View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by AIR Universita degli studi di Milano Even worms matter: cave habitat restoration for a planarian species increased environmental suitability but not abundance R AOUL M ANENTI,BENEDETTA B ARZAGHI,GIANBATTISTA T ONNI G ENTILE F RANCESCO F ICETOLA and A NDREA M ELOTTO Abstract Invertebrates living in underground environ- ponds and wetlands have been restored successfully ments often have unusual and sometimes unique adapta- (Bergmeier et al., ; Romano et al., ; Lü et al., ; tions and occupy narrow ranges, but there is a lack of Merenlender & Matella, ) but there are not, to our knowledge about most micro-endemic cave-dwelling inver- knowledge, any documented cases of freshwater restoration tebrate species. An illustrative case is that of the flatworm involving cave habitats. Dendrocoelum italicum, the first survey of which was per- Subterranean environments generally exhibit environ- formed years after its description. The survey revealed mental stability and are heterotrophic systems of key im- that the underground stream supplying water to the pool portance for the surrounding surface habitats (Culver & from which the species was first described had been diverted Pipan, ; Barzaghi et al., ): they work as recharge into a pipe for human use, thus severely reducing the avail- sites for surface waters, control water flux and exchanges able habitat for the species. Here we describe the results of with the surface, and provide shelter for key organisms such what we believe is the first habitat restoration action per- as bats, which sustain a variety of ecosystem services, includ- formed in a cave habitat for the conservation of a flatworm. ing pollination, seed dispersal and pest control (Souza Silva The water-diverting structure was removed, with the in- et al., ). Cave environments are sensitive to threats such volvement of local protected area administrators, citizens as climate change and groundwater pollution, but are also and volunteers from local organizations. The intervention affected by other local or regional factors such as quarrying resulted in the restoration of a large, stable pool inside the (Di Maggio et al., ), irresponsible exploitation for tour- cave, thus creating an optimal habitat for this threatened ism (Ivanova, ), and water harnessing and diversion planarian, with increased availability of prey and a stable (Achurra & Rodriguez, ). All of these threats are likely population. This report of habitat restoration for a neglected to affect cave and subterranean ecosystems significantly, but invertebrate offers insights for the protection of other they have been poorly studied. micro-endemic species. Underground habitats are of special importance for biodiversity conservation because they often host a highly Keywords Cave, Dendrocoelum italicum, flatworm, fresh- specialized fauna (Culver & Pipan, ; Romero, ). water, hypogean, Italy, planarian, restoration, subterranean Moreover, most organisms that live in caves are highly re- stricted geographically and low in abundance (Zagmajster et al., ;Delić et al., ). Predators, sunlight and envi- ronmental variations occurring on the surface may be Introduction important environmental conditions for a number of cave- ubterranean environments such as caves, shallow sub- adapted organisms (Culver & Pipan, ). Micro-endemic Sterranean habitats and underground aquifers are invertebrate species, both stygobionts (specialized aquatic among the most vulnerable habitats, often requiring conser- cave-dwelling organisms) and troglobionts (specialized vation attention (Culver & Pipan, ; Pipan et al., ). terrestrial cave-dwelling organisms), are in some cases Increasingly, studies are emphasizing the importance of known only from one or a few caves (Culver & Pipan, ; conservation approaches based on habitat restoration Mammola & Isaia, ; Wei et al., ). (Perring et al., ; Chazdon et al., ; Canedoli et al., However, endemic invertebrate species are rarely con- ). Ecologically important areas such as ecotones, sidered in conservation programmes (Cardoso et al., ; Noreika et al., ) despite their ecological importance. Cave-dwelling endemic invertebrates can play an important RAOUL MANENTI (Corresponding author), BENEDETTA BARZAGHI,GENTILE functional role in karst ecosystems, facilitating nutrient FRANCESCO FICETOLA and ANDREA MELOTTO Dipartimento di Scienze e Politiche Ambientali, Università degli Studi di Milano, Via Celoria, 26, Milano 20133, recycling and biomass exchange (Schneider et al., ). Italy. E-mail [email protected] orcid.org/0000-0001-6071-8194 Among cave invertebrates, planarians are free-living flat- GIANBATTISTA TONNI Monumento Naturale Altopiano di