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Disentangling the roles of climate, propagule pressure and land use on the current and potential elevational distribution of the invasive weed Oxalis pes-caprae L. on Crete
ARTICLE IN PRESS Perspectives in Plant Ecology, Evolution and Systematics Perspectives in Plant Ecology, Evolution and Systematics 10 (2008) 251–258 www.elsevier.de/ppees
Disentangling the roles of climate, propagule pressure and land use on the current and potential elevational distribution of the invasive weed Oxalis pes-caprae L. on Crete Louise C. Rossa,b,, Philip W. Lambdonb, Philip E. Hulmeb,c a
School of Biological Sciences, University of Aberdeen, Cruickshank Building, St Machar Drive, Aberdeen AB24 3UU, UK NERC Centre for Ecology and Hydrology, Hill of Brathens, Banchory, Aberdeenshire AB31 4BW, UK c National Centre for Advanced Bio-Protection Technologies, P.O. Box 84, Lincoln University, Canterbury, New Zealand b
Received 23 November 2006; received in revised form 11 June 2008; accepted 16 June 2008
Abstract Climatic warming and land use change are likely to facilitate range expansions in invasive plant species, although the ability to predict such changes requires a better mechanistic understanding of the biological limits of populations. The introduced weed Oxalis pes-caprae, a significant pest of cultivation in many Mediterranean-type ecosystems, presents a suitable case study. The species distribution in the Mediterranean Basin closely follows that of olive cultivation, limited to below 600 m; yet its potential to colonise vulnerable areas at higher elevations has yet to be adequately assessed. To investigate the possibility, plant performance was assessed by experimentally sowing O. pes-caprae bulbils along an altitudinal gradient in the Lefka Ori mountains, Crete. The survivorship and bulbil biomass of the resulting plants all declined significantly with elevation, irrespective of soil type, initial bulbil size or seasonal variation. Whilst plants survived vegetatively up to 1400 m, seasonal bulbil productivity, likely to be critical to population viability, exceeded that of the sown bulbil biomass only below 750 m. These data indicate that the current elevation of O. pes-caprae is close to, but not at, its current climatic limit, and that low propagule pressure and scarcity of suitable habitat probably also act to limit the altitudinal distribution. Plant performance was correlated strongly with the duration of spring snow cover. Despite a 2 1C difference in mean spring temperatures in the 2 years of study, the predicted elevational change was only 37 m higher in the milder conditions. Overall, our results suggest that while O. pes-caprae performance is strongly linked to climate and is currently close to its climatic limit on Crete, there is limited scope for further spread unless land use and/or propagule pressure change at higher elevations. For this species, these elements are likely to be more significant drivers of invasion risk than the predicted changes of future climates. r 2008 Ru¨bel Foundation, ETH Zu¨rich. Published by Elsevier GmbH. All rights reserved. Keywords: Altitude; Biological invasions; Climate change; Land use change; Population viability; Propagule pressure
Corresponding author at: School of Biological Sciences, University
of Aberdeen, Cruickshank Building, St Machar Drive, Aberdeen AB24 3UU, UK. Tel.: +44 7910385167; fax: +44 1224 272703. E-mail addresses: [email protected] (L.C. Ross), [email protected] (P.W. Lambdon), [email protected] (P.E. Hulme).
Introduction Invasions by non-native species often severely compromise the biodiversity, ecological functioning and economic value of invaded ecosystems (Mack et al., 2000; Hulme, 2006). Future global changes, such as
1433-8319/$ - see front matter r 2008 Ru¨bel Foundation, ETH Zu¨rich. Published by Elsevier GmbH. All rights reserved. doi:10.1016/j.ppees.2008.06.001
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climatic warming and an increased tendency towards human-dominated land use, are likely to favour invasive species and exacerbate their impacts (Dukes and Mooney, 1999; Vila` et al., 2006b). The Mediterranean region is often considered to be particularly susceptible to the combined effects of biological invasions and anthropogenic disturbance (Sala et al., 2000; Gritti et al., 2006); yet few experimental studies have attempted to examine the relationship between land use and climate on the distribution of alien species (Becker et al., 2005; Thuiller et al., 2006). Correlative models suggest that climate is a major constraint on the distribution of many alien plant species (e.g. Kriticos et al., 2005; Dunlop et al., 2006). Whilst several studies have suggested likely range shifts based on such analyses (e.g. McDougall et al., 2005; Thuiller et al., 2005; Gritti et al., 2006), the ecological processes that limit plant distribution often remain largely unknown. However, the power of correlative assessments is reduced when the species range is not at equilibrium with the current climate (Hulme, 2005), propagule dispersal is limited, or where environmental gradients (e.g. agricultural land use and climate) are spatially confounded (Willis and Hulme, 2002). Elevation appears to be an important correlate of alien species richness (Ullmann et al., 1995; Becker et al., 2005; McDougall et al., 2005) as well as distribution (Kitayama and Mueller-Dombois, 1995) and is often used as a proxy to explore the role of climatic limitation (Ko¨rner, 2007). Yet, low numbers of alien species at higher elevations may also reflect reduced propagule supply (Aragon and Morales, 2003), lower disturbance frequency (Kitayama and Mueller-Dombois, 1995) or simply the time since introduction (Becker et al., 2005). Thus, disentangling the relative importance of climate, habitat availability and propagule supply on the potential for invasion under a future warmer climate requires experimental rather than solely biogeographical (Thuiller et al., 2005) or observational (Becker et al., 2005; McDougall et al., 2005) approaches. Experimental sowing of species within and beyond their existing distributional range provides a means to assess the relative roles of climate, propagule supply and edaphic factors (e.g. soil type) on species abundance and performance (Carter and Prince, 1985; Willis and Hulme, 2002; Akasaka and Tsuyuzaki, 2005; Ramirez et al., 2006; Paiaro et al., 2007). Yet, in contrast to the numerous observational studies linking alien species elevational distributions to climatic limits (e.g. Kitayama and Mueller-Dombois, 1995; Aragon and Morales, 2003; Arevalo et al., 2005; Becker et al., 2005; Daehler, 2005; McDougall et al., 2005; Pauchard and Alaback, 2004), relatively few experimental approaches have been undertaken to examine alien plant species distributions along elevational gradients (Willis and Hulme, 2002; Akasaka and Tsuyuzaki, 2005; Paiaro et al., 2007).
