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Uncovering the Current Distribution Pattern of the Rediscovered Hula Painted Frog (Latonia Nigriventer) Using Environmental DNA

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Uncovering the Current Distribution Pattern of the Rediscovered Hula Painted Frog (Latonia Nigriventer) Using Environmental DNA Received: 9 February 2017 | Revised: 11 September 2017 | Accepted: 25 September 2017 DOI: 10.1111/mec.14420 ORIGINAL ARTICLE Living quarters of a living fossil—Uncovering the current distribution pattern of the rediscovered Hula painted frog (Latonia nigriventer) using environmental DNA Sharon Renan1 | Sarig Gafny2 | R. G. Bina Perl2,3 | Uri Roll4,5 | Yoram Malka6 | Miguel Vences3 | Eli Geffen1 1Department of Zoology, George S. Wise Faculty of Life Sciences, Tel-Aviv Abstract University, Tel Aviv, Israel One of the greatest challenges of effective conservation measures is the correct 2The School of Marine Sciences, Ruppin identification of sites where rare and elusive organisms reside. The recently redis- Academic Center, Michmoret, Israel 3Division of Evolutionary Biology, covered Hula painted frog (Latonia nigriventer) has not been seen for many decades Zoological Institute, Braunschweig and was therefore categorized extinct. Since its rediscovery in 2011, individuals University of Technology, Braunschweig, Germany from the critically endangered species have been found, with great effort, only in 4School of Geography & the Environment, four restricted sites. We applied the environmental DNA (eDNA) approach to search University of Oxford, Oxford, UK for new populations of the Hula painted frog in suitable aquatic habitats. We fur- 5Mitrani Department of Desert Ecology, Ben-Gurion University of the Negev, ther used the eDNA data to classify the landscape factors associated with the spe- Midreshet Ben-Gurion, Israel cies distribution and to predict its suitable habitats. We sampled 52 aquatic sites in 6 Israel Nature and Parks Authority, the Hula Valley during the spring of 2015 and 2016 and amplified the samples with Jerusalem, Israel a species-specific qPCR assay. DNA of the Hula painted frog was detected in 22 of Correspondence the sites, all of which clustered within three main areas. A boosting classification Sharon Renan, Department of Zoology, George S. Wise Faculty of Life Sciences, model showed that soil type, vegetation cover and the current and former habitats Tel-Aviv University, Tel Aviv, Israel. are all key predictors of the frog’s current distribution. Intriguingly, the habitat suit- Email: [email protected] ability models reveal a high affinity of the species to its long-lost habitat of the his- Funding information torical wetlands. Our findings encourage a series of informed searches for new The Israel Nature and Parks Authority; U.S. Fish & Wildlife Services, Grant/Award populations of this threatened frog and provide guidance for future conservation Number: F14AP00886 management programmes. In the era of global conservation crisis of amphibians, developing the eDNA approach, a reliable detection method for many critically endangered and elusive amphibians, is of particular importance. KEYWORDS amphibians, conservation genetics, genetic monitoring, species distribution modelling 1 | INTRODUCTION years have been focusing on protecting the remaining amphibian populations and species across the world. Many of the conservation Amphibians are considered the most threatened class of vertebrates efforts focus on monitoring spatial distributions and determining sta- on earth (Hoffmann et al., 2010; Stuart et al., 2004). The IUCN Red tus and health of amphibian populations. As many of the critically List classifies 41% of amphibian species as threatened with 546 spe- endangered amphibians are highly elusive species, monitoring them cies listed as “critically endangered” (IUCN 2016). Major threats to can be an arduous task. Moreover, when monitoring rare species, amphibians include habitat loss, pollution, diseases and climate especially in aquatic environments, false-negative detections (type II change (Primack & Sher, 2016), and conservations effort in recent errors) are commonly obtained as detection probabilities are often | Molecular Ecology. 