Elsevier

Biological Conservation

Volume 212, Part A, August 2017, Pages 216-229
Biological Conservation

Living on the edge: Forecasting the trends in abundance and distribution of the largest hoverfly genus (Diptera: Syrphidae) on the Balkan Peninsula under future climate change

https://doi.org/10.1016/j.biocon.2017.06.026Get rights and content

Highlights

  • We analyse impact of climate change on distribution and abundance of hoverfly genus.

  • Ranges of all and abundances of many species are projected to decrease in the future.

  • Climatic variables were more important in determining abundance than occurrence.

  • High mountain species are projected to almost vanish from Balkan Peninsula by 2080.

  • Nationally-designated protected areas are insufficient for species conservation.

Abstract

Responses of hoverflies (Diptera: Syrphidae) to climate change remain mostly unexplored. Here, for the first time, we investigate the impact of climate change on both presence/absence and abundances of hoverfly species. We used generalized linear models to analyse the relationships of climatic and soil variables with the occurrence and abundance of Cheilosia species on the Balkan Peninsula. Our results show that the ranges of all and the abundances of many species are projected to decrease in the future. Climatically suitable conditions for mountainous species are predicted to generally shift northwards. Species adapted to high mountains are projected to almost vanish from the Balkans and only regions of the Alps would remain suitable for them. We found climatic variables were more important in determining abundance than occurrence. Given that environmental factors differed in terms of their impact on abundance and occurrence, we highlight the importance of monitoring both parameters to ensure effective conservation. Considering the different projected responses of hoverflies to future climate change, as well as their value as pollinators and the increasing threats they currently face, knowledge on their responses to the major drivers of their life-histories is indispensable for proper management and conservation action. We reveal that nationally-designated protected areas are insufficient to conserve the species considered here, both currently and under projected climate change. We recommend implementation of an integrated conservation management plan that can provide a continuum of protected areas along the Dinaric mountain chain to facilitate movement of species to enhance species survival.

Introduction

Many studies have focused on how insects respond to climate change (Cammel and Knight, 1992, Parmesan et al., 1999, Bale et al., 2002, Hickling et al., 2005, Luoto et al., 2005, Musolin, 2007, Schweiger et al., 2008, Schweiger et al., 2010, Schweiger et al., 2012, Devictor et al., 2012, Kerr et al., 2015). Musolin (2007) suggested six categories of responses: changes in distribution range, abundance, phenology, voltinism, physiology and behavior, and community structure. Range shifts are the most easily observed and most often reported response (Musolin and Fujisaki, 2006). Many insects have tracked climate change rather than adapted to it (Coope, 1987). If unable to adapt, species can either remain in isolated pockets of unchanged environment (refugia) or become extinct (Thomas et al., 2004, Nogués-Bravo et al., 2008, Morueta-Holme et al., 2010). The effects of temperature on insect development rates and voltinism can also be reflected in changes in geographical distributions; a fact supported by fossil evidence (Coope, 1987, Ashworth, 1997). Existing studies on phytophagous insects have identified temperature as the dominant abiotic factor that directly affects development, survival, range and abundance (Bale et al., 2002, Kaloveloni et al., 2015). Such climatic effects are likely to differ among species, depending on their existing environments and life-histories, as well as their ability to adapt. Polyphagous species occupy different habitat types and show high phenotypic and genotypic plasticity. Such species are less likely to be adversely affected by climate change than those species that occupy narrow niches in extreme environments (Bale et al., 2002).

Global climate change is considered a major threat and is not only a conservation problem for the future, but has also been found to impact recent distributional patterns of pollinators (Kerr et al., 2015). Changes in pollinator communities not only affect wild plants, but have additional important impacts on agricultural crops (Free, 1993, Klein et al., 2007). Moreover, it has been emphasized that many factors other than climate (habitat loss, altered land use, introduction of alien species) can significantly influence distributions of plant and pollinator species and increase the risk of local and global extinction (Hill et al., 1999, Biesmeijer et al., 2006, Memmott et al., 2007, Potts et al., 2011). Soil conditions for instance determine types and distributions of plants that are floral resources for pollinator species and larval hosts for some phytophagous genera. Also, habitat destruction can affect mutualistic plant-pollinator networks (Steffan-Dewenter et al., 2002).

