Conservation priorities differ at opposing species borders of a European orchid
Introduction
Understanding the degree to which populations from different regions within the distribution of a species contribute to the long-term adaptive potential and survival of that species has important implications for formulating conservation actions (Thomas et al., 2008). Yet, sparse or patchy information on presence data for many species (‘Wallacean shortfall’, cf. Whittaker et al., 2005) as well as shortfalls in knowledge about local population trends, threats and responses to changes in climate (IPCC, 2007) and land use (Sala et al., 2000) are a significant barrier for priority assessments (Kozlowski, 2008).
The position of a population within the overall distribution of a species is assumed to result in variation of population traits and genetic identity partly through density independent factors and also due to biogeographical history (Hewitt, 2004, Hampe and Petit, 2005). Geographical concepts on spatial variation in population structure and dynamics include the central-marginal concept (CMC, Hengeveld and Haeck, 1982, Kluth and Bruelheide, 2005; also termed ‘abundant centre model’) and the ‘rear edge versus leading edge’ concept (RLEC, Hampe and Petit, 2005). The well-established CMC assumes a decrease in population growth rate, density and fitness from the centre to the margins of the range of a species (Hengeveld and Haeck, 1982, Brown, 1984, Gapare et al., 2005). These decreases have been linked to increasing environmental stress and decreasing availability of suitable habitat patches towards the range margins (Brussard, 1984), where species are presumed to be at their environmental distribution limit (Holt and Keitt, 2000). The formation of range boundaries of the species is thought to be mainly determined by particular climatic variables, such as low temperatures limiting the northward spread of the species and water availability being one of the limiting factors at the southern periphery (Woodward, 1996, Woodward, 1997) Genetic consequences of the CMC include reduced gene flow and genetic diversity of populations at the range periphery (Giles and Goudet, 1997, Ellstrand and Hoffman, 1990) because populations are farther apart and swamping of the edge zone gene pool by pollen or seeds from core populations which significantly slow adaptation to edge habitats (Baack et al., 2006). A major consequence of this theory is that the emphasis of a management regime would be better placed on central populations to ensure optimal use of project resources, because management targets may become increasingly difficult to achieve towards the edge of a species range, as suggested from the research on insects at the pan-European level (Bourn and Thomas, 2002). However, evidence for the demographic assumptions (reviewed by Sagarin and Gaines (2002)) and the genetic implications (reviewed by Eckert et al. (2008)) of the CMC remains inconclusive and so conservation projects may not be based on these assumptions alone.
Recent findings stress the importance of populations at the range peripheries for species survival (Hampe and Petit, 2005, Pearson et al., 2009). Marginal rather than central populations may harbour much of the genetic diversity of a species shaped by past climate-driven range dynamics (Hewitt, 2004) and may contain genotypes evolved under variable, extreme and suboptimal conditions indicating specific adaptations (Channell and Lomolino, 2000). Hampe and Petit (2005) reviewed literature conducted across taxa and ecosystems and suggested that ‘rear edge’ populations (populations residing at the low-latitude margins of the distribution of species) may be disproportionally important as long-term stores for genetic diversity and foci of speciation. Conversely, Pearson et al. (2009) showed that small populations of the seaweed Fucus serratus at the southern periphery of its distribution are less resilient to abiotic stresses probably because of reduced fitness and lower adaptive capacity.
In the study presented here, information on the geographic structure of demographic and genetic traits of populations of Himantoglossum hircinum (L.) Spreng. (Orchidaceae) have been used to test the assumptions of both the CMC and RLEC and consequently discuss the implications for formulating conservation measures. Detailed knowledge on life history (Carey and Farrell, 2002), climatic drivers of population dynamics (Pfeifer et al., 2006a, Pfeifer et al., 2006b), and distribution of H. hircinum makes the species a suitable model system for this task. Furthermore, H. hircinum is one of few species, where recent, climate-induced range shifts have apparently taken place demonstrated by the earlier onset of flowering and increases in abundance and population numbers at the species north and north-eastern range margins (Good, 1936, Carey, 1999, Carey et al., 2002, Pfeifer et al., 2006a), while decline in abundance and extinctions were observed along its southern range margin. Recent genetic diversity assessment showed that, contrary to expectations, genetic diversity of peripheral populations is not necessarily reduced (Pfeifer et al., 2009). Furthermore, the species is emblematic, being one of the tallest and hence most reliably recorded orchid species in Europe. At the northern range margins it tends to occur on threatened and highly diverse habitat patches. Both of these factors mark it out as a flagship for studying conservation requirements of communities rich in plant species originating from the Submediterranean–Subatlantic bio-geographic element (Preston and Hill, 1997) of the European flora and could act as an indicator of their response to climatic changes.
