macrotrachela insolita, pans and other inland waters, but those data still await a Philodina acticornis) and monogononts (Dicranophorus detailed review. In their survey of more than 100 sites in permollis, Encentrum mucronatum, Keratella cochlearis, Mongolia, Jersabek and Bolortsetseg [80] list more than Keratella quadrata, Lecane closterocerca) [133]. Presence 240 taxa in 55 genera, with potentially 16 species being of the voracious carnivore, D. permollis, indicates a new to science. It is likely that many more new species will tritrophic food web in this otherwise simple ecosystem. be discovered in aridland waters. In two desert playas at In frozen habitats like these, rotifers likely arrive as Hueco Tanks State Park and Historic Site, Walsh and her windblown propagules [97]. colleagues found a total of 45 species, as well as several In a recent study that combines field and laboratory unidentified bdelloid species. The rotifer community of experiments of invertebrate communities found within the these sites underwent pronounced seasonal succession, pitcher plant S. purpurea, Kneitel [134] shows trade-offs albeit with small population sizes. For example, in one site, that may promote coexistence, but results varied between Platyias quadricornis (found during the entire filled period) the local and regional community scale. At the local level, and Brachionus quadridentatus were dominant during the evidence was found for a trade-off in competitive ability summer months, followed by several species during the versus predator tolerance; this appeared to be mediated by late summer and early fall (e.g., Lecane quadridentata, intrinsic factors of the species such as body size. Yet, he Collotheca sp., Epiphanes chihuahuaensis, E. dilatata, did not observe trade-offs expected to be associated with Euchlanis triquetra, and Squatinella rostrum). Two species coexistence for the regional scale. were prominent in late fall and early winter (P. quadricornis and Rotoria sp.), followed by dominance of Keratella spp. 5.5 Population and community dynamics during winter months (Fig. 1). Seasonal forest pools that fill in the spring and/or fall are A good example of how population and community common and important habitat for small vertebrates and dynamics change in response to filling cycle is seen in some invertebrates (e.g., fairy shrimp), but knowledge of Lake Chilwa [37]. Before Chilwa dried in 1966–1968, three the rotifer community often is limited to a few species such species of rotifer were present mainly in the wet months as the bdelloids, P. roseola and Rotaria citrina, and the and only at 1–5% of zooplankton abundance (Brachionus monogonont, E. senta [11]. Large populations can develop calyciflorus, Keratella tropica, Filinia opoliensis). During rapidly in these systems, with different species dominating drying the water became very turbid, highly alkaline, and through the hydroperiod. For example, in the temporary

Figure 1. Phenology of rotifer population dynamics in a temporary, impounded playa at Hueco Tanks State Park and Historic Site (El Paso, TX, USA). Key to taxa ¼ 1. Collotheca sp.; 2. Euchlanis triquetra;3.Brachionus quadridentatus;4. Asplanchnopus sp.; 5. Philodina acuticornis;6.Polyarthra dolichoptera;7.Squatinella rostrum;8.Epiphanes chihuahuaensis;9.Euchlanis dilatata; 10. Pleuretra lineata; 11. Hexarthra n.sp.; 12. Rotoria sp.; 13. Keratella spp.; 14. Lecane quadridentata; 15. Platyias quadricornis. ponds of an Italian shrubland, Seminara et al. [138] found ment showed that B. plicatilis populations subjected to that Brachionus urceolaris and Filinia terminalis were short hydroperiods evolved a higher propensity for sex and common just before the summer drought, but upon dormancy. Interclonal variation in the propensity for mixis rewetting in the fall the pond was recolonized by a was reported in two monogononts (Epiphanes ukera and community dominated by B. quadridentatus. However, this Rhinoglena frontalis), where the proportion of mictic autumnal community collapsed and a different assem- daughters ranged from 14 to 50% [141]. In ﬁeld studies, blage, comprising K. tropica, P. vulgaris/dolichoptera, and Schröder et al. [26] reported that the stem females of an Sinantherina socialis, developed over the winter. undescribed species of Hexarthra from rock pools in the Chihuahuan Desert immediately produced mictic females. This feature likely provides a long-term adaptive strategy 5.6 Adaptations for a population that lives in ephemeral habitats that may dry up within a few days or weeks after a rain (see Bet- 5.6.1 Frequency of mixis hedging below). In addition, in populations of B. plicatilis from ponds of varying hydroperiod in the Iberian Peninsula, In most monogonont rotifers, diapausing embryos are the diapausing embryo hatching frequency is negatively product of sexual