In this regard, rapid progress in predicting the distributions of species has been made and tools are now available to assess the impact of climate change on species (Thomas et al., 2004, Hijmans and Graham, 2006, Guisan and Thuiller, 2005). Species distribution models (SDMs) provide a useful way of incorporating predicted future conditions into conservation management and decision-making practices, but the limitations of these models must be considered before they can be applied to making policy decisions. Truly predictive models would require input parameters that are incompletely known, so we will never be able to predict the future with absolute accuracy. The performance of climate-driven range shift models can be diminished because of uncertain predictions of local climate change, inaccurate estimates of the climatic tolerance of species, and unforeseen evolutionary changes in populations (Araújo et al., 2005, Araújo and Rahbek, 2006). Additionally, these models disregard possible time-lags and indirect effects of climate change, such as biotic interactions, habitat changes and disturbance-driven perturbations (Hampe, 2004, Thom et al., 2016). However, the potential benefits of using our existing limited knowledge of bioclimatic modeling in biodiversity conservation still far outweigh the risks of incorrect actions or inaction.

In light of general pollinator decline, hoverflies (Diptera: Syrphidae) have been recognized as a threatened group at the European level (Biesmeijer et al., 2006). Although Carvalheiro et al. (2013) showed that declines in pollinator species richness have recently slowed down; this study was restricted to NW-European countries, while conditions in other European regions like the Balkan Peninsula remain unknown. Previous studies on hoverflies dealt mainly with current community compositions (Biesmeijer et al., 2006, Schweiger et al., 2007, Thom et al., 2016), and only a few have examined species distributions and projected shifts (Rotheray and Gilbert, 2011, Nikolić et al., 2013, Kaloveloni et al., 2015, Aguirre-Gutiérrez et al., 2017), but none investigated the impact of climate change on both presence/absence and abundance. However, climate change may also impact the abundance of a species, which is of even greater concern, since pollination services are sensitive to changes in abundances (Winfree et al., 2015). Whether climate change will impact distributions and abundances in the same manner is still a matter of debate (Renwick et al., 2012, Gutiérrez et al., 2013, Johnston et al., 2013).

The genus Cheilosia Meigen, 1822 (Fig. 1) is one of the most widely distributed and species-rich hoverfly taxa. It comprises around 300 Palaearctic, > 120 Nearctic, and at least 50 Oriental species, and a few species whose distribution extends into the northern Neotropics (Ståhls et al., 2004). It is the most speciose in Europe, followed by two other phytophagous genera, Merodon Meigen, 1803 and Eumerus Meigen, 1822 (Speight, 2015). Adults of Cheilosia are commonly encountered visiting flowers of Salix spp. from early spring and, then during the summer, visiting yellow (e.g. Ranunculus spp., composites) or white flowers (umbellifers). Flowers are visited to ingest their nectar and pollen. The immature stages are known for approximately thirty species, and feeding modes comprise phytophagy, fungivory and sap-feeding from coniferous trees (Rotheray, 1993, Stuke, 2000, Stuke and Carstensen, 2000, Stuke and Carstensen, 2002, Bartsch et al., 2009a, Bartsch et al., 2009b, Dussaix, 2013, Speight, 2015).

