Combining citizen science with spatial analysis at local and biogeographical scales for the conservation of a large-size endemic invertebrate in temperate forests
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.
Section snippets
Study area
The native forests of the coastal range are distributed from approximately 35° to 46° S (Smith-Ramírez, 2004; Fig. 2). During the events of the last glaciation, they became important refuges for biodiversity before the environmental and geographical changes of the territory produced by the progress of periglacial ice (Villagrán and Hinojosa, 1997), which modulated the distribution patterns of the fauna related to coastal forests (Smith-Ramírez et al., 2007). In addition, these circumstances
Local scale
Only 44 opportunistic citizen science and active search records were assessed under the questions to know micro- and macro- habitat characteristics of the A. valdiviana leech (Table S1). Twenty-four, 55.54% (n = 24), were found in primary and secondary forests. Another 15.90% of the records (n = 7) were also found in secondary and mixed forest (native forest and exotic pine plantations) each. Regarding the microhabitat, 63.63% of records (n = 28) were found moving in the leaf-litter; 27.27%
Assumptions and potentialities
Our approach was useful to analyze the current state of A. valdiviana populations at local and biogeographical scales, contributing with new insight for its conservation. However, a series of assumptions need to be discussed to ensure the correct interpretation of our results and reproducibility of the analysis. Usually, the quality of modeling would be affected by the distribution of occurrences that influence the generation bias in the model associated with sampling effort (Phillips, 2009).
Author contributions
RMBS, CSR and AJA conceived the idea and wrote the first draft; RMBS, AJA and PMV carried out and revised the statistical analysis. JFA performed the taxonomic confirmation and photography of fixed animals. RMBS, VD-S, EFF, JG, RM-I, JP-S, FR, DR, VR, CV-D, MW, CSR, and JFA contributed to the dataset. All authors contributed equally to write and revise the draft and the final version of this study.
Data Availability Statement
Dataset is available in the link https://figshare.com/s/0c6b975f1bb2956fc97d (doi:https://doi.org//10.6084/m9.figshare.10003403). Abundance data of Americobdella valdiviana are available in the link https://figshare.com/s/82b538595f411c1f0d54 (doi: https://doi.org//10.6084/m9.figshare.10003409). Geospatial data will be available by email from the corresponding author on request.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
We are thankful to Cristian Villagra, Constanza Schapheer, and Andrea Riveros for their support in the logistics of manuscript preparation. Rodrigo Barahona-Segovia was funded by ANID-FONDECYT 3200817. Alberto J. Alaniz was funded by ANID-PFCHA/Doctorado Nacional 2020-21201496.
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