Warmer and richer? Predicting the impact of climate warming on species richness in small temperate waterbodies V E �� R O N I Q U E R O S S E T *, A N T H O N Y L E H M A N N w and B E AT O E R T L I * *Department of Nature Management, Hepia University of Applied Sciences Western Switzerland, hepia Geneva technology, architecture and landscape, CH 1254 Jussy-Geneva, Switzerland, wInstitute for Environmental Sciences, University of Geneva, CH 1227 Carouge, Switzerland Abstract Climate change is expected to affect communities worldwide. Many studies focus on responses at the regional level and show an increase in species richness. However, less is known about the consequences of climate change at the local scale (in ecosystems). Small waterbodies, such as ponds, could play an important role for the assessment of the impact of future changes in climate at the local level. We evaluated here the potential changes due to climate warming in the species richness for various groups (plants, snails, beetles, dragonflies, amphibians) across 113 lowland and high altitude ponds in Switzerland. We modelled the relationships between species richness and environmental variables (including temperature) and predicted species richness changes for the end of the century (2090���2100 using the A2 IPCC scenario). Temperature rise could significantly increase pond species richness. For the five taxonomic groups pooled, species richness would potentially increase from 41 to 75 (1 83%) in lowland ponds. In presently species-poor high altitude ponds, the potential increase would be particularly marked, with a proportional increase (1 150% from 14 to 35 species) almost double that in lowland areas. A strong increase in species richness also resulted from models including changes in additional variables, such as landuse or water quality. Future reductions in water quality (e.g. increase in nutrients) may limit the predicted increase in lowland species richness or, conversely, result in a greater increase in species richness in high altitude areas. Nutrient enrichment is shown to affect the taxonomic groups differentially, with plant species richness the most negatively influenced. Climate warming could therefore affect species richness of temperate ponds not only regionally, but also at the local, within ecosystems-scale species richness could increase markedly in temperate regions, and especially so at higher altitude. Keywords: amphibians, aquatic macrophytes, biodiversity, climate warming, Coleoptera, Gastropoda, macroinvertebrates, Odonata, ponds, predictive model Received 6 July 2009 revised version received 17 December 2009 and accepted 20 January 2010 Introduction Global average temperature has increased by approxi- mately 0.74 1C since the early 20th century (IPCC, 2007) and is expected to continue rising. Some parts of the world are more impacted than the average. For example, temperature increases are predicted to be particularly high in mountain regions (Nogues-Bravo et al., 2007). Climate change is expected to affect biological sys- tems worldwide (Rosenzweig et al., 2008). Most re- search is involved in the description and prediction of changes affecting species or taxonomic groups (Walther et al., 2002 Parmesan & Yohe, 2003 Parmesan, 2006) and describe, for example, species distribution shifts upwards in elevation and northwards in latitude (Hickling et al., 2006 Lenoir et al., 2008), or changes in phenology and voltinism (Menzel et al., 2006 Morin et al., 2009). All these processes have an important impact on species composition at the regional or local scale. Changes in composition of species assemblages have often been described at the regional level (biogeo- graphic regions or political entities) or at the local scale (e.g. site or ecosystem diversity). Such changes have been detected in Europe and North America for various taxa like diatoms (Ruhland et al., 2008), invertebrates (Burgmer et al., 2007), birds (Lemoine & Bohning-Gaese, 2003), and fish (Fodrie et al., 2009). For species richness, values at the regional scale have been shown to increase under the influence of climate warming in Europe and North America (e.g. Iverson & Prasad, 2001 Daufresne & Boet, 2007 Buisson et al., 2008). It is also well-known and well-described in almost every ecology textbook, that terrestrial and freshwater species richness tends to be lower in colder Correspondence: Veronique �� Rosset, tel. 141 22 546 68 68, fax 1 41 22 546 68 01, e-mails: veronique.rosset@hesge.ch beat.oertli@hesge.ch Global Change Biology (2010) 16, 2376���2387, doi: 10.1111/j.1365-2486.2010.02206.x 2376 r 2010 Blackwell Publishing Ltd