Cariadeghe, Serle, Italy worms generally characterized by zoophagous feeding be- Received March . Revision requested April . haviour, preying mainly on small living invertebrates and Accepted May . First published online December . grazing on decaying organisms (Reynoldson & Young, Oryx, 2019, 53(2), 216–221 © 2018 Fauna & Flora International doi:10.1017/S0030605318000741 Downloaded from https://www.cambridge.org/core. NATO Defence College, on 23 May 2019 at 14:21:41, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms . https://doi.org/10.1017/S0030605318000741 Even worms matter 217 ). Most planarian species are particularly sensitive to organic matter pollution and water quality (Horvat et al., ; Alonso & Camargo, ; Manenti, ). Nearly species, including marine and freshwater species, have been recorded in cave habitats (Romero, ). Most of the species described are blind and depigmented, thus showing a strong adaptation to cave life (Stocchino et al., ). Cave-dwelling planarians occur in subterranean habitats worldwide (Gourbault, ; Carpenter, ; Sluys et al., ), but most of the described species have extremely narrow ranges, in many cases being confined to a single cave (De Beauchamp, ). For most known cave-dwelling planarians no further study has been conducted beyond the description of the species. Generally, no additional PLATE 1 The restored pool in the Bus del Budrio cave (Fig. )in February . Photograph by Luana Aimar. information has been reported after collection of the speci- mens used for description, and even the information re- ported with the description is often secondhand. In many and after m forms a waterfall. In , when D. italicum cases descriptions were performed by anatomists specialized was described, a small waterfall filled a large pool, with a in Platyhelminthes, who never entered the caves but surface area of at least × m(Fig. ). During the s received specimens from speleologists. Moreover, cave- the water was diverted to a farm close to the cave (GT, dwelling planarians are adapted to interstices in which pers. obs.). This left only a small trickle flowing down to they shelter, and even when cave pools or streams host form a bipartite rivulet m long and cm wide (Fig. a). abundant populations, planarians are not easily detected As a result of this environmental alteration, the pool dried (Gourbault, ) and, consequently, it is difficult to assess up permanently. their conservation status. This situation is exemplified by the flatworm Dendrocoe- Methods lum italicum (Benazzi, ), which was described in in the Bus del Budrio cave in the Italian Prealps (Vialli, ). Habitat restoration The description of the species includes information about the habitat where it was found: a large subterranean pool In April we observed that the planarian D. italicum below a small waterfall. In we discovered that the spe- still occurred in the small rivulet. The rivulet appeared cies was threatened by a structure that was diverting water to be suboptimal, having a consistent flow and apparently from the waterfall into a pipe. Water was no longer reaching poor prey occurrence, whereas the typical requirements the pool, which had completely dried up, and D. italicum of Dendrocoelum planarians are for standing waters was confined to a short rivulet and a couple of tiny second- (Gourbault, ) with relatively abundant invertebrate ary pools. prey (Reynoldson & Young, ). We therefore began what we believe is the first habitat Firstly, we assessed the status and distribution of the restoration action performed in a cave habitat (Plate ) for species at the site (see below). Secondly, we informed the the conservation of a flatworm species, aiming to investigate administrators of the protected area about the critical whether the restoration technique applied was appropriate. condition of the species and the need for immediate In particular, we predicted that () the abundance of this conservation action. Thirdly, we helped the protected area cave-dwelling planarian would increase shortly after the res- administrators to raise awareness about the species amongst toration, and () habitat restoration would increase the citizens that use the reservoir for recreational activities and occurrence of the invertebrate prey of D. italicum. to obtain the agreement of the farmer responsible for divert- ing the water. Fourthly, we involved a local caving group, who volunteered to remove the structure diverting the Study site water flow. On December we collected all the planar- ians occurring in the rivulet, stored them in plastic tanks in- The Bus del Budrio cave is in the Italian Prealps (Fig. )in side the cave, and removed both the duct feeding the small the regional protected area