reproduction and hence the frequency, correlated with habitat permanence (rho ¼0.795, duration, and timing of mixis are important determinates of p ¼ 0.006; Table 5). long-term population persistence in temporary habitats. The frequency of mixis has been characterized for a small 5.6.2 Bet-Hedging number of species in lab and ﬁeld studies. Fussmann et al. [139] reported that offspring produced early or late in Hexarthra n. sp. has a life cycle that deviates radically from a female’s reproductive series had a lower probability of the norm in its highly ephemeral habitats. In this case, being mictic than those produced by mid-aged females. In rather than hatchlings from diapausing embryos develop- this study, no females produced 100% mictic offspring. ing into amictic stem females, 85% develop as mictic Smith and Snell [140] in a laboratory chemostat experi- females [26] with males and diapausing embryos

12 © 2014 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim International Review of Hydrobiology 2014, 99,3–19 Rotifers of temporary waters appearing within 2 days of filling. Embryonic development tools show that stress proteins hsp 40, 60,and70 are rates and time to maturity are quicker in this taxon than in required for thermal tolerance in Brachionus manjava- animals from more permanent habitats [26]. These traits cas. Further, Denekamp et al. [150, 151] note that are proposed as important bet-hedging strategies for diapausing embryos express genes for low molecular survival of the population, facilitating the production of weight hsps. Unlike in other species that enter diapausing stages that can ensure population survival in anhydrobiosis, desiccation tolerance in bdelloid rotifers the event of a dry spell. is not dependent on production of the stabilizing sugar trehalose [84, 152, 153], and in fact several species lack 5.6.3 Osmoregulation the genes encoding these sugars [84]. Late embryogen- esis abundant (LEA) proteins [151, 153] and multiple The defining feature of temporary habitats is the copies of alpha tubulin [154] appear to be important in pronounced change they undergo as they dissipate. The desiccation tolerance. In addition, ability to recover from habitat may disappear quickly by freezing, or slowly by anhydrobiosis is dependent on time and other environ- evaporation, or very slowly by percolation into the ground. mental conditions. In each case, there are concomitant changes in the Damaging effects of UVR and presence of protective physical and chemical factors. Addition of large amounts of adaptations have been demonstrated for a variety of water to a basin also can quickly alter water temperature, invertebrates, including rotifers [155, 156], and are best chemistry, and osmotic conditions [99, 142]. In fact, during characterized in bdelloids. In a seminal paper, Glady- flashfloods, the volume of an entire pool can be replaced shev and Meselson [157] demonstrated that bdelloids many times over within minutes. Moreover, some spates have an extraordinary tolerance to ionizing radiation that are capable of scouring a basin [143] or filling it with rock is probably mediated by DNA repair mechanisms for debris (pers. obs.). We do not know much about the ability double stranded breaks. More recently Krisko et al. [158] of rotifers to withstand such rapid changes, although some show that anti-oxidants also are involved in this works have investigated ability to tolerate specific tolerance. In a recent study on monogononts, it was stressors such as salinity shifts. found that UVR exposure can modulate hsp gene Green [144] proposed that Asplanchna priodonta expression in a brachionid species [159]. Yet overall, osmoregulates after observing individuals increasing or studies on the effects of UVR on dormant stages are decreasing the contractions rate of their bladders as a rare [160, 161]. function of salinity. Based on reports of the salinity of the habitats in which they are found, Bayly [145] suggested 5.6.5 Experimental evolution and rapid that B. plicatilis, H. fennica, and Hexarthra jenkinae should adaptation be osmoconformers. Further evidence for osmoconform- ing in B. plicatilis came from studies with a microcryoscope Although theoretical work has predicted associations of [146]. However, Lowe et al. [147] reported elevated ATP sex and dormancy with ephemeral habitats [162] and field consumption at high salinities and activity of Naþ/Kþ ATP- studies have noted correlations of hydroperiod with ase as evidence of osmoregulation in B. plicatilis. It is clear species’ presence or traits, few experiments have been that the mechanisms of salinity tolerance need further done to demonstrate casual evolution. However, the study. ability to maintain long-term semi-continuous or continuous flow-through (chemostat) cultures has been employed 5.6.4 Desiccation, heat, and