Going against the flow: potential mechanisms for unexpected downslope range shifts in a warming climate

Abstract

In as much as the elevation gradient in species composition is often thought to be driven by the corresponding temperature gradient, species ranges are both expected and predicted to shift upward in response to climate warming. Indeed, there are numerous reports of species moving towards higher elevations in response to the rising temperatures for both animals (Konvicka et al. 2003, Tryjanowski et al. 2005, Wilson et al. 2005, Franco et al. 2006, Hickling et al. 2006, Moritz et al. 2008, Raxworthy et al. 2008, Chen et al. 2009) and plants (Klanderud and Birks 2003, Walther et al. 2005, Pauli et al. 2007, Kelly and Goulden 2008, Lenoir et al. 2008, Parolo and Rossi 2008, Vittoz et al. 2008, Lenoir et al. 2009), and the evidence for significant upslope migrations now seems overwhelming regardless of the position along latitudinal (Klanderud and Birks 2003, Konvicka et al. 2003, Wilson et al. 2005, Raxworthy et al. 2008, Chen et al. 2009) or elevational (Walther et al. 2005, Pauli et al. 2007, Kelly and Goulden 2008, Lenoir et al. 2008, Vittoz et al. 2008, Lenoir et al. 2009) gradients. Due to this empirical evidence and, perhaps, the intuitive expectation of rising elevational ranges as a consequence of a warming climate, ecologists have primarily focused on elaborating on the mechanisms and consequences of such upslope shifts including (Colwell et al. 2008): 1) biotic attrition in the lowland tropics, 2) gaps between current and projected elevational ranges (range-shift gaps), and 3) mountaintop extinctions in the long-term. However, most of the studies that reported expected range shifts towards higher elevations have detected species moving towards lower elevations as well. Table 1 provides an illustrative, non-comprehensive survey of such studies from the recent years: in summary they demonstrate that ca 65% of the species have shifted their mid-range positions upslope, 10% have not changed their mid-range positions, and 25% have shifted their mid-range positions downslope (Table 1). In addition, according to a global review of the literature published until the beginning of the 21st century (Parmesan and Yohe 2003) ca 20% of the species have adjusted their ranges towards lower elevations and/or southern latitudes. Hence, a considerable fraction of the investigated species has shown range shifts that are inconsistent with the forecasted effects of climate warming. These downslope movements seem very unlikely to occur as a direct consequence of rising temperatures, but the potential mechanisms involved have received little attention. Stochastic fluctuations in the positions of individuals, or populations, together with measurement errors, represent one such potential “mechanism”. However, many, though not all of the studies reporting downslope shifts have explicitly tested the observed changes in single species’ ranges for significant deviation from random fluctuations. For plants, significant downslope shifts have been reported for 5 of 46 species displaying significant mid-range shifts between the periods 1905–1985 and 1986–2005 (Table S2 in Lenoir et al. (2008)). For reptiles and amphibians, Raxworthy et al. (2008) have found significant downslope shifts for 2 of 7 species displaying significant mid-range shifts between 1993 and 2003. For birds, Archaux (2004) has reported significant downslope shifts for 5 of 8 species displaying significant mid-range shifts between the 1970s and the 2000s. However, it could be argued that starting from the near-consensual report of a general and strong upward shift signal in species mid-range positions along the elevation gradient, the relevant random distribution of species mid-range shifts for testing the occurrence of significant downslope movements should be centred around some expected upslope shift, according to the observed climatic trends, rather than around zero (i.e. a null expectation of constant distributions). Indeed, the relevant question is: which proportion of species would we expect to shift their mid-range position downslope by chance alone (i.e. due to random population fluctuations, data idiosyncrasies, and observer errors) despite an average upslope trend of z m? This proportion is highly dependent on the variation in mid-range shifts caused by such “stochastic processes” alone (Fig. 1): the narrower this variability, the lower the proportion of species likely to show such stochastic downslope shifts. However, if random fluctuations and observer errors do not fully explain the observed downslope shifts, what mechanisms might then drive these unexpected range changes? Null expectation of the proportion of downslope mid-range shifts despite an average upslope trend of z m for (a) narrower range of random variation and (b) wider range of random variation. Broken curves represent the observed distribution of shifts in species mid-range elevation from a colder to a warmer period. Unbroken curves represent the random distribution in species mid-range elevation within a single statistical population. The gray filling illustrates the expected proportion of random downslope shifts in mid-range positions in the absence of climate change (50%). The black filling illustrates the expected proportion of random downslope shifts in mid-range positions