While some national and regional red lists have already been published (Jentzsch, 1998, Ssymank and Doczkal, 1998, Stuke et al., 1998, Doczkal et al., 1999, Cederberg et al., 2010, Ssymank et al., 2011), a European Red List of hoverflies still awaits collation as part of the Red List of European pollinators being generated under the EU's Status and Trends of European Pollinators (STEP) (2010–2015) project. Serbia is one of few countries in Europe that has adopted conservation policies for hoverflies in national law, with two important legal tools: 1) since 2010, 77 hoverfly species and their habitats have been protected by national law Code on declaration and protection of strictly protected and protected wild species of plants, animals and fungi (Official Gazette of RS, no. 5/2010), and 2) specific site protection due to the diversity and importance of hoverflies (Pil and Vujić, 2004). In total, 18 Cheilosia species are protected under Serbian legislation. Furthermore, Vujić et al. (2016) defined prime areas for hoverfly conservation (PHA - Prime Hoverfly Areas) in Serbia. Their results showed that although the area of proposed PHA outside of the nationally protected areas was very small (1.36% of the national territory), its protection would greatly improve hoverfly conservation.

Although Europe has the most extensive network of conservation areas in the world (100,000 sites across 54 countries), its borders were defined without taking into account the effects of climate change. Araújo et al. (2011) assessed the effectiveness of protected areas and the Natura 2000 network (an EU-wide network of nature protection areas established under the Habitats and Birds directives - http://ec.europa.eu/environment/nature/natura2000/index_en.htm) to conserve a large proportion of European plant and terrestrial vertebrate species under climate change. They showed that by 2080, 58 ± 2.6% of the species would lose suitable climate conditions in protected areas, whereas losses affected 63 ± 2.1% of species of European concern occurring in Natura 2000 areas. According to their results, protected areas were expected to retain climatic suitability for species better than unprotected areas, which was not the case for Natura 2000 areas. They emphasized the need to create new policies to avert the risk of jeopardizing ongoing efforts to conserve Europe's biodiversity from climate change.

Here, we analyse potential differences in the relative importance of climatic and soil variables for both distribution and abundance of the hoverfly genus Cheilosia on the Balkan Peninsula. We further project the consequences of such potential differences to future climate change scenarios. In order to assess the contribution of nationally designated protected areas for protecting regional biodiversity of Cheilosia species under climate change, we compared projected shifts inside and outside conserved areas and tested whether current protection offers any buffer to climate change.

Section snippets

Study area

The Balkan Peninsula is an area of southeastern Europe surrounded by the Adriatic Sea to the west, the Ionian, Aegean and the Marmara seas to the south, and the Black Sea to the east. Its northern boundary is often prescribed as being delimited by the Danube, Sava and Kupa rivers. Most of the Peninsula is occupied by massive mountain ranges, including the Dinaric, Balkan, Carpathian, Pindus, Rila, Pirin and Rhodopes mountains. Hilly areas predominate between these high mountain ranges, with

Results

Model performance for current distributions and abundance for Cheilosia species was good to excellent (following Landis and Koch, 1977 for TSS): R2 for abundance models ranged between 0.51 and 0.78 (mean ± SD: 0.67 ± 0.074); TSS for presence/absence models ranged between 0.83 and 0.99 (mean ± SD: 0.89 ± 0.30).

The relative importance of environmental variables differed for abundance and occurrence of Cheilosia species (Fig. 3; Tables S1 and S2). Soil texture was the most important variable for both

Discussion

Our results suggest that environmental factors can differ in their effects on species abundance and occurrence. These results are in accordance with other studies showing that environmental factors influencing abundance may differ from those limiting distribution, and that occurrence probability is not a good surrogate of abundance (Nielsen et al., 2005, Duff et al., 2011, Van Der Wal et al., 2009). Even if a species is projected to be stable or to lose only small amounts of area, nevertheless

Acknowledgements

This work was financially supported by the Ministry of Education, Science and Technological Development of Republic of Serbia, Grant No. OI173002 and III43002. We acknowledge the support of the European Commission Framework Programme (FP) 7 via the Integrated Project STEP (grant no. 244090, Potts et al. 2011). We thank John O'Brien for checking the English version and John Smit (Naturalis Biodiversity Center, Netherlands) for providing us with the photo of Cheilosia albitarsis.

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