UV radiation to follow evolutionary changes in the laboratory. These tolerance studies have revealed loss of sex in constant laboratory cultures [163], associated evolution of mixis with adapta- Tolerance to prolonged desiccation, high temperature, tion to heterogeneous environments [164], and suggested and ultraviolet radiation (UVR) as embryonic propagules the potential for eco-evolutionary dynamics where invest- (monogononts), or anhydrobiotic embryos and adults ment in sex and dormancy involves a feedback with (bdelloids), is critical to persistence of rotifer populations population growth [165]. Rotifers have been proposed in ephemeral habitats. This is especially true in desert as good models for macro- and microevolutionary regions where dormant stages in shallow, dried sedi- research [166], and recently permanent and ephemeral ments may be exposed to full sunlight for months with laboratory cultures of B. plicatilis sensu stricto were temperatures reaching up to 60°C [148]. Most work on established to experimentally test evolution in response to tolerance to these environmental extremes in monog- manipulation of hydroperiod. Over 385 days or 84 ononts has been limited to the B. plicatilis species generations (six simulated growth seasons) ephemeral complex. Smith et al. [149] review existing knowledge on versus permanent cultures evolved to produce greater the hsp stress proteins and using a variety of molecular numbers of diapausing embryos, maintain higher

© 2014 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim 13 E. J. Walsh et al. International Review of Hydrobiology 2014, 99,3–19 frequencies of sexual females, and more readily induce his insights on desert waters. We thank Drs. Wim De Smet mixis [140]. Individuals’ longevity was not affected by (University of Antwerp) and Russ Shiel (University of hydroperiod, potentially due to the long hydroperiod Adelaide) for use of their unpublished data, and Katherine duration (9 weeks) of ephemeral cultures relative to the White (Georgia Institute of Technology) for her aid in short generation time (4 days). processing diapausing embryos. We also thank Kate Moody (Ripon College), Dr. Christian Jersabek (University of Salzburg), and Dr. Károly Schöll (Hungarian Academy of 6 Conclusions and suggestions for Sciences) for their help in locating some of the references. further research Samples in St. John (USVI) were obtained under permit VIIS-2012-SCI-0007, and those at Hueco Tanks State Here, we reviewed an assortment of temporary waters, Park and Historic Site (El Paso, Texas, USA) under permit unified by presenting an aqueous habitat for rotifer TPWD 02-04 to E.J.W. We are grateful for permission to community development but at times transitioning into an sample and assistance from Laguna del Camino de inhospitable terrestrial realm of dried sediment or ice. The Villafranca and Laguna de Manjavacas of the Junta de majority of temporary waters across the globe have Comunidades de Castilla-La Mancha, the Managers and received little attention despite their potential importance Forest Rangers of Refugio de Fauna Silvestre de la in contribution to local and regional biodiversity and in Laguna de Gallocanta and Salada de Chiprana of the providing ecosystem services. For instance, the vast array Gobierno de Aragón, the Parque Natural del Hondo de of the habitats that occur in desert ecosystems have Elche, and finally to the Parque Natural del Prat de received little attention by researchers (e.g., [62, 67, 110, Cabanes-Torreblanca of the Generalitat Valenciana. We 167]). Several quantitative differences exist among tempo- thank Drs. M. Serra and M. J. Carmona (Universitat de rary water bodies, such as hydroperiod duration and Valencia) and members of their laboratory, including frequency of drying/freezing. Yet, whether these differences Montero-Pau, Dimas-Flores, and Tebar, for aid and result in graded selection pressures (e.g., for dormancy) support in sample acquisition or processing. Walsh was and/or thresholds exist (e.g., minimal hydroperiod duration supported in part by grants from the National Center for necessary for survival) remains unclear. Likewise, qualita- Research Resources (5 G12 RR008124) and the National tive distinctions occur, such as whether the wet phase is Institute on Minority Health and Health Disparities (8 G12 broken by desiccation or by freezing. The relative impor- MD007592) from the National Institute of Health. The tance of qualitative versus quantitative differences in contents of this paper are solely the responsibility of the structuring rotifer communities, and the degree of abiotic authors and do not necessarily represent the official views and biotic similarity among different hydroperiod categories, of NIH. warrants further research. 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