We analyse demographic traits of populations of H. hircinum for several central and peripheral regions within the distribution of the species. Geographical structuring of habitat quality is assessed by investigating site-specific environmental traits (soil, climate, management Plant stress is known to alter the 13C/12C ratio (hereafter called δ13C) in the plant tissue due to variation in photosynthetic capacity and stomatal conductance (Farquhar and Richards, 1984, Rundel et al., 1988) and this measure has been used in the work presented here to be an indicator of plant stress. Note that foliar carbon isotope variation is not related with plant stress per se, but with water use efficiency (WUE), and some studies have shown strong links between rainfall patterns and foliar δ13C variation (Stewart et al., 1995). Thereby, low WUE results in greater discrimination against 13C so that δ13C can be used as indicator of long-term water stress in individual plant species (Caldeira et al., 2001). Patterns of genetic traits, analysed in Pfeifer et al. (2009), are discussed in the light of geographical concepts and their implications for conservation planning.
We addressed four questions by the study presented below: (1) Do demographic traits (population size, number of flowering plants, flower production) vary between regions within the species geographical range? (2) Is habitat quality (e.g. soil attributes and climatic parameters) reduced at the periphery of the distribution of the species? (3) Is habitat quality reflected in demographic traits and physiology of the plants? (4) Do ‘rear edge’ populations differ from ‘expanding edge’ populations/core populations in their demographic traits and genetic structure and should they consequently be at the centre of attention for any conservation measures?
Section snippets
Study area and study species
Thirty-two populations of H. hircinum (L.) Spreng. located across the European distribution range of the species (Fig. 1) were studied.H. hircinum is a Submediterranean Subatlantic distributed orchid species that perennates via tubers. Leaves emerge from below-ground tubers in autumn and grow over the winter months; plants start to develop inflorescences in late April (Carey and Farrell, 2002). Population growth rate, transition probabilities between life stages and flowering probability of H.
Geographical structuring of population traits
Population size differed significantly among regions (KWT, log Nest: p = 0.05) (Fig. 2A, Table 2), caused by significantly higher population sizes at the northern and eastern peripheries compared to Atlantic and Italian populations (WT, log Nest: p < 0.05, pbonf < 0.1). But, population size did not differ significantly between the centre of the distribution and Northern and Eastern peripheries. Note the peculiarity of FR6, a population at the southern coast of France (Table 2). There, H. hircinum
Geographic population structuring and concepts
Inter- and intra-regional variations in population traits dominate the geographical patterns in population structures of H. hircinum. Demographic differences were linked, albeit weakly, to the location of populations at opposing borders of the species’ range. Populations at the north-eastern peripheries (‘leading edge’) are larger than sites at the southern peripheries (‘rear edge’), and flowering percentage as well as flower production were especially low in the Italian refugium. δ13C does not
Conclusions
Our study shows that geographical patterns of H. hircinum demographic traits are at least partly in line with the ‘leading edge versus rear edge’ concept. Climate appears to be the main driver of an observed range shift towards the Northern latitudes, supporting population growth beyond original species distribution limits at the north-eastern peripheries, and exerting stress on populations at the southern periphery. At the species level, planning exercises will have to account for the
Acknowledgements
We thank Peter Steinfeld, Helmut Heimeier, Michael Koltzenburg, Bernard Haynold, Beat Bäumler, Sonia Bernardos, Roberto Gamarra and Eric Walravens for supplying information on population locations. Special thanks go to Helga Küchly and Michael Gömmel for their help with laboratory analyses. We thank Ewan Shilland, Martin Mathaj and Carsten Buchmann for their support in the field. Manuscript structure and focus was improved by comments of anonymous referees. This study is part of the research
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Present address: Department of Plant Sciences, University of Cambridge, Downing Street, Cambridge, CB2 3EA, UK.