In this study, experimental sowing of the Bermuda buttercup Oxalis pes-caprae L. (Oxalidaceae, hereafter Oxalis) along an elevation gradient on the Mediterranean island of Crete is used to examine the relative roles of climate, propagule supply and soil type on current distributional limits. While it is trivial to identify that climate presents an absolute limit to species elevational distribution, the key question is whether this physiological constraint coincides with the current limits. Thus the objective is to test whether the current distribution limit is absolute and determined uniquely by physiology through plant survivorship or is a demographic limit, reflecting constraints on plant population persistence. In the former case, the species response to future climatic changes may be predicted from a knowledge of bioclimatic surfaces or plant physiological models. Demographic limits are likely to occur at lower elevations than those imposed by physiological constraints and thus species response may also be conditional on changes to habitat suitability and propagule supply (Hulme, 2003). Oxalis is particularly well suited to these questions since it is a serious widespread economic weed of Mediterranean agriculture (Hulme et al, 2008), causes oxalate poisoning in livestock if eaten in sufficient quantities (Gimeno et al., 2006), and reduces both native species richness (Vila` et al., 2006c) and net primary production (Petsikos et al., 2007) where it occurs. The regional distribution is well described by bioclimatic niche models (Thuiller et al., 2005) and thus the responsiveness of Oxalis to climate will be essential information for predicting future risks and guiding management.
Materials and methods Study species Oxalis, a native to the Cape Region of South Africa, is an invasive alien weed in Italy, Greece, the Iberian Peninsula and North Africa, and beyond the Mediterranean basin in Portugal, south-west England, California, Florida, Australia, India and New Zealand (Vila` and Gimeno, 2007). The species was introduced to Crete in 1880 (Rackham and Moody, 1996), and is now prolific in anthropogenic habitats where the frequency of disturbance is high and the soil well-drained and fertile, especially in olive (Olea europaea ssp. europaea L.) groves and on other cultivated land (Rackham and Moody, 1996). The current distribution of Oxalis on Crete follows the boundaries of olive cultivation closely and has an altitudinal limit of 600 m above sea level (Turland et al., 1993), a pattern that is likely to have been facilitated by disturbances such as ploughing (Sala et al., 2007). Further colonisation is probably limited by poor dispersal of the bulbils away from
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Table 1.
253
Description of sites located along the elevation transect
Elevation (m)
186
459 606 781 1022 1190 1402
Vegetation type
Margins of olive grove, with Prunus dulcis (Mill.) D.A.Webb, Anagyris foetida L., Olea europaea Margins of olive grove, with Prunus dulcis, Olea europaea Dry grassland with scattered Pyrus spinosa Forssk., Olea europaea Sub-alpine shrubland, with Pyrus spinosa, Sarcopoterium spinosum (L.) Spach Pasture on Omalos plateau, heavily grazed by goats and sheep, with Pyrus spinosa Sub-alpine shrubland, with Pyrus spinosa, Berberis cretica L., Acer sempervirens L Alpine dwarf shrubland, with Acer sempervirens, Prunus prostrata Labill
Mean temperature in 2002–2003 (1C)
Mean temperature in 2003–2004 (1C)
October–May
February–May
October–May
February–May
10.05 (70.26)
5.76 (70.47)
9.69 (70.30)
7.65 (70.57)
8.97 (70.23)
5.07 (70.43)
7.85 (70.28)
7.18 (70.58)
7.72 (70.26)
4.30 (70.40)
7.30 (70.25)
5.36 (70.40)
5.66 (70.26)
3.36 (70.40)
N/A
N/A
3.64 (70.28)
1.89 (70.38)
3.29 (70.24)
3.21 (70.29)
2.80 (70.23)
1.43 (70.37)
1.79 (70.24)
2.70 (70.28)
1.95 (70.20)
1.51 (70.39)
1.38 (70.20)
2.75 (70.30)
Mean temperatures (7 standard error) are given for the complete season (October–May) and the spring growth period (February–May). N/A— temperature logger damaged in shrubland fire.
ploughed agricultural areas, but the degree to which climatic limitations play a role in distributions is not known. Oxalis is also a good model species for studies of population dynamics. Although regularly producing flowers, it is a heterostylous outbreeder and only the short-styled morph is common in the Mediterranean (Lane, 1984). As a result, populations tend to be clonal and genetic variation is limited (Rottenberg and Parker, 2004). Vegetative plants die back completely during the dry season, and reproduce almost entirely by the propagation of subterranean bulbils (Clarke, 1934). Since the bulbils therefore represent the only investment that is effectively passed on to the next generation, their crop is a comprehensive indicator of annual performance and population viability (Vila` et al., 2006a).
Study area Field sites were located in the Lefka Ori (White Mountains), which reach 2452 m in western Crete. They are composed chiefly of limestone and experience a typical Mediterranean climate of mild, wet winters and hot, dry summers (Blondel and Aronson, 1999). Olive and citrus groves are cultivated at lower elevations to approximately 600 m. These give way to typical thermoMediterranean maquis, and above 900 m is sparse montane vegetation consisting of dwarf shrubs and prostrate herbs, with the exception of the fertile mountain plateau of Omalos at 1000 m a.s.l. (Rackham
and Moody, 1996). Seven sites at approximately 200 m altitudinal intervals from 200 m (351 24.102N, 231 56.456E) to 1400 m (351 18.265N, 231 54.506E) were selected along the road leading up to the Omalos plateau (Table 1), in order to determine the threshold zone for the survival of Oxalis populations. All sites had a similar northerly aspect.
