Phenology of Three Coexisting Annual Fish Species: Seasonal Patterns In

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Phenology of Three Coexisting Annual Fish Species: Seasonal Patterns In Hydrobiologia (2018) 809:323–337 https://doi.org/10.1007/s10750-017-3484-9 PRIMARY RESEARCH PAPER Phenology of three coexisting annual fish species: seasonal patterns in hatching dates Daniel Garcı´a . Marcelo Loureiro . Emanuel Machı´n . Martin Reichard Received: 7 September 2017 / Revised: 12 December 2017 / Accepted: 16 December 2017 / Published online: 21 December 2017 Ó Springer International Publishing AG, part of Springer Nature 2017 Abstract Annual fish are specialized freshwater year (until late spring) in the pools that did not fishes that are adapted to live in seasonal freshwater desiccate. Our study demonstrates how annual fish can pools. Their life cycle is tightly adapted to seasonally cope with unexpected seasonal rainfall patterns that predictable aquatic and desiccated phases in their may be a consequence of current climate change. habitat. We used daily increments in otoliths to test the hypothesis of the direct association between seasonal Keywords Birth date Á Climate change Á Intraguild rains and hatching dates of three coexisting Aus- predation Á Killifish Á Hatching synchrony Á Otoliths trolebias species across 14 temporary pools in the Uruguayan pampa. Hatching was relatively syn- chronous within and between species across a small but topographically diverse region. Hatching occurred Introduction over 1 month in midautumn and peaked between 15 and 20 April 2015. The prediction of earlier hatching Temporary pools are extreme habitats that alternate of a large predatory annual fish species was not between aquatic and dry phases, typically associated confirmed. Unexpectedly, an unusual desiccation with cycles of precipitation and evaporation. Direct event in the middle of the winter growing season links with permanent waters and connections among (May–July) affected many pools. Some pools re-filled adjacent pools may be established during major after extensive precipitation in August, followed by flooding events. In other cases, groundwater flow the hatching of a new cohort in some (but not all) of systems can affect the water level and desiccation of those pools. The first cohort survived throughout the temporary pools. The relative importance of each factor in the seasonal dynamics of the aquatic phase and the connectivity of temporary pools depends Handling editor: I. A. Nagelkerken primarily on their distance from water sources and the local topography (Winter, 1999; Williams, 2006). ´ ´ D. Garcıa Á M. Loureiro Á E. Machın Community structure in temporary pools is strongly Departamento de Ecologı´a y Evolucio´n, Facultad de Ciencias, Instituto de Biologı´a, Universidad de la associated with the duration of the aquatic phase Repu´blica, Igua´ 4225, Montevideo, Uruguay (Schneider & Frost, 1996) and is highly resilient following a desiccation event (Brock, 1998). Organ- & M. Reichard ( ) isms either recolonize the pools actively (e.g. colo- Institute of Vertebrate Biology, Czech Academy of Sciences, Kveˇtna´ 8, 603 65 Brno, Czech Republic nization from permanent water bodies during flooding e-mail: [email protected] 123 324 Hydrobiologia (2018) 809:323–337 by many fishes or via active flight by insects) or hatch under different climatic conditions. Most tropical from dormant life stages that are present in the annual fishes, such as Nothobranchius in Africa and desiccated substrate (e.g. desiccation-resistant eggs of Austrofundulus in the Neotropics, hatch in the sum- crustaceans or diapausing embryos of annual fishes) mer, at the beginning of the rainy season, spending (Brock et al., 2003; Polacˇik & Podrabsky, 2015). their post-hatching lifespan in high water temperatures Species that inhabit temporary pools are often and completing their embryonic development when tightly adapted to their seasonal cycle. Fish may either the water from the highly seasonal rains evaporates exploit temporary pools seasonally by colonizing from the pool (Podrabsky et al., 1998; Blazˇek et al., them from adjacent permanent habitats during floods 2013; Reichard, 2016). In contrast, temperate annual or possess specific adaptations to complete their entire fishes from the southern Neotropics inhabit regions life cycle in temporary pools (Polacˇik & Podrabsky, with no distinct rainy and dry seasons and an even 2015). Annual fishes are a specialized group of small distribution of precipitation during the year. Instead, freshwater fishes that are closely adapted to the life the seasonality of the aquatic phase is driven by high cycle of temporary pools. They all belong to the evaporation during the hot summer months. Hence, suborder Aplocheiloidei (Cyprinodontiformes) where fish hatch in the autumn and live through the cold similar adaptations in response to seasonal