Combining citizen science with spatial analysis at local and biogeographical scales for the conservation of a large-size endemic invertebrate in temperate forests

Highlights

• Citizen science and species distribution models allowed to estimate threat status and habitat loss/fragmentation.

• North and center zones of the species range have the highest habitat loss and fragmentation.

• Under IUCN Red List criteria, we qualified A. valdiviana as endangered.

• A. valdiviana were mainly found in primary and secondary native forests.

• The abundance of A. valdiviana was positively affected by canopy cover.

Abstract

The ecology of leeches worldwide has been scarcely studied, with the ecology of Neotropical leeches remaining highly unknown. Americobdella valdiviana, an endemic, carnivorous, and giant leech that inhabits the Valdivian evergreen forest in southern Chile, an ecosystem that has experienced an increase in its net loss from 3.6% to 12% in the last decades due to various human activities. Here, we combined citizen science with species distribution models (SDM) to analyze (i) the effect of habitat variables with the abundance A. valdiviana, (ii) the distribution range, (iii) the habitat loss and fragmentation of A. valdiviana, and (iv) their conservation status. First, we asked each user or scientist for the observed relative abundance and a series of environmental variables, which were then correlated by using Generalized Linear Models. Then, distribution ranges were estimated using SDM, which was combined with multiannual forest cover maps to identify habitat loss and fragmentation between 2000 and 2018. Finally, we used IUCN criteria to evaluate the conservation status of this species. Abundance was related mainly to the canopy coverage, while suitability was positively associated to temperature seasonality and canopy cover. Suitability was higher in forests with levels of primary productivity. We found that the north and center zones of the species range experienced high habitat loss and fragmentation. Under IUCN Red List criteria, we qualified this species as endangered. Our results support that the combination of citizen science, SDM, and spatial analysis at local and biogeographical scales can inform conservation actions of poorly known and threatened macroinvertebrate fauna.

Introduction

Invertebrates have the largest number of species, abundance, and functional diversity of any group of animals in the planet, inhabiting all ecosystems worldwide, from eternal ice to the deepest points under the sea (Cardoso et al., 2011a, Leather, 2015, Mora et al., 2011). The protection of invertebrate biota is a priority for sustainable ecosystem management since they support essential provisioning, regulation, and recreational ecosystem services (Cardoso et al., 2011a, Leather, 2015, Prather et al., 2013). However, the lack of knowledge on the abundance and distribution patterns of invertebrates represents the most critical shortcomings for their conservation (Cardoso et al., 2011b, Troudet et al., 2017), making this information necessary under the current and future scenarios of land use change, fragmentation, and climate warming (Haddad et al., 2015).

Some invertebrate species are usually considered flagship or focal species due to their bright colors or large sizes, or their presence is even considered an indicator of ecosystem health (Alaniz et al., 2018, Barua et al., 2012, Bond, 1994, Cobbaert et al., 2010). However, there is a large proportion of invertebrates of which information is scarcely available, which could hinder the development of conservation actions for based on the study of their ecological dynamics (Troudet et al., 2017). Different approaches have been used to solve this limitation, among which citizen science could represent an important tool to increase the knowledge of this species (Koshkina et al., 2017). In fact, different citizen science projects have successfully generated new data on different invertebrates such as bumblebees, coccinellids, and flies (Alaniz et al., 2018, Barahona-Segovia and Barceló, 2021a, Barahona-Segovia and Barceló, 2021b, Grez et al., 2016, Montalva et al., 2017). An important data parameter of citizen science is linked with geographical coordinates, which can be combined with ecological niche modeling techniques to estimate distributions and habitat spatial dynamics, such as loss and fragmentation (Carvajal et al., 2018, Alaniz et al., 2018). Hence, the combination of citizen science and niche modelling opens new opportunities to study the effects of land use change on invertebrates within ecosystems that have been highly exposed to human pressures.

Southern South American forest have been seriously affected by land use change during the last decades, which have been mainly concentrated in the central-south zone of Chile between 30° and 40°S (Miranda et al., 2017, Rodríguez-Echeverry et al., 2018, Smith-Ramírez, 2004, Zamorano-Elgueta et al., 2015). These changes have caused high habitat loss and fragmentation of coastal native forests, which have a high number of poorly known endemic species and had been considered a biodiversity hotspot (Myers et al., 2000). One of these species is Americobdella valdiviana (Philippi, 1872), which is part of the leech family (Hirudinea) individuals belonging to a taxonomically diverse group (ca. 680 species), distributed across all continents, except Antarctica and the Pacific Islands, occupying terrestrial, marine, and freshwater habitats (Sket and Trontelj, 2007, Tessler et al., 2018). Americobdella valdiviana is a monogeneric species of Americobdellidae, which is the single family of Americobdelliformes order (Ringuelet, 1985, Tessler et al., 2018; Fig. 1A–F; Fig. S1, fixed animals). This species could be considered a top-predator species in ecological assemblages in temperate forest soils, which feed on native earthworms and have an essential role as population controller (Ringuelet, 1985). This species is more active during the humid season (autumn–winter), which coincides with an increase in the abundance of the earthworm, which promotes the predatory activity of the A. valdiviana. The latter is an unusual and scarcely collected species of giant leech, considered easily recognizable for its robust body and large size (reaching up to 27 cm), endemic to temperate forests of southern South America (Borda and Siddall, 2004, Moore, 1924, Ringuelet, 1985, Sket and Trontelj, 2007). Its color is variable, generating speculation on the presence of different species, with its dark gray color being the most common morphotype (Fig. 1E), followed by that of a dark gray body with orange bands on the edges (Fig. 1C–E; Ringuelet, 1985). However, a recent molecular analysis ruled out that the color-based morphotypes were different species (Alún, 2013). Scientific knowledge about the natural history of A. valdiviana remains neglected, which hinders the generation of analysis focused on its conservation. This species is intrinsically associated with the old-growth forest growing along the coastal mountain range (Alún, 2013, Christoffersen, 2008, Ringuelet, 1985). Described as a rare species that uses both terrestrial habitats and streams within the forest (Alún, 2013, Christoffersen, 2008, Philippi, 1872, Ringuelet, 1985), it could be considered a potential bio-indicator of ecosystem health in temperate forests.

The high dependence of A. valdiviana on the native forest, in addition to its low dispersal capacity, could make it particularly sensitive to habitat loss and fragmentation, as found for similar local invertebrates (Barahona-Segovia, 2019). The estimation of these effects of habitat variables at a local scale and habitat loss and fragmentation at a biogeographical scale have not yet been explored; however, the response of this species could be considered representative to the rest of leech community of the biome. Therefore, assessing the abundance and distribution patterns of the A. valdiviana may allow for the assessment of its conservation status by addressing the criteria of the International Union for Conservation Nature (IUCN) Red List. At the same time, it could inform appropriate conservation measures and priority areas for this species.

In this study, we aim to i) Estimate the effect of habitat variables on the relative abundance of A. valdiviana at local scale, ii) Determine the geographical distribution of the species and the effect of environmental variables on its habitat suitability at a biogeographical scale, iii) Analyze the habitat loss and fragmentation of the A. valdiviana between 2000 and 2018, and iv) Assess its conservation status based on the IUCN Red List criteria.