Altitudinal gradient experiment At each of the seven sites, four experimental pots (15 cm diameter, 12 cm deep) were established, each containing five Oxalis bulbils collected from the same lowland olive grove (Megala Horafia: 351 26.987N, 241 07.628E). The three lowest sites were already colonised by Oxalis. Since sowing took place under field conditions, individual bulbils could not be weighed, but they were standardised in size, with one large (410 mm diameter), two medium (4–10 mm diameter) and two small (o4 mm diameter) sown in a matrix in each pot. The initial weight per replicate was therefore approximately constant and estimated from average mass of the three bulbil size classes. The pots were filled with commercially produced plant potting soil and buried to the brim at each site. Each pot was perforated with large holes to ensure free drainage and positioned under dense shrub vegetation, thus protecting it from grazing by large herbivores and ensuring a sheltered microclimate. These microsites were mostly under shrubs belonging to the Rosaceae so that leaf litter should be comparable. A data logger
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(Tinytag Plus, 30 1C to +50 1C, Gemini Data Loggers, Chichester, UK) was buried to 5 cm depth at each site, and used to record temperature at four hourly intervals. The first experiment was established on 6th September 2002 and revisited in November 2002 (‘‘Autumn 2002’’) and April 2003 (‘‘Spring 2003’’). At each visit, the plants were counted and in late May 2003, each pot was sifted for bulbils and the total biomass was taken to be the bulbil productivity. A second experiment was established the following year on 28th September 2003 to gauge inter-annual variation in plant performance. This second experiment followed the same design and the same sites as in the previous year with the exception of an additional treatment. To assess how changes in soil type influenced plant performance with increasing elevation, a further set of four pots containing five bulbils each was established at each of the seven sites but using soil indigenous to the site. The plants arising from the second experiment were counted and measured in November 2003 (‘‘Autumn 2003’’) and April 2004 (‘‘Spring 2004’’), and total bulbil biomass was assessed in late May 2004.
Statistical analysis Generalised linear models (GLMs) were used to describe how the growth responses of the plants were related to elevation and measurement date (+ interactions). These were solved by residual maximum-likelihood estimation using the GLIMMIX procedure in SAS/STAT 9.1 (SAS Institute Inc., 2002), with link functions and error distributions chosen as appropriate to each analysis. For survivorship, a binomial error with a logit link was used. For bulbil productivity, total bulbil biomass per pot was log transformed, and a normal distribution was assumed. In all cases, replicate was included as a random term and degrees of freedom were specified manually. From the temperature data, eight climatic variables were selected and GLMs were used to examine whether any of these could explain differences in plant performance. The dependent variable was the total bulbil biomass per pot (identity link function). The variables were mean temperature (1C), average minimum daily temperature (1C), total number of degree hours above 4 1C and the total number of hours of snow cover (where temperatures were below 0.1 1C), with each calculated for both the entire growth season (November–May) and the active spring growth phase only (February–May). All climate variables were normally distributed. Best-fit models were constructed using forward selection, starting with the variable displaying the highest explanatory power and testing all bivariate combinations, including interaction terms.
1 Proportion surviving
254
0.8 0.6 0.4
Autumn 2002 Spring 2003
0.2
Spring 2004
0 0
200
400
600 800 Altitude (m)
1000
1200
1400
Fig. 1. Survivorship of Oxalis along the altitudinal gradient.
Results Effect of elevation on plant survivorship The following analyses refer to the commercially produced plant potting soil treatment since this facilitated inter-annual comparisons. During the first experiment, a single replicate (one pot) was lost though grazing at the 400 and 600 m site. Data from the remaining pots highlighted that survivorship declined with increasing elevation despite a high degree of variability between replicates (F1,77 ¼ 50.4, po0.001; Fig. 1). In Autumn 2002, most plants survived up to 1400 m, but mortality was severe at higher elevations over the first winter. Over the comparatively mild winter of 2003–2004, mortality was greatly reduced, with at least 40% survivorship at all sites. The decline in survivorship with elevation differed significantly between the spring and autumn measurements (elevation season interaction in 2002–2003, F1,43 ¼ 10.8, p ¼ 0.002), and between the springs of 2003 and 2004 (elevation year interaction, F1,50 ¼ 10.3; p ¼ 0.002).
Effect of elevation on total bulbil biomass There was a significant decline in total bulbil biomass with elevation (F1,39 ¼ 42.7, po0.001) and the elevation year interaction was significant (F1,41 ¼ 12.9, p ¼ 0.001). Overall, biomass declined more steeply with increasing elevation in 2003 than in the milder 2004. According to the fitted trend, positive biomass replication, i.e. where the production of bulbil biomass was greater than the estimated initial biomass of sown bulbils, was achieved up to 740 m in 2002–2003 and 777 m in 2003–2004 (Fig. 2). The forced curves are intended mainly as a visual guide, but the true point of parity is undoubtedly close and differences between years are therefore relatively small. Our predictions suggest that differences in the climate severity raised the population viability threshold by 37 m.
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6
2002-03 2003-04
5
Bulbils, 2002-03
4 In (mean weight)
Mean bulbil biomass per pot (g)
L.C. Ross et al. / Perspectives in Plant Ecology, Evolution and Systematics 10 (2008) 251–258
Bulbils, 2003-04
2 0 -2 -4 -6 -8
0 0
200
400
600 800 Altitude (m) Ψ 37 m
1000
1200
1400
Fig. 2. Production of bulbil biomass along the altitudinal gradient. Values are mean totals per replicate (g dry weight), 7 standard error. A sigmoid curve was fitted to the altitudinal means by iteration, with the maximum asymptote forced as 5. The interpolated line indicates the estimated initial biomass of sown bulbils.
-10 0
100
200
300
400
500
600
Hours of spring snow
Fig. 3. Relationship between number of hours of spring snow and average bulbil biomass per pot.
snow, but less severely as the duration of snow cover increases subsequently (Fig. 3).
Effect of soil type on bulbil production
Discussion
Although plants were larger in the indigenous soil treatment (F1,22 ¼ 25.1, po0.001), this was only individually significant for the site at 1400 m (F1,4 ¼ 28.9, p ¼ 0.006). There was no significant elevation soil treatment interaction (F1,21 ¼ 2.23, p ¼ 0.15). Thus, over the course of a full season, plants generally fared better in the native substrate, especially at high elevations.