desiccation winter period (Lane´s et al., 2014, 2016), with embry- have evolved repeatedly in Africa (Nothobranchiidae) onic development completed over the following and in the Neotropics (Rivulidae) (Furness et al., 2015; summer (Arezo et al., 2005). This difference suggests Loureiro & de, 2016). The key adaptation involves that the adaptations and environmental clues that resistant eggs that survive desiccation buried in the control hatching may be quite distinct among temper- pool sediment, with embryos possessing special ate compared to tropical annual fishes. developmental adaptations to these harsh conditions, A remarkable feature of annual fish populations is including a series of three diapauses (Wourms, the lack of overlap among generations. After hatching, 1972a,b, c; Podrabsky et al., 2001; Berois et al., annual fishes express rapid growth and reach sexual 2012; Podrabsky et al., 2017). Although the existence maturity within a very short time; from less than of desiccation-resistant life stages is common in 3 weeks in tropical species (Blazˇek et al., 2013)to aquatic invertebrates (Williams, 1997; Brendock & 12 weeks in subtropical/temperate species (Berois De Meester, 2003; Brock et al., 2003), it is extremely et al., 2012). Adults reproduce daily, but their eggs do rare in aquatic vertebrates (Burton, 1990; Polacˇik & not hatch and embryos likely remain in the sediment in Podrabsky, 2015). one of the developmental diapauses (Reichard, 2016; One remarkable adaptation of annual fishes is their Podrabsky et al., 2017). Current evidence suggests that ability to time their hatching to the start of the aquatic the next generation hatches during a subsequent phase of the pools. The timing of the hatching event is aquatic phase when desiccated period had eliminated thought to be triggered by environmental cues (partial parental generation. In African Nothobranchius from oxygen pressure, substrate humidity, temperature) regions with erratic precipitation, pools may complete (Watters, 2009), with sensitivity to threshold values several phases of desiccation and re-filling during a being determined by genetic background at the single rainy season (Polacˇik et al., 2014), always with interspecific level (Reichard et al., 2017) and varying a new cohort of fish (Reichard et al., 2017). While individually as a consequence of maternal effects there is some indication of several age cohorts (Polacˇik et al., 2017). Such complex control of coexisting in subtropical Cynopoecilus fishes on the hatching is believed to distribute its timing, minimiz- basis of size distribution of adult fish (Arenzon et al., ing the risk of complete failure of any offspring to 2001) and possibility of continuous hatching in reach sexual maturity in the case of non-seasonal Cynopoecilus fishes (Arenzon et al., 1999), no study rains, extensive dry periods, or too rapid desiccation of has thus far focused on estimating hatching dates (and newly filled pools (Podrabsky et al., 2016). their variability) in Neotropical annual fishes. Hatch- Annual fishes inhabit temporary pools in tropical, ing synchrony (or lack thereof) has been demonstrated subtropical and temperate zones. Interestingly, annual to be a strongly selected adaptive strategy in several fishes experience fundamentally different conditions taxa (Howe, 1976; Findlay & Cooke, 1982; Flint et al., during their embryonic and post-hatching periods 1994; Hillstro¨m & Olsson, 1994; Huss et al., 2010); 123 Hydrobiologia (2018) 809:323–337 325 yet no direct information is available for Neotropical et al., 2009; Brazeiro et al., 2014). The adjacent Rı´o annual fishes. Negro river directly floods a fraction of the study area The genus Austrolebias (Cyprinodontiformes, (region Rinco´n) during the highest river discharge. Rivulidae) is a group of annual fishes with 39 currently The terrestrial vegetation of Pampa Biome is charac- recognized species that all have restricted geographic terized by subtropical grasslands, but including native distributions throughout the subtropical and temperate trees such as Acacia caven and Prosopis nigra zones of southeastern South America (Loureiro & de, (Brazeiro et al., 2014). 2016). Their high diversity has been attributed to short The study area has a moist subtropical climate. The generation time (1 year), fragmented habitat that mean annual rainfall is 1,130 mm year-1, varying restricts dispersal and promotes population isolation from 224 mm in February (summer) to 42 mm in June (D’Anatro & Loureiro, 2005), and genomic instability (winter). The mean annual temperature is 17.3°C, (Garcı´a et al., 2001). The post-hatching part of ranging from 11.3°C in winter to 23.4°C in summer Austrolebias’ life cycle is limited to the cold period (https://es.climate-data.org/location/50536/). The of the year when evaporation is low. Under normal year of the
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