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Improving the Ecological Understanding of Species Complexes: the Case of Piscivory and Protracted Spawning in the Carp Gudgeon Group Hypseleotris Spp

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Improving the Ecological Understanding of Species Complexes: the Case of Piscivory and Protracted Spawning in the Carp Gudgeon Group Hypseleotris Spp Turkish Journal of Zoology Turk J Zool (2016) 40: 543-551 http://journals.tubitak.gov.tr/zoology/ © TÜBİTAK Research Article doi:10.3906/zoo-1507-1 Improving the ecological understanding of species complexes: the case of piscivory and protracted spawning in the carp gudgeon group Hypseleotris spp. (Eleotridae, Teleostei) Lorenzo VILIZZI*, Ali Serhan TARKAN Faculty of Fisheries, Muğla Sıtkı Koçman University, Kötekli, Muğla, Turkey Received: 02.07.2015 Accepted/Published Online: 29.02.2016 Final Version: 09.06.2016 Abstract: Species complexes are a common occurrence in freshwater fish assemblages and may often pose a challenge to the understanding of their ecology. A typical case is the ‘cryptic’ carp gudgeon group Hypseleotris spp. in southeastern Australia, which is thought to comprise four closely related species occurring sympatrically within the Murray–Darling Basin (MDB), where flow delivery scenarios have been proposed for the management and conservation of the native fish faunas. The objective of this study was to provide a deeper insight into the occurrence of piscivory and protracted spawning seasons in Hypseleotris spp. based on six years of sampling, and to cast the findings within the broader context of interrelationships between species complexes and their ecology. It is argued that what has been so far referred to as conspecific predation (cannibalism) in Hypseleotris spp. could be explained alternatively as ‘congeneric’ predation, or even as a combination of both. Furthermore, the presence of larvae all year round should be accounted for when assessing the effectiveness of taxon-specific water allocation programs. Better matching of taxonomy with ecology is, therefore, essential for the successful management and conservation of species complexes, and further insights may be provided through the assessment of altricial/precocial forms. Key words: Cryptic species, cannibalism, Murray–Darling Basin, Bayesian analysis 1. Introduction 2005). Among these, H. klunzigeri, together with Murray– In biology, a species complex is a group of closely related Darling, Midgley’s, and Lake’s carp gudgeon, are believed species very similar in appearance, such that boundaries to occur sympatrically within the Murray–Darling Basin between them are often unclear (Mayr, 1970). In fish, (MDB) in southeastern Australia (Unmack, 2001; Thacker several species complexes have been described (e.g., Taylor et al., 2007), even though the distributional ranges of H. and Dodson, 1994; Allibone et al., 1996; Klingenberg et klunzigeri and Midgley’s carp gudgeon also extend to the al., 2003; Barluenga and Meyer, 2004; Østbye et al., 2006), coastal drainages of the east (Thacker et al., 2007). including those from the freshwater fish fauna of Australia Yet, taxonomical difficulties in species identification (e.g., Crowley et al., 1986; Crowley and Ivanstoff, 1991; combined with extensive hybridization (Bertozzi et al., Musyl and Keenan, 1992; Jerry and Woodland, 1997; 2000; Schmidt et al., 2011) have resulted in the MDB carp Hammer et al., 2007), among which the genus Hypseleotris gudgeons to be referred to either as western carp gudgeon has long been regarded as ‘cryptic’ (Bertozzi et al., 2000; (in the broad sense) or as a species complex Hypseleotris Vilizzi and Kováč, 2014). Hypseleotris is widespread and spp., otherwise known as ‘carp gudgeon group’ (Humphries abundant across Australia, with eleven species recognized et al., 1999; King et al., 2003; Vilizzi, 2012). Across the so far (Unmack, 2000, 2001; Pusey et al., 2004). In MDB, Hypseleotris spp. are generally encountered in eastern and southeastern Australia, there are three slow-flowing or still waters of the littoral zone, normally described Hypseleotris species, namely empire gudgeon in association with macrophyte beds or other aquatic H. compressa, firetailed gudgeon H. galii, and western carp vegetation. They comprise generalist predators and gudgeon H. klunzigeri, and at least three undescribed taxa, opportunistic carnivores known to consume a wide namely Murray–Darling carp gudgeon Hypseleotris sp. variety of prey (Pusey et al., 2004), including terrestrial 3, Midgley’s carp gudgeon Hypseleotris sp. 4, and Lake’s insects and micro- and macroinvertebrates (Nielsen et carp gudgeon Hypseleotris sp. 5 (Thacker and Unmack, al., 1999, 2000a, 2000b; Meredith et al., 2003; Stoffels and * Correspondence: [email protected] 543 VILIZZI and TARKAN / Turk J Zool Humphries, 2003; Balcombe and Humphries, 2006). In events have resulted in lower accuracy compared to other addition, Meredith et al. (2003) were the first to refer to species (Vilizzi et al., 2013). the occurrence of ‘conspecific predation’ (piscivory) in As part of a long-term investigation on fish larvae Hypseleotris spp. from littoral riverine environments, and responses