With increasing elevation, the survivorship and total bulbil biomass of Oxalis declined significantly. The trends remained similar irrespective of seasonal variation in climate, initial bulbil size or soil type. However, the different measures of performance suggested different patterns of population viability. Whereas survivorship was often high even at 1400 m, the replication threshold for bulbil biomass production was much lower, between 740 and 777 m. Above this elevation, population maintenance is apparently not sustainable in the long term, despite the short-term survival of plants and production of small bulbils at much higher elevations. The current elevation limit of Oxalis is around 100 m lower than this critical zone, which suggests that the availability of suitable habitat such as ploughed fields also contributes to the distribution limits, though climate clearly plays a significant role. Clearly the production of bulbils alone does not guarantee successful establishment of new populations, and a high propagule pressure is likely to be necessary for this to occur. The comparison of soil types in 2003–2004 showed that the plants in indigenous soil grew significantly better than those in nutrient-rich commercially produced plant potting soil. The reasons for this remain unclear. West Crete has shallow, clayey, water-retaining soil (Rackham and Moody, 1996) and this may have been of greater benefit to plant growth than the commercially produced plant potting soil that tends to dry out rapidly. Climatic factors would seem to be a key constraint in defining the limits of the distribution of Oxalis, in that survivorship improved substantially over the much milder second winter of the study. Other studies have also found that temperature has a large effect on the
Effect of climate on plant performance Overall, the season (October–May) of 2002–2003 was milder than that of 2003–2004 (Table 1). However, the spring growth period (February–May) of 2002–2003 was considerably colder than the equivalent period of the following year, with mean temperatures 2.1 1C lower at 400 m. The most marked differences in climatic variables were for snow lie, which, at 1400 m, persisted 2.68 times as long in 2002–2003 compared to 2003–2004. Snow was recorded at as low as 800 m in the first winter, but did not occur below 1000 m in the second winter. Of the climatic variables assessed, the number of hours of spring snow was most clearly distinct from the other factors (for bivariate correlations against the other spring variables r ¼ 0.64–0.83, and against the entireseason variables r ¼ 0.74–0.75). Spring snow proved to be the best correlate of changes in bulbil biomass, being the only significant explanatory variable in statistical models and no additional difference between years (year: F1,8 ¼ 1.14, p40.32; year elevation: F1,8 ¼ 3.5, p40.10). However, the overall fit displayed some non-linearity (r2 ¼ 0.67): performance is retarded strongly by a little
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germination and growth of the species (Peirce, 1979). The occurrence of snow lie seemed to coincide particularly well with the decline in performance, since both factors become evident at 800 m and increased rapidly with elevation above this level. However, the effect appeared to be much more strongly correlated with conditions in spring than across the entire season. The persistence of snow in this key period of flowering and bulbil production may be particularly important in inhibiting development, and thus may have a considerable impact on long-term survival. Previous authors have suggested that frost sensitivity may be a major limiting factor, mainly from examining the biogeographic distribution of the species (Clarke, 1934; Preston et al., 2002) and while low temperatures certainly play a part, length of snow lie appears a better explanatory variable in this study. This study highlights that an integrated performance function, such as population viability, is likely to be better reflection of the likelihood of invasion, and in common with other studies (McPeek and Peckarsky, 1998; Goldberg et al., 1999; Willis and Hulme, 2004; Weih and Nordh, 2005) illustrates that growth, fecundity or survival measures alone (e.g. Baret et al., 2004) do not provide adequate measures to predict likely distribution limits. Population viability thresholds in relation to alien distribution limits have previously been estimated only for two annual plants: Lactuca seriola (Carter and Prince, 1985) and Impatiens glandulifera (Willis and Hulme, 2002). The ultimate success of alien plant species depends not only on a positive rate of population increase, but also widespread dispersal (Pysˇ ek and Hulme, 2005) and the ecological constraints of the invaded community (Hulme, 2006). Oxalis was first introduced to Crete in 1880 (Rackham and Moody, 1996) and given its widespread dispersal in soil on agricultural machinery, is likely to have reached most cultivated areas suitable for establishment. Ploughed fields are scarce above 600 m on Crete, the exceptions being the 25 fertile montane plateaus above 850 m (Rackham and Moody, 1996). The absence of Oxalis from the cultivated mountain plateaus, often tilled with wheat and potatoes, is indicative of climatic constraints on plant establishment even though suitable habitat exists. Thus the current findings suggest that at present, Oxalis is restricted to the lowlands by both climate and land use, even though plants can tolerate reasonably extreme temperatures in the short term. However, with rising global temperatures, several studies have shown the advance of thermophilic species to higher elevations and the demise of specialised alpine communities unable to adapt to the altered conditions (Grabherr et al., 1994; Penuelas and Boada, 2003; Sanz-Elorza et al., 2003). It is therefore relevant to ask whether range expansions are likely to occur in Oxalis in the future. Our findings suggest that major expansions are unlikely in the
absence of land use change. The population viability threshold increased by less than 40 m between the 2 years despite a 2 1C difference in mean spring temperatures and much shorter snow lie in 2003–2004. This is equivalent to the expected average rise in Mediterranean winter temperatures by the year 2050 (Gritti et al., 2006). Thus, existing cultivated areas on montane plateaus above 850 m a.s.l. do not appear to face a particularly high risk of Oxalis invasion under expected future climatic warming. Although wild olives can be found growing at 1000 m a.s.l. on Crete (Rackham and Moody, 1996), the limit of economic cultivation is significantly lower. Intensification of olive cultivation in Crete, and across the Mediterranean, has been encouraged by subsidies from the European Union, leading to rapid landscape change (Allen et al., 2006). Thus, land use change could also be driven by climatic warming if olive cultivation becomes viable at higher elevations, facilitating the introduction of bulbils into new areas and creating suitable habitats, though this will also depend on availability of suitable soil, aspect and slope. In summary, the steep decline in bulbil production above 600 m reflects a switch from favourable growth conditions to an environment where growth appears to be strongly linked to climatic factors, particularly duration of spring snow lie. Range expansion seems to be restricted by these constraints, which operate at the level of population viability rather than plant survival. Therefore, in the absence of land use change at higher elevations, Oxalis is not likely to extend its altitudinal range markedly in the near future, even in the face of a warmer future climate. This conclusion would probably not have been possible through observational or bioclimatic analyses and emphasises the power of experimental approaches in the study of species distribution limits.
Acknowledgements Thanks to Laura Hayton, Louise Newell, Marie Pandolfo, Linda Turner and Laura Flegg for assistance with the fieldwork and data entry. We are grateful to Carsten Dormann, Ruth Mitchell, Antoine Guisan and two anonymous referees for their helpful comments on the manuscript. This study is part of the European Commission Fifth Framework Project EPIDEMIE (Exotic Plant Invasions: Deleterious Effects on Mediterranean Island Ecosystems), Contract number EVK2CT-2000-00074.