2017;26:6801–6812. wileyonlinelibrary.com/journal/mec © 2017 John Wiley & Sons Ltd 6801 6802 | RENAN ET AL. very low (Gu & Swihart, 2004). In some cases, calling surveys can be The recently rediscovered Hula painted frog (Latonia nigriventer) useful for detecting rare and elusive amphibians (Heyer, Donnelly, has not been detected in the wild for almost 60 years and was McDiarmid, Hayek, & Foster, 1994); however, this tool is not appli- consequently declared extinct by the International Union for the cable when monitoring silent species that produce low-intensity Conservation of Nature (IUCN) in 1996. Having been rediscovered calls. Moreover, when more than one species is present in the in October 2011, the Hula painted frog is now one of the most water, the acoustic monitoring is inefficient in detecting all species, endangered vertebrates on earth and listed by the IUCN Red List especially the rare ones (Pellet & Schmidt, 2005). These challenges as Critically Endangered. It was first described as Discoglossus lead to uncertainty about amphibian occurrence and often result in nigriventer following the discovery of two specimens on the east ineffective conservation action. This lack of systematic and reliable shore of the Hula Lake in northern Israel in 1940 (Mendelssohn & data on extremely rare amphibian species resulted in the designation Steinitz, 1943). In 1951, the Hula Valley wetlands were drained of some of these species as “extinct”; several of which were redis- with the aim of transforming the swamp into agricultural land. The covered at a later stage (Scheffers, Yong, Harris, Giam, & Sodhi, drainage of the Hula Valley, however, had severe ecological conse- 2011). quences, including the extinction of various unique species endemic Environmental DNA (eDNA) is rapidly becoming a ‘go-to’ tool for to the Hula Lake and swamp. During the drainage years, a third detecting species presence in aquatic environments and has been specimen of the Hula painted frog was found (Steinitz, 1955), and utilized in several studies (Bohmann et al., 2014; Goldberg, Strickler, since then, despite frequent surveys in its habitat, the species was & Pilliod, 2015; Taberlet, Coissac, Hajibabaei, & Rieseberg, 2012). In not seen for 56 years. The loss of the Hula painted frog became the last decade, eDNA techniques have been successfully applied to one of the symbols of the ecological catastrophe of the Hula Valley identify the presence of invasive species in the early stages of inva- drainage. sion (Dejean et al., 2012; Ficetola, Miaud, Pompanon, & Taberlet, Following its rediscovery in October 2011, molecular and mor- 2008), for detecting the presence of rare and endangered species phological analysis revealed not only that this species had ‘come (Goldberg, Pilliod, Arkle, & Waits, 2011; Jerde, Mahon, Chadderton, back from the dead’, but that it is also a living fossil belonging to the & Lodge, 2011; Laramie, Pilliod, & Goldberg, 2015; Olson, Briggler, & genus Latonia known previously only from fossil records (Biton et al., Williams, 2012; Pilliod, Goldberg, Arkle, & Waits, 2013; Sigsgaard, 2013). Intensive efforts have now been made to find more individu- Carl, Møller, & Thomsen, 2015; Spear, Groves, Williams, & Waits, als in order to assess the population condition, learn more about the 2015; Thomsen et al., 2012; Wilcox et al., 2013) and for assessing species’ life history and attempt a genetic study of the population. aquatic and terrestrial biodiversity (Andersen et al., 2012; Lodge Before this study began, only 34 individuals had been found at four et al., 2012). Quantitative PCR (qPCR) has been suggested to be par- restricted sites in the Hula area, all in terrestrial habitats neighbour- ticularly useful for eDNA studies due to its high sensitivity, as it was ing water bodies. Moreover, these individuals are cryptic, burrowing shown to have a higher detection probability than traditional sam- in the moist detritus, and uncovering them is a difficult task. During pling tools (Dejean et al., 2012; Thomsen et al., 2012) and conven- the initial searching for individuals, no tadpoles were found and 18 tional PCR techniques (Spear et al., 2015; Wilcox et al., 2013). This of the discovered individuals were very small juveniles (16–26 mm advantage is important in the study of rare and elusive species as it snout–vent length and 0.5–1.8 g weight; Perl et al., 2017), suggest- increases the probability of finding species at sites of low population ing that the tadpole stage of the Hula painted frog is of short dura- density. It thereby often reduces the probability of false negatives, a tion. As both adults and tadpoles are very difficult to detect, critical factor in conservation practice. This method is of particular monitoring the species and identifying potential new sites have appeal to organisms, such as amphibians, that spend at least part of remained a great challenge. their life cycle in an aquatic medium. In this study, we employed the eDNA approach to detect the Usage of presence data to identify landscape factors that are asso- presence of the Hula painted frog in potentially suitable aquatic ciated with species distribution and to construct habitat suitability habitats across the entire Hula Valley region. We then used this maps is an approach increasingly applied in ecology and conservation presence–absence data to identify the important landscape attri- practice in general (for a review, see Guisan & Zimmermann, 2000), butes associated with the Hula painted frog’s preferred habitat. and in the study of endangered amphibians in particular (Blank & We further constructed a habitat
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