Fairy Shrimps in Distress

Hydrobiologia (2013) 700:313–327 DOI 10.1007/s10750-012-1240-8 PRIMARY RESEARCH PAPER Fairy shrimps in distress: a molecular taxonomic review of the diverse fairy shrimp genus Branchinella (Anostraca: Thamnocephalidae) in Australia in the light of ongoing environmental change Tom Pinceel • Bram Vanschoenwinkel • Aline Waterkeyn • Maarten P. M. Vanhove • Adrian Pinder • Brian V. Timms • Luc Brendonck Received: 17 January 2012 / Revised: 22 June 2012 / Accepted: 23 June 2012 / Published online: 8 July 2012 Ó Springer Science+Business Media B.V. 2012 Abstract Australia, and especially South-Western gene of 31 presumed species, complemented with Australia, is a diversity hotspot for large branchiopod analysis of morphological structures holding taxo- crustaceans. A significant proportion of this diversity nomic information. Results revealed the presence of at is found in the anostracans (Crustacea, Anostraca) and least three new cryptic species. On the other hand, particularly in the diverse genus Branchinella with at some Branchinella lineages, surviving in environ- least 34 species. Members of this genus are found ments subjected to contrasting selection regimes, exclusively in temporary aquatic habitats which are appeared to be conspecific. This suggests substantial increasingly threatened by secondary salinization and physiological plasticity or important adaptive varia- other anthropogenic pressures. The development of tion present in some species, potentially enabling them adequate conservation strategies is therefore consid- to better cope with environmental change, such as ered a priority. To define conservation units, however, secondary salinization. Overall, these results further thorough knowledge of the taxonomy and phyloge- illustrate the benefits of combining molecular markers netic position of extant lineages is essential. We and classic morphological taxonomy and phylogeny to reconstructed a large scale phylogeny of the Austra- assess biodiversity and define conservation units in lian Branchinella by analyzing the 16S mitochondrial cryptic groups. Keywords Branchinella Á Molecular taxonomy Á Handling editor: Koen Martens Secondary salinization Á Conservation Á Australia Electronic supplementary material The online version of this article (doi:10.1007/s10750-012-1240-8) contains supplementary material, which is available to authorized users. T. Pinceel (&) Á B. Vanschoenwinkel Á A. Pinder A. Waterkeyn Á L. Brendonck Department of Environment and Conservation, Wildlife Laboratory of Aquatic Ecology and Evolutionary Biology, Place, Woodvale, WA 6026, Australia KULeuven, Charles Deberiotstraat 32, 3000 Leuven, Belgium B. V. Timms e-mail: [email protected] Australian Museum, 6-9 College St, Sydney 2000, Australia M. P. M. Vanhove Laboratory of Animal Diversity and Systematics, B. V. Timms KULeuven, Charles Deberiotstraat 32, 3000 Leuven, Australian Wetland and Rivers Centre, BEES, University Belgium of New South Wales, Kensington, NSW 2052, Australia 123 314 Hydrobiologia (2013) 700:313–327 Introduction aquatic habitats that periodically dry out (Fig. 1a). Some brine shrimp species, however, do occur in Australia, and South-Western Australia in particular, permanent salt lakes. With over 300 described is considered one of the world’s main diversity species worldwide, the anostracans are a diverse hotspots, not only for plants and terrestrial organ- group (Brendonck et al., 2008) which differs from isms (Myers et al., 2000) but also for freshwater other branchiopods by their predominantly pelagic invertebrates (Belk, 1998; Halse et al., 2000; Seger habitat use, relatively large size and lack of a & Shiel, 2003; Pinder et al., 2010). Over one protective carapace. In Australia, only five anostr- thousand freshwater invertebrate species have been acan genera occur that thrive in a wide variety of recorded in the Wheatbelt area in South-West habitats such as rock pools, clay pans and swamps Australia alone, of which about 20% are endemic (Timms, 2004, 2012). In contrast to the low generic (Pinder et al., 2004). A significant proportion of this diversity, Australia harbours at least 58 anostracan freshwater biodiversity is represented by primitive species, 40 of which occur in Western Australia. crustacean groups, such as the classes Ostracoda and This comprises about 15% of the world’s and 70% Branchiopoda (e.g. Halse, 2002; Halse & McRae, of the Australian anostracan diversity. Roughly 60% 2004; Pinder et al., 2004; Brendonck et al., 2008; (34 species) of the known Australian species belong Timms, 2008, 2012). Among branchiopod crusta- to Branchinella (Sayce, 1903; Timms, 2008, 2012) ceans, anostracans are generalist filter feeders typ- while the rest are mostly salt lake specialists and ical for the macrozooplankton community in fishless classified as Parartemia Daday, 1910. Fig. 1 a Example of a large branchiopod crustacean assem- sampled Australian Branchinella populations. Localities from blage from a typical habitat: a clay pan in Western Australia. specimens obtained from Genbank could not be mapped as no b Illustration of the effects of secondary salinization of a lake exact coordinates were available. The Wheatbelt area in system in the West Australian Wheatbelt area. c Overview of the Western Australia, which is severely threatened by secondary salinity tolerance of Australian anostracan species as recon- salinization, is highlighted in white. (Photo 1a and 1b by Bram structed from literature and additional field measurements (for Vanschoenwinkel) references, see text). d Geographical locations of the newly 123 Hydrobiologia (2013) 700:313–327 315 Many temporary aquatic habitats in Australia are genetic variation through the protection of Evolution- threatened by ongoing anthropogenic impact includ- ary Significant Units (ESUs). ing unsustainable agriculture, mining, river regulation, Our goal is to re-evaluate the phylogenetic rela- groundwater resource development and climate tionships in the diverse anostracan genus Branchinella change. One of the greatest threats, especially in the in Australia using primarily 16S mtDNA data and to Western Australian Wheatbelt area, is human induced assess the usefulness of these molecular data to define (secondary) salinization and altered hydrology appropriate conservation units by uncovering cryptic (McFarlane et al., 2004; Natural Resource Manage- genetic diversity. In order to achieve these goals we ment Ministerial Council, 2010) (Fig. 1b, d). Over the construct a molecular phylogeny based on a data set past 180 years, at least 18.3 million ha of South- which includes about 85% of the Branchinella species Western Australia was cleared of its natural deep- currently known to science as well as a number of rooted vegetation (mostly Eucalyptus and Acacia spp.) recently discovered lineages. Furthermore, based on to make way for shallow-rooted annual crops (Clarke this phylogeny, genetic distances among lineages as et al., 2002; Jardine et al., 2011). As a result, well as morphological and ecological information, we groundwater levels rose, carrying salts from deeper evaluate to what extent there is support for the large layers to the surface, resulting in salinity increases in number of species that have recently been described the topsoil and in surface waters as well as in an and discuss the taxonomic status of four newly altered hydrology (including prolonged hydroperiod discovered (currently undescribed) lineages. Finally, of temporary waters). Consequently, freshwater using information on the autecology of lineages communities are gradually replaced by less diverse, (salinity tolerance in particular), we assess the halotolerant or halophilic species assemblages, lead- potential impact of secondary salinization on Branchi- ing to a general diversity loss (Pinder et al., 2004). nella in the South-Western Australian diversity hot- Despite significant efforts of governments and land- spot and discuss the importance of demarcating proper holders (e.g. Wallace et al., 2011), many hundreds of units for conservation management. This approach is wetlands are affected. an essential step in developing conservation strategies In the development of adequate management for Australian branchinellids, which may be an strategies and sustainable agricultural practices, the example for other taxonomic groups and regions. accurate demarcation of appropriate biological conservation units is required (Mayden & Wood, 1995). Although no absolute consensus is reached on how to Methods best approach this, for groups with often subtle morphological differences among nominal species Studied organisms such as some anostracans, delimitation of conservation units should consider cryptic genetic diversity Branchinella and five other genera (Dendrocephalus (Crandall et al., 2000; Moritz, 2002; Hebert et al., Daday, 1908, Phallocryptus Birabeń, 1951, Spirali- 2003). Presently, the taxonomy of Australian anostra- frons Dixon, 2010, Thamnocephalus Packard, 1877 cans is almost exclusively based on morphological and Carinophallus Rogers, 2006) constitute the data, which may not accurately reflect diversity of the Thamnocephalidae (Rogers, 2006). Including around evolutionary lineages in the region. As of date, 42 described species from Australia, Asia, and Africa, phylogenetic relations in Australian anostracans are Branchinella is one of the most species rich fairy poorly known, with only limited taxonomic coverage shrimp genera (Belk & Brtek, 1995; Rogers, 2006; in preliminary molecular studies on

Load more