Debugging diversity – a pan‐continental exploration of the potential of terrestrial blood‐feeding leeches as a vertebrate monitoring tool

Abstract

The use of environmental DNA (eDNA) has become an applicable noninvasive tool with which to obtain information about biodiversity. A subdiscipline of eDNA is iDNA (invertebrate-derived DNA), where genetic material ingested by invertebrates is used to characterize the biodiversity of the species that served as hosts. While promising, these techniques are still in their infancy, as they have only been explored on limited numbers of samples from only a single or a few different locations. In this study, we investigate the suitability of iDNA extracted from more than 3,000 haematophagous terrestrial leeches as a tool for detecting a wide range of terrestrial vertebrates across five different geographical regions on three different continents. These regions cover almost the full geographical range of haematophagous terrestrial leeches, thus representing all parts of the world where this method might apply. We identify host taxa through metabarcoding coupled with high-throughput sequencing on Illumina and IonTorrent sequencing platforms to decrease economic costs and workload and thereby make the approach attractive for practitioners in conservation management. We identified hosts in four different taxonomic vertebrate classes: mammals, birds, reptiles and amphibians, belonging to at least 42 different taxonomic families. We find that vertebrate blood ingested by haematophagous terrestrial leeches throughout their distribution is a viable source of DNA with which to examine a wide range of vertebrates. Thus, this study provides encouraging support for the potential of haematophagous terrestrial leeches as a tool for detecting and monitoring terrestrial vertebrate biodiversity.

Vertebrate diversity revealed by metabarcoding of bulk arthropod samples from tropical forests

“…Although study areas and design differ, this is comparable to the number of vertebrates detected in iDNA studies targeting specific invertebrate taxa such as carrion flies in Côte d'Ivoire and Madagascar , carrion flies in Panama (Rodgers et al, 2017), leeches in Borneo (Schnell et al, 2018), blowflies in Malaysia (Lee et al, 2016), leeches in Vietnam (Schnell et al, 2012), and even higher than when targeting ticks in Canada (Gariepy et al, 2012). Thirty-two vertebrate taxa were detected in the study sites in Brazil and Tanzania.…”

“…Since the field of iDNA originated, targeted collection followed by iDNA analyses of gut contents has been carried out on different invertebrate taxa such as leeches (Drinkwater et al, 2019;Pérez-Flores, Rueda-Calderon, Kvist, Siddall, & Oceguera-Figueroa, 2016;Schnell et al, 2018;Weiskopf et al, 2018), sand flies (Kocher, De Thoisy, et al, 2017), blow and flesh flies Hoffmann et al, 2018;Lee, Gan, Clements, & Wilson, 2016;Lee, Sing, & Wilson, 2015;Rodgers et al, 2017;Schubert et al, 2015), mosquitoes (Kocher, De Thoisy, et al, 2017), ticks (Gariepy et al, 2012), marine copepods (Meekan et al, 2017), and shrimps (Siegenthaler et al, 2019). This has offered a new and promising tool to complement traditional vertebrate monitoring methods, something of great value in the ongoing biodiversity monitoring efforts (Bohmann et al, 2013).…”

Occurrence of blood‐feeding terrestrial leeches (Haemadipsidae) in a degraded forest ecosystem and their potential as ecological indicators

“…To analyze how forest structure influences the distribution of the two sympatric terrestrial leech types, we surveyed sites across a gradient of habitat quality. Our naming of the two leech species follows (Borda, Oceguera‐Figueroa & Siddall, ; Schnell et al., ; Tessler et al., ), but we recognize that genetic relationships among leeches are not always well resolved, and it is possible that some taxa might in time become recognized as species complexes (Borda et al., ; Schnell et al., ; Tessler et al., ). The surveys were conducted at the Stability of Altered Forest Ecosystems Project (SAFE project), a 72,000 ha fragmentation experiment in Sabah, Malaysian Borneo (4°33′N,117°16′E) (Ewers et al., ).…”

“…To test whether abundance of available prey influences leech detectability, we used a reduced leech survey dataset to compare the fit of models with and without the inclusion of mammal abundance as a covariate. In this study, we focus on mammals as a measure of available prey, because previous studies conducted in the same area were unsuccessful in detecting any other vertebrate groups in the diets of these two Bornean leech species (Drinkwater et al., ; Schnell et al., ). Firstly, we generated the covariate for mammal abundance from camera traps which had been deployed across the SAFE landscape from 2015 to 2017.…”

Host selection of hematophagous leeches (Haemadipsa japonica): Implications for iDNA studies

“…Calvignac‐Spencer, Merkel, et al () collected 201 individuals of carrion flies in Madagascar and Côte d'Ivore and detected 4 and 22 species of vertebrates (mostly mammals), respectively. Recently, Axtner et al (), Abrams et al () and Schnell et al () examined large numbers of leeches (1,532 and 3,427) to confirm if iDNA from leeches can be used to monitor biodiversity in a species‐rich tropical rain forest ecosystem. They suggested experimental and statistical workflows under the assumption of imperfect detection by iDNA.…”