despite a warming-driven upslope trend of z m (<50%). The vertical broken line displays the average upslope trend of z m. One potential mechanism is land-use-related habitat modification, which has already been shown to cause downslope range shifts in particular settings (Hättenschwiler and Körner 1995, Archaux 2004). In addition, however, such shifts may also result from changes in species interactions (facilitation, competition, and predation) in response to climate warming (Hughes 2000). Here, we propose a conceptual and testable model that explains the observed downslope shifts of species as resulting from the effects that both climate and land use change, separately or in concert, might have on species interactions. We start from the proposition that species are often limited by physical stresses at one margin, but by biotic interactions at the other, more favourable, margin of their distribution along environmental gradient (McArthur 1972, Connell 1978, Brown et al. 1996, Brown and Lomolino 1998, Leathwick and Austin 2001, Normand et al. 2009). We then argue that both climate warming and land-use-related habitat modification may increase levels of disturbance in these ecosystems leading to: 1) a transient reduction of the importance of competition as a limiting factor on species distributions; and 2) an associated potential range expansion towards lower elevations for species whose lower elevation margin was previously strongly limited by competition. Climate warming may not only affect species distributions via altering abiotic conditions but also by changing the importance or intensity of species interactions (Hughes 2000, Brooker 2006). Indeed, it has been demonstrated that changes in species interactions may override autecological responses to a changing climate and even reverse community trajectories (Suttle et al. 2007). Before explaining our model which is based on such changes in species interactions, we would like to pinpoint the two most important conceptual cornerstones it rests upon. First of all, the lower-margin-competition versus higher-margin-stress limitation concept (McArthur 1972, Connell 1978, Brown and Lomolino 1998) suggests competitive effects as the major mechanism for setting the lower limit of species’ elevational ranges. More generally, the importance of competition is thought to increase as environmental severity decreases, a theory known as the stress-gradient hypothesis in plant ecology (Bertness and Callaway 1994, Callaway and Walker 1997, Brooker et al. 2005, Maestre et al. 2009). This concept might be less applicable towards the lowest elevations of the lowest latitudes in subtropical to tropical areas, where temperature and water stress vary in opposite directions, and where lower range margins may be relatively often set by drought-induced stress (Normand et al. 2009). However, the stress-gradient hypothesis appears generally valid in elevational ranges where the macroclimate does not present drought-induced stress gradients that complicate the effect of the elevational gradient (Callaway 1998, Callaway et al. 2002). Thus, this concept will apply to many mountainous regions, notably in moist temperate and tropical areas. As a corollary, many species in such systems will likely be characterized by realised climatic niches being smaller than fundamental ones (Vetaas 2002) in particular towards lower elevations (due to biotic interactions). For example, Vetaas (2002) has suggested that competition plays an important role in constraining the climatic ranges of four Himalayan Rhododendron species in their native habitat as compared to their climatic ranges in ornamental gardens and arboreta, three of which being able to grow there under a far wider range of climatic conditions (generally warmer). Therefore, any mechanism that alleviates competitive exclusion is likely to induce changes in species realised distributions. Secondly, the importance of competition in structuring communities is likely reduced by increased levels of disturbance (Dayton 1971, Connell 1978, Huston 1979, McAuliffe 1984, Brooker and Callaghan 1998, Brooker 2006). Thus, if climate warming increases disturbance levels within a specific ecosystem, it is reasonable to expect that it will, to a certain degree, relax the role of competition as a selective filter for community assembly. Indeed, climate warming affects ecosystems stochastically through an increasing frequency and intensity of events such as drought-induced insect outbreaks (Allen et al. in press), heat-induced wildfires (Schumacher and Bugmann 2006), windthrows (Usbeck et al. in press), and permafrost degradations (Cannone et al. 2007). All these climatic-extremes-induced effects can be viewed as disturbances under definitions such as destruction of plant biomass (Grime 1979), cause of mortality (Huston 1979), and disruption of ecosystem, community or population structure (Pickett and White 1985). Indeed, the increasing frequency of climatic extremes, indicated by changes in the interannual variability around mean values of climate parameters, have already been reported to influence species range margins (Zimmermann et al. 2009). The interplay between the idea of disturbance-related release from competition and the above-mentioned stress-gradient hypothesis gives the key to understanding potential downslope range shifts despite climate warming. We start outlining our conceptual model by restricting the temperature-elevation-stress relationship to elevational ranges where heat and drought have hardly any impacts, e.g. from temperate montane to alpine ecosystems (Fig. 2a). Following the stress-gradient hypothesis, the importance of competition is therefore likely to decrease upwards along the elevation gradient (Fig. 2b), from favourable abiotic conditions at low elevations (warmer conditions) to harsh abiotic conditions at high elevations (cold damage during winter, reduced energy during the growing season). To simplify matters in our conceptual model, we distinguish between two illustrative species with exactly the same realised distribution along the elevation gradient (as defined from their realised niche), but differing in the way they fill their potential distribution area (as defined from their fundamental ecophysiological niche) (Fig. 2c, d). Hereafter, we will consistently refer to the “potential distribution” as the range corresponding to the species’ fundamental ecophysiological niche, and to the “realised distribution” as the range corresponding to the species’ realised niche. The first illustrative species is strongly limited at the lower margin of its elevational distribution by competitors from below (low “realisation” of the potential distribution), whereas the second one is much less limited by biotic interactions (high “realisation” of the potential distribution). It is difficult to infer the physiological climatic requirements of these two species from their actual range since their elevational distributions are identical. Nevertheless, they might respond differently to climate warming because of this distinct “realisation” of their ecophysiological range. Conceptual model of changes in species’ elevational distributions in response to climate warming. Panels depict: (a) the general decreasing trend in mean annual temperature along the elevation gradient, and an overall warming between two periods; (b) the general decrease in the importance of competition along a gradient of environmental severity represented by the elevation gradient, and the potential impact of warmer conditions on the relationship between elevation and the importance of competition; (c) the realised and the potential distributions along the elevation gradient for a species strongly limited by competitors from below, and the potential upslope and/or downslope range shifts of the realised distribution due to both climate warming and competitive release; (d) the realised and the potential distributions along the elevation gradient of a species less limited by competitors from below, and the resulting upslope range shift of the realised distribution due to climate warming (competitive release does not allow shifts towards lower elevations that are no longer climatically suitable); and (e) all the resulting combinations of changes in species elevational distributions involving contraction, expansions, or both simultaneously, and the observed proportions of species displaying upward, stable, and downward shifts in elevation in response to recent climate warming. Blue colours represent initial conditions before climate warming, whereas red colours represent changed conditions after an increase in temperatures. Red broken lines represent the impact of a reduction in the importance of competition after climate warming. The elevation gradient considered in our conceptual model ranges from temperate montane to alpine ecosystems where heat and drought have hardly any impact. Let us now introduce the effect of climate warming in our conceptual model (red colours in Fig. 2). As argued above, warming-induced disturbances are likely to transiently reduce the importance of competition along the elevation gradient (Fig. 2b). Simultaneously, climate warming is likely to shift species’ potential distribution along the elevation gradient towards higher elevations (Fig. 2c, d). However, the transient reduction in the importance of competition at the lower margin of a species’ elevational distribution is likely to particularly benefit species that currently have a greater part of their potential distribution unfilled because of competition. For such species, climate warming allows range expansion towards lower elevations from which they had hitherto been competitively excluded (Fig. 2c). In contrast, species which are currently little limited by competition and largely fill their potential distribution areas along the elevation gradient will not be able to move downwards due to the upward shift of habitats climatically suitable to them (Fig. 2d). Figure 2e gives a full account of the climatically driven range shifts along the elevation gradient conceivable under this model. To sum up, species with a low “realisation” of their potential distribution areas along the elevation gradient are especially good candidates for downslope shifts, if they additionally have good dispersal abilities and a wide fundamental climatic niche. For example, Vetaas (2002) has suggested that Rhododendron species with their lower margins hitherto set by competition can grow under warmer climatic conditions, i.e. expand towards lower elevations. Additionally, species mid-range shifts might result not only from expansions at range margins alone, but also from changes in species local abundance (Fig. 2