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Disentangling the roles of climate, propagule pressure and land use on the current and potential elevational distribution of the invasive weed Oxalis pes-caprae L. on Crete Louise C. Rossa,b,, Philip W. Lambdonb, Philip E. Hulmeb,c a
School of Biological Sciences, University of Aberdeen, Cruickshank Building, St Machar Drive, Aberdeen AB24 3UU, UK NERC Centre for Ecology and Hydrology, Hill of Brathens, Banchory, Aberdeenshire AB31 4BW, UK c National Centre for Advanced Bio-Protection Technologies, P.O. Box 84, Lincoln University, Canterbury, New Zealand b
Received 23 November 2006; received in revised form 11 June 2008; accepted 16 June 2008
Abstract Climatic warming and land use change are likely to facilitate range expansions in invasive plant species, although the ability to predict such changes requires a better mechanistic understanding of the biological limits of populations. The introduced weed Oxalis pes-caprae, a significant pest of cultivation in many Mediterranean-type ecosystems, presents a suitable case study. The species distribution in the Mediterranean Basin closely follows that of olive cultivation, limited to below 600 m; yet its potential to colonise vulnerable areas at higher elevations has yet to be adequately assessed. To investigate the possibility, plant performance was assessed by experimentally sowing O. pes-caprae bulbils along an altitudinal gradient in the Lefka Ori mountains, Crete. The survivorship and bulbil biomass of the resulting plants all declined significantly with elevation, irrespective of soil type, initial bulbil size or seasonal variation. Whilst plants survived vegetatively up to 1400 m, seasonal bulbil productivity, likely to be critical to population viability, exceeded that of the sown bulbil biomass only below 750 m. These data indicate that the current elevation of O. pes-caprae is close to, but not at, its current climatic limit, and that low propagule pressure and scarcity of suitable habitat probably also act to limit the altitudinal distribution. Plant performance was correlated strongly with the duration of spring snow cover. Despite a 2 1C difference in mean spring temperatures in the 2 years of study, the predicted elevational change was only 37 m higher in the milder conditions. Overall, our results suggest that while O. pes-caprae performance is strongly linked to climate and is currently close to its climatic limit on Crete, there is limited scope for further spread unless land use and/or propagule pressure change at higher elevations. For this species, these elements are likely to be more significant drivers of invasion risk than the predicted changes of future climates. r 2008 Ru¨bel Foundation, ETH Zu¨rich. Published by Elsevier GmbH. All rights reserved. Keywords: Altitude; Biological invasions; Climate change; Land use change; Population viability; Propagule pressure
Corresponding author at: School of Biological Sciences, University
of Aberdeen, Cruickshank Building, St Machar Drive, Aberdeen AB24 3UU, UK. Tel.: +44 7910385167; fax: +44 1224 272703. E-mail addresses: [email protected] (L.C. Ross), [email protected] (P.W. Lambdon), [email protected] (P.E. Hulme).
Introduction Invasions by non-native species often severely compromise the biodiversity, ecological functioning and economic value of invaded ecosystems (Mack et al., 2000; Hulme, 2006). Future global changes, such as
1433-8319/$ - see front matter r 2008 Ru¨bel Foundation, ETH Zu¨rich. Published by Elsevier GmbH. All rights reserved. doi:10.1016/j.ppees.2008.06.001
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climatic warming and an increased tendency towards human-dominated land use, are likely to favour invasive species and exacerbate their impacts (Dukes and Mooney, 1999; Vila` et al., 2006b). The Mediterranean region is often considered to be particularly susceptible to the combined effects of biological invasions and anthropogenic disturbance (Sala et al., 2000; Gritti et al., 2006); yet few experimental studies have attempted to examine the relationship between land use and climate on the distribution of alien species (Becker et al., 2005; Thuiller et al., 2006). Correlative models suggest that climate is a major constraint on the distribution of many alien plant species (e.g. Kriticos et al., 2005; Dunlop et al., 2006). Whilst several studies have suggested likely range shifts based on such analyses (e.g. McDougall et al., 2005; Thuiller et al., 2005; Gritti et al., 2006), the ecological processes that limit plant distribution often remain largely unknown. However, the power of correlative assessments is reduced when the species range is not at equilibrium with the current climate (Hulme, 2005), propagule dispersal is limited, or where environmental gradients (e.g. agricultural land use and climate) are spatially confounded (Willis and Hulme, 2002). Elevation appears to be an important correlate of alien species richness (Ullmann et al., 1995; Becker et al., 2005; McDougall et al., 2005) as well as distribution (Kitayama and Mueller-Dombois, 1995) and is often used as a proxy to explore the role of climatic limitation (Ko¨rner, 2007). Yet, low numbers of alien species at higher elevations may also reflect reduced propagule supply (Aragon and Morales, 2003), lower disturbance frequency (Kitayama and Mueller-Dombois, 1995) or simply the time since introduction (Becker et al., 2005). Thus, disentangling the relative importance of climate, habitat availability and propagule supply on the potential for invasion under a future warmer climate requires experimental rather than solely biogeographical (Thuiller et al., 2005) or observational (Becker et al., 2005; McDougall et al., 2005) approaches. Experimental sowing of species within and beyond their existing distributional range provides a means to assess the relative roles of climate, propagule supply and edaphic factors (e.g. soil type) on species abundance and performance (Carter and Prince, 1985; Willis and Hulme, 2002; Akasaka and Tsuyuzaki, 2005; Ramirez et al., 2006; Paiaro et al., 2007). Yet, in contrast to the numerous observational studies linking alien species elevational distributions to climatic limits (e.g. Kitayama and Mueller-Dombois, 1995; Aragon and Morales, 2003; Arevalo et al., 2005; Becker et al., 2005; Daehler, 2005; McDougall et al., 2005; Pauchard and Alaback, 2004), relatively few experimental approaches have been undertaken to examine alien plant species distributions along elevational gradients (Willis and Hulme, 2002; Akasaka and Tsuyuzaki, 2005; Paiaro et al., 2007).