to in-channel flow pulses (Vilizzi,2012 ), the this finding was supported by later studies reporting ‘large’ occurrence of piscivory (Vilizzi et al., 2008) and the individuals feeding occasionally on ‘small’ individuals presence of protracted spawning seasons (Vilizzi, 2011, within emergent littoral macrophytes (Stoffels and 2012) in Hypseleotris spp. were briefly documented. The Humphries, 2003; Balcombe and Humphries, 2006). objective of the present study is to shed further light on Both across the MDB and worldwide, environmental these important ecological aspects of Hypseleotris spp. flow programs, aimed at the management and conservation and place them within the wider context of the ecological of freshwater fish faunas in human-altered water courses, understanding of species complexes (see Vilizzi and Kováč, have become an essential component for improved 2014). Based on current taxonomical knowledge, the ecosystem services, and have led to the development of implications of the findings are discussed in terms of their flow delivery scenarios tailored to the flow requirements relevance for understanding the ecology of Hypseleotris of different fish guilds (Baumgartner et al., 2014). Clearly, spp. in particular, and of species complexes in general, for the successful implementation of such intervention with a view to management and conservation measures. measures, an extensive knowledge of the ecology and biology of fish fauna is essential. However, in the case 2. Materials and methods of Hypseleotris spp., despite its recent categorization as a 2.1. Study area, sampling, and processing foraging generalist with a spawning season lasting from Lindsay Island (34°06′ S, 141°09′ E) is a periodically- September to April (Baumgartner et al., 2014), more inundated 15,000-ha anabranch system of the lower extended spawning periods have been reported (Vilizzi, Murray River (VIC, Australia) (Figure 1). Bounded by 2011, 2012), and predictive models for managed inundation the Lindsay River to the south and the Murray River to s e l a a l a W r t h s t u u A o S h t w u e o S N Murray Rver Lock 7 a l a r t a s r u o A t c h t V u Lndsay o Lower Creek S Lndsay Mullaroo Rver Mullaroo Lower Creek Island Upper Lndsay Rver Study stes Figure 1. Map of the Lindsay Island anabranch system showing the location of the study sites (marked by asterisks) along four different reaches (‘flow habitats’): Upper Lindsay River, Lower Lindsay River, Murray River, Mullaroo Creek. Arrows indicate direction of flow (black: fast flow; grey: slow flow; white-double: no flow). 544 VILIZZI and TARKAN / Turk J Zool the north, Lindsay Island is interwoven by a complex as ‘unidentified larvae’, and the total number and species anabranch network that is dually regulated by a lock and of larvae consumed by individual predators was then weir system in the Murray River main channel, and by a recorded. Finally, to investigate the length of spawning series of earthen and concrete structures located at key seasons, the abundance of larvae was computed as catch- anabranch effluent points (Vilizzi, 2012). Four reaches per-unit-effort (CPUE; details in Vilizzi, 2012). make up Lindsay Island: (i) the Upper Lindsay River, a no- 2.2. Data analysis flow shallow-ponded habitat; (ii) the Lower Lindsay River, Because of the large number of zero values resulting from a slow-flow weir pool and weir pool/riverine habitat; (iii) the absence of larvae in the gut of several Hypseleotris spp. the Murray River, a riverine habitat by definition; and (iv) individuals, a two-component model was used in which Mullaroo Creek, a fast-flow anabranch habitat. observed absences were modeled separately from observed From October 2001 to July 2007, fish larvae were presences (Kuhnert et al., 2005). Accordingly, in the model sampled from all reaches on Lindsay Island, except for the for presence/absence: Murray River reach, where sampling commenced later, in z ~ Bernoulli(p), June 2002 (sampling event 12 onwards). There were a total i of 76 sampling events over six seasons (each taken to last where 1if0yi 2 from August to July; Vilizzi, 2012): 13 in 2001–02, 14 in zi = 2002–03, 12 in 2003–04, 12 in 2004–05, 13 in 2005–06, and % 0otherwise 12 in 2006–07. Sampling schedule was every 3 to 5 weeks, and in the model for abundance conditional on presence: with three sites sampled at each reach. At each site, three yi | zi = 1 ~ truncated Poisson(λ). light traps (22 L × 22 W × 30 H cm) were deployed in the Modeling was within a Bayesian framework, using early–mid-afternoon in slackwater areas, left overnight, a Beta(1, 1) and a Gamma (0.001, 0.001) distribution as and reclaimed the next morning. Modified quatrefoil light uninformative priors for p and λ, respectively (Gelman traps were used during the first season (2001–02), but et al., 2004). For model fit comparisons, a Poisson from the second season onwards (i.e. 2002–03 to 2006– distribution was also fitted to the entire data set (i.e. 07) a 3-mm knot-to-knot mesh was wrapped around the including zero values), using an uninformative Gamma entrance chambers of the light traps to exclude potentially (0.001, 0.001) prior distribution.
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