areas, i.e. at higher altitude or latitude (e.g. Gaston & Spicer, 2004 Nagy & Grabherr, 2009). This trend has also been well-described at the local scale for plants, invertebrates, and vertebrates (review in Rahbek, 1995). In contrast, the resultant changes in patterns of species richness associated specifically with climate warming have seldom been investigated, especially at the ecosystem level. Among the few existing studies, Henderson (2007) and Hiddink & ter Hofstede (2008), using time series, report an increase in fish species richness in marine ecosystems in response to climate warming. The local scale has generally been more often investigated through plots rather than for the whole ecosystem. For example, long-term monitoring of vege- tation plots in terrestrial environments indicates an increase in local species richness (Pauli et al., 2007 Vittoz et al., 2009). For freshwater ecosystems, whose biodiversity is highly endangered (Dudgeon et al., 2006), knowledge remains patchy about future trends under climate change (Heino et al., 2009). Freshwater studies are scarcer than those covering the terrestrial environment and existing work tends to describe species composition of assemblages rather than local species richness. How- ever, the elevational gradient of local biodiversity (a decline of species richness with altitude) has been described by a number of studies (e.g. Lods-Crozet et al., 2001 Jacobsen, 2008). Understanding the effects of climate change at the local scale is currently one of the main challenges of ecology, particularly in fresh- water ecosystems. Ponds are defined here as ���waterbodies between 1 m2 and 2 ha in surface area, which may be permanent or seasonal, and include both man-made and natural waterbodies��� (Biggs et al., 2005). Ponds are extremely numerous worldwide, and taking into account only the largest ponds (1000���10 000 m2) there are an estimated 277 million across the globe (from Downing et al., 2006). Furthermore, at the regional scale, they collectively support a very diverse, and in some cases unique biodiversity, often richer than those found in running waters or lakes (e.g. Williams et al., 2004 Angelibert �� et al., 2006). Ponds are therefore central to the conserva- tion and management of freshwater biodiversity (Oertli et al., 2009). Ponds have numerous characteristics, which enable them to play an essential role in the assessment and monitoring of the impacts of climate changes at the local level. Firstly, they are small and their community structure is relatively simple (De Mee- ster et al., 2005). Secondly, freshwater systems respond strongly to physical environmental changes, such as climate change (Heino et al., 2009). Thirdly, as ponds collectively host a large part of regional freshwater species richness (e.g. Williams et al., 2004), their monitoring in relation to anthropogenic pressure (such as climate change) is of critical importance. Finally, it is also evident that because ponds have relatively well- defined boundaries, their species richness at the eco- system level is easier to measure than for systems with less well-defined limits. Most studies of the effects of climate change on biodiversity have focused on a restricted selection of taxonomic groups, such as terrestrial vegetation, but- terflies, or birds (Root et al., 2003), making these taxa of particular interest as bioindicators. However, as species with different generation times or dispersal capacities might show different responses to changes in climate, responses of well-studied taxa could be nonrepresenta- tive of biodiversity changes as a whole (Thomas et al., 2004). It is therefore important to conduct investigations across a range of taxonomic groups to ascertain the impact of climate change on species richness. The main aim of this paper is to evaluate the potential effects of climate warming (independently of other physical changes) on biodiversity at the local scale (ecosystem) we therefore hypothesize that local rich- ness, as does regional richness, would increase in the future. We focus on species richness, one important component of biodiversity according to the Rio Con- vention (1992), and the most commonly used biodiver- sity measure in ecology (Magurran, 2004) and in bioassessments. Freshwater communities from ponds are taken here as a model, with five representative groups, which are taxonomically and ecologically dis- tinct: vascular plants, invertebrates (beetles, snails, and dragonflies), and vertebrates (amphibians). These taxa are ecologically complementary with respect to their life cycles (amphibiotic vs. aquatic) and colonization abil- ities (passives vs. actives). The questions investigated are: (i) will pond species richness increase in response to future warming? (ii) what will be the impacts of other variables expected to change with climate warming (e.g. landuse and water quality)? (iii) are there differences in response between taxonomic groups? (iv) will the response be of similar magnitude in lowland and high altitude areas? To conduct the study, species richness was assessed in 113 ponds across Switzerland, a country characterized by different altitudes (from lowland to high altitude) and therefore heterogeneous thermal conditions. The relationship between species richness and environmen- tal variables (including temperature and other variables e.g. landuse and water chemistry) was used to build predictive models [Generalized Additive Models (GAM)]. To begin, we predicted the future changes in species richness for the end of the next century accord- ing to the temperature increase from the A2 IPCC emission scenario. We then took into consideration P O N D S P E C I E S R I C H N E S S U N D E R C L I M AT E WA R M I N G 2377 r 2010 Blackwell Publishing Ltd, Global Change Biology, 16, 2376���2387