In this study, experimental sowing of the Bermuda buttercup Oxalis pes-caprae L. (Oxalidaceae, hereafter Oxalis) along an elevation gradient on the Mediterranean island of Crete is used to examine the relative roles of climate, propagule supply and soil type on current distributional limits. While it is trivial to identify that climate presents an absolute limit to species elevational distribution, the key question is whether this physiological constraint coincides with the current limits. Thus the objective is to test whether the current distribution limit is absolute and determined uniquely by physiology through plant survivorship or is a demographic limit, reflecting constraints on plant population persistence. In the former case, the species response to future climatic changes may be predicted from a knowledge of bioclimatic surfaces or plant physiological models. Demographic limits are likely to occur at lower elevations than those imposed by physiological constraints and thus species response may also be conditional on changes to habitat suitability and propagule supply (Hulme, 2003). Oxalis is particularly well suited to these questions since it is a serious widespread economic weed of Mediterranean agriculture (Hulme et al, 2008), causes oxalate poisoning in livestock if eaten in sufficient quantities (Gimeno et al., 2006), and reduces both native species richness (Vila` et al., 2006c) and net primary production (Petsikos et al., 2007) where it occurs. The regional distribution is well described by bioclimatic niche models (Thuiller et al., 2005) and thus the responsiveness of Oxalis to climate will be essential information for predicting future risks and guiding management.
Materials and methods Study species Oxalis, a native to the Cape Region of South Africa, is an invasive alien weed in Italy, Greece, the Iberian Peninsula and North Africa, and beyond the Mediterranean basin in Portugal, south-west England, California, Florida, Australia, India and New Zealand (Vila` and Gimeno, 2007). The species was introduced to Crete in 1880 (Rackham and Moody, 1996), and is now prolific in anthropogenic habitats where the frequency of disturbance is high and the soil well-drained and fertile, especially in olive (Olea europaea ssp. europaea L.) groves and on other cultivated land (Rackham and Moody, 1996). The current distribution of Oxalis on Crete follows the boundaries of olive cultivation closely and has an altitudinal limit of 600 m above sea level (Turland et al., 1993), a pattern that is likely to have been facilitated by disturbances such as ploughing (Sala et al., 2007). Further colonisation is probably limited by poor dispersal of the bulbils away from
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Table 1.
253
Description of sites located along the elevation transect
Elevation (m)
186
459 606 781 1022 1190 1402
Vegetation type
Margins of olive grove, with Prunus dulcis (Mill.) D.A.Webb, Anagyris foetida L., Olea europaea Margins of olive grove, with Prunus dulcis, Olea europaea Dry grassland with scattered Pyrus spinosa Forssk., Olea europaea Sub-alpine shrubland, with Pyrus spinosa, Sarcopoterium spinosum (L.) Spach Pasture on Omalos plateau, heavily grazed by goats and sheep, with Pyrus spinosa Sub-alpine shrubland, with Pyrus spinosa, Berberis cretica L., Acer sempervirens L Alpine dwarf shrubland, with Acer sempervirens, Prunus prostrata Labill
Mean temperature in 2002–2003 (1C)
Mean temperature in 2003–2004 (1C)
October–May
February–May
October–May
February–May
10.05 (70.26)
5.76 (70.47)
9.69 (70.30)
7.65 (70.57)
8.97 (70.23)
5.07 (70.43)
7.85 (70.28)
7.18 (70.58)
7.72 (70.26)
4.30 (70.40)
7.30 (70.25)
5.36 (70.40)
5.66 (70.26)
3.36 (70.40)
N/A
N/A
3.64 (70.28)
1.89 (70.38)
3.29 (70.24)
3.21 (70.29)
2.80 (70.23)
1.43 (70.37)
1.79 (70.24)
2.70 (70.28)
1.95 (70.20)
1.51 (70.39)
1.38 (70.20)
2.75 (70.30)
Mean temperatures (7 standard error) are given for the complete season (October–May) and the spring growth period (February–May). N/A— temperature logger damaged in shrubland fire.
ploughed agricultural areas, but the degree to which climatic limitations play a role in distributions is not known. Oxalis is also a good model species for studies of population dynamics. Although regularly producing flowers, it is a heterostylous outbreeder and only the short-styled morph is common in the Mediterranean (Lane, 1984). As a result, populations tend to be clonal and genetic variation is limited (Rottenberg and Parker, 2004). Vegetative plants die back completely during the dry season, and reproduce almost entirely by the propagation of subterranean bulbils (Clarke, 1934). Since the bulbils therefore represent the only investment that is effectively passed on to the next generation, their crop is a comprehensive indicator of annual performance and population viability (Vila` et al., 2006a).
Study area Field sites were located in the Lefka Ori (White Mountains), which reach 2452 m in western Crete. They are composed chiefly of limestone and experience a typical Mediterranean climate of mild, wet winters and hot, dry summers (Blondel and Aronson, 1999). Olive and citrus groves are cultivated at lower elevations to approximately 600 m. These give way to typical thermoMediterranean maquis, and above 900 m is sparse montane vegetation consisting of dwarf shrubs and prostrate herbs, with the exception of the fertile mountain plateau of Omalos at 1000 m a.s.l. (Rackham
and Moody, 1996). Seven sites at approximately 200 m altitudinal intervals from 200 m (351 24.102N, 231 56.456E) to 1400 m (351 18.265N, 231 54.506E) were selected along the road leading up to the Omalos plateau (Table 1), in order to determine the threshold zone for the survival of Oxalis populations. All sites had a similar northerly aspect.
Altitudinal gradient experiment At each of the seven sites, four experimental pots (15 cm diameter, 12 cm deep) were established, each containing five Oxalis bulbils collected from the same lowland olive grove (Megala Horafia: 351 26.987N, 241 07.628E). The three lowest sites were already colonised by Oxalis. Since sowing took place under field conditions, individual bulbils could not be weighed, but they were standardised in size, with one large (410 mm diameter), two medium (4–10 mm diameter) and two small (o4 mm diameter) sown in a matrix in each pot. The initial weight per replicate was therefore approximately constant and estimated from average mass of the three bulbil size classes. The pots were filled with commercially produced plant potting soil and buried to the brim at each site. Each pot was perforated with large holes to ensure free drainage and positioned under dense shrub vegetation, thus protecting it from grazing by large herbivores and ensuring a sheltered microclimate. These microsites were mostly under shrubs belonging to the Rosaceae so that leaf litter should be comparable. A data logger
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(Tinytag Plus, 30 1C to +50 1C, Gemini Data Loggers, Chichester, UK) was buried to 5 cm depth at each site, and used to record temperature at four hourly intervals. The first experiment was established on 6th September 2002 and revisited in November 2002 (‘‘Autumn 2002’’) and April 2003 (‘‘Spring 2003’’). At each visit, the plants were counted and in late May 2003, each pot was sifted for bulbils and the total biomass was taken to be the bulbil productivity. A second experiment was established the following year on 28th September 2003 to gauge inter-annual variation in plant performance. This second experiment followed the same design and the same sites as in the previous year with the exception of an additional treatment. To assess how changes in soil type influenced plant performance with increasing elevation, a further set of four pots containing five bulbils each was established at each of the seven sites but using soil indigenous to the site. The plants arising from the second experiment were counted and measured in November 2003 (‘‘Autumn 2003’’) and April 2004 (‘‘Spring 2004’’), and total bulbil biomass was assessed in late May 2004.
Statistical analysis Generalised linear models (GLMs) were used to describe how the growth responses of the plants were related to elevation and measurement date (+ interactions). These were solved by residual maximum-likelihood estimation using the GLIMMIX procedure in SAS/STAT 9.1 (SAS Institute Inc., 2002), with link functions and error distributions chosen as appropriate to each analysis. For survivorship, a binomial error with a logit link was used. For bulbil productivity, total bulbil biomass per pot was log transformed, and a normal distribution was assumed. In all cases, replicate was included as a random term and degrees of freedom were specified manually. From the temperature data, eight climatic variables were selected and GLMs were used to examine whether any of these could explain differences in plant performance. The dependent variable was the total bulbil biomass per pot (identity link function). The variables were mean temperature (1C), average minimum daily temperature (1C), total number of degree hours above 4 1C and the total number of hours of snow cover (where temperatures were below 0.1 1C), with each calculated for both the entire growth season (November–May) and the active spring growth phase only (February–May). All climate variables were normally distributed. Best-fit models were constructed using forward selection, starting with the variable displaying the highest explanatory power and testing all bivariate combinations, including interaction terms.
1 Proportion surviving
254
0.8 0.6 0.4
Autumn 2002 Spring 2003
0.2
Spring 2004
0 0
200
400
600 800 Altitude (m)
1000
1200
1400
Fig. 1. Survivorship of Oxalis along the altitudinal gradient.
Results Effect of elevation on plant survivorship The following analyses refer to the commercially produced plant potting soil treatment since this facilitated inter-annual comparisons. During the first experiment, a single replicate (one pot) was lost though grazing at the 400 and 600 m site. Data from the remaining pots highlighted that survivorship declined with increasing elevation despite a high degree of variability between replicates (F1,77 ¼ 50.4, po0.001; Fig. 1). In Autumn 2002, most plants survived up to 1400 m, but mortality was severe at higher elevations over the first winter. Over the comparatively mild winter of 2003–2004, mortality was greatly reduced, with at least 40% survivorship at all sites. The decline in survivorship with elevation differed significantly between the spring and autumn measurements (elevation season interaction in 2002–2003, F1,43 ¼ 10.8, p ¼ 0.002), and between the springs of 2003 and 2004 (elevation year interaction, F1,50 ¼ 10.3; p ¼ 0.002).
Effect of elevation on total bulbil biomass There was a significant decline in total bulbil biomass with elevation (F1,39 ¼ 42.7, po0.001) and the elevation year interaction was significant (F1,41 ¼ 12.9, p ¼ 0.001). Overall, biomass declined more steeply with increasing elevation in 2003 than in the milder 2004. According to the fitted trend, positive biomass replication, i.e. where the production of bulbil biomass was greater than the estimated initial biomass of sown bulbils, was achieved up to 740 m in 2002–2003 and 777 m in 2003–2004 (Fig. 2). The forced curves are intended mainly as a visual guide, but the true point of parity is undoubtedly close and differences between years are therefore relatively small. Our predictions suggest that differences in the climate severity raised the population viability threshold by 37 m.
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6
2002-03 2003-04
5
Bulbils, 2002-03
4 In (mean weight)
Mean bulbil biomass per pot (g)
L.C. Ross et al. / Perspectives in Plant Ecology, Evolution and Systematics 10 (2008) 251–258
Bulbils, 2003-04
2 0 -2 -4 -6 -8
0 0
200
400
600 800 Altitude (m) Ψ 37 m
1000
1200
1400
Fig. 2. Production of bulbil biomass along the altitudinal gradient. Values are mean totals per replicate (g dry weight), 7 standard error. A sigmoid curve was fitted to the altitudinal means by iteration, with the maximum asymptote forced as 5. The interpolated line indicates the estimated initial biomass of sown bulbils.
-10 0
100
200
300
400
500
600
Hours of spring snow
Fig. 3. Relationship between number of hours of spring snow and average bulbil biomass per pot.
snow, but less severely as the duration of snow cover increases subsequently (Fig. 3).
Effect of soil type on bulbil production
Discussion
Although plants were larger in the indigenous soil treatment (F1,22 ¼ 25.1, po0.001), this was only individually significant for the site at 1400 m (F1,4 ¼ 28.9, p ¼ 0.006). There was no significant elevation soil treatment interaction (F1,21 ¼ 2.23, p ¼ 0.15). Thus, over the course of a full season, plants generally fared better in the native substrate, especially at high elevations.
With increasing elevation, the survivorship and total bulbil biomass of Oxalis declined significantly. The trends remained similar irrespective of seasonal variation in climate, initial bulbil size or soil type. However, the different measures of performance suggested different patterns of population viability. Whereas survivorship was often high even at 1400 m, the replication threshold for bulbil biomass production was much lower, between 740 and 777 m. Above this elevation, population maintenance is apparently not sustainable in the long term, despite the short-term survival of plants and production of small bulbils at much higher elevations. The current elevation limit of Oxalis is around 100 m lower than this critical zone, which suggests that the availability of suitable habitat such as ploughed fields also contributes to the distribution limits, though climate clearly plays a significant role. Clearly the production of bulbils alone does not guarantee successful establishment of new populations, and a high propagule pressure is likely to be necessary for this to occur. The comparison of soil types in 2003–2004 showed that the plants in indigenous soil grew significantly better than those in nutrient-rich commercially produced plant potting soil. The reasons for this remain unclear. West Crete has shallow, clayey, water-retaining soil (Rackham and Moody, 1996) and this may have been of greater benefit to plant growth than the commercially produced plant potting soil that tends to dry out rapidly. Climatic factors would seem to be a key constraint in defining the limits of the distribution of Oxalis, in that survivorship improved substantially over the much milder second winter of the study. Other studies have also found that temperature has a large effect on the
Effect of climate on plant performance Overall, the season (October–May) of 2002–2003 was milder than that of 2003–2004 (Table 1). However, the spring growth period (February–May) of 2002–2003 was considerably colder than the equivalent period of the following year, with mean temperatures 2.1 1C lower at 400 m. The most marked differences in climatic variables were for snow lie, which, at 1400 m, persisted 2.68 times as long in 2002–2003 compared to 2003–2004. Snow was recorded at as low as 800 m in the first winter, but did not occur below 1000 m in the second winter. Of the climatic variables assessed, the number of hours of spring snow was most clearly distinct from the other factors (for bivariate correlations against the other spring variables r ¼ 0.64–0.83, and against the entireseason variables r ¼ 0.74–0.75). Spring snow proved to be the best correlate of changes in bulbil biomass, being the only significant explanatory variable in statistical models and no additional difference between years (year: F1,8 ¼ 1.14, p40.32; year elevation: F1,8 ¼ 3.5, p40.10). However, the overall fit displayed some non-linearity (r2 ¼ 0.67): performance is retarded strongly by a little
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germination and growth of the species (Peirce, 1979). The occurrence of snow lie seemed to coincide particularly well with the decline in performance, since both factors become evident at 800 m and increased rapidly with elevation above this level. However, the effect appeared to be much more strongly correlated with conditions in spring than across the entire season. The persistence of snow in this key period of flowering and bulbil production may be particularly important in inhibiting development, and thus may have a considerable impact on long-term survival. Previous authors have suggested that frost sensitivity may be a major limiting factor, mainly from examining the biogeographic distribution of the species (Clarke, 1934; Preston et al., 2002) and while low temperatures certainly play a part, length of snow lie appears a better explanatory variable in this study. This study highlights that an integrated performance function, such as population viability, is likely to be better reflection of the likelihood of invasion, and in common with other studies (McPeek and Peckarsky, 1998; Goldberg et al., 1999; Willis and Hulme, 2004; Weih and Nordh, 2005) illustrates that growth, fecundity or survival measures alone (e.g. Baret et al., 2004) do not provide adequate measures to predict likely distribution limits. Population viability thresholds in relation to alien distribution limits have previously been estimated only for two annual plants: Lactuca seriola (Carter and Prince, 1985) and Impatiens glandulifera (Willis and Hulme, 2002). The ultimate success of alien plant species depends not only on a positive rate of population increase, but also widespread dispersal (Pysˇ ek and Hulme, 2005) and the ecological constraints of the invaded community (Hulme, 2006). Oxalis was first introduced to Crete in 1880 (Rackham and Moody, 1996) and given its widespread dispersal in soil on agricultural machinery, is likely to have reached most cultivated areas suitable for establishment. Ploughed fields are scarce above 600 m on Crete, the exceptions being the 25 fertile montane plateaus above 850 m (Rackham and Moody, 1996). The absence of Oxalis from the cultivated mountain plateaus, often tilled with wheat and potatoes, is indicative of climatic constraints on plant establishment even though suitable habitat exists. Thus the current findings suggest that at present, Oxalis is restricted to the lowlands by both climate and land use, even though plants can tolerate reasonably extreme temperatures in the short term. However, with rising global temperatures, several studies have shown the advance of thermophilic species to higher elevations and the demise of specialised alpine communities unable to adapt to the altered conditions (Grabherr et al., 1994; Penuelas and Boada, 2003; Sanz-Elorza et al., 2003). It is therefore relevant to ask whether range expansions are likely to occur in Oxalis in the future. Our findings suggest that major expansions are unlikely in the
absence of land use change. The population viability threshold increased by less than 40 m between the 2 years despite a 2 1C difference in mean spring temperatures and much shorter snow lie in 2003–2004. This is equivalent to the expected average rise in Mediterranean winter temperatures by the year 2050 (Gritti et al., 2006). Thus, existing cultivated areas on montane plateaus above 850 m a.s.l. do not appear to face a particularly high risk of Oxalis invasion under expected future climatic warming. Although wild olives can be found growing at 1000 m a.s.l. on Crete (Rackham and Moody, 1996), the limit of economic cultivation is significantly lower. Intensification of olive cultivation in Crete, and across the Mediterranean, has been encouraged by subsidies from the European Union, leading to rapid landscape change (Allen et al., 2006). Thus, land use change could also be driven by climatic warming if olive cultivation becomes viable at higher elevations, facilitating the introduction of bulbils into new areas and creating suitable habitats, though this will also depend on availability of suitable soil, aspect and slope. In summary, the steep decline in bulbil production above 600 m reflects a switch from favourable growth conditions to an environment where growth appears to be strongly linked to climatic factors, particularly duration of spring snow lie. Range expansion seems to be restricted by these constraints, which operate at the level of population viability rather than plant survival. Therefore, in the absence of land use change at higher elevations, Oxalis is not likely to extend its altitudinal range markedly in the near future, even in the face of a warmer future climate. This conclusion would probably not have been possible through observational or bioclimatic analyses and emphasises the power of experimental approaches in the study of species distribution limits.
Acknowledgements Thanks to Laura Hayton, Louise Newell, Marie Pandolfo, Linda Turner and Laura Flegg for assistance with the fieldwork and data entry. We are grateful to Carsten Dormann, Ruth Mitchell, Antoine Guisan and two anonymous referees for their helpful comments on the manuscript. This study is part of the European Commission Fifth Framework Project EPIDEMIE (Exotic Plant Invasions: Deleterious Effects on Mediterranean Island Ecosystems), Contract number EVK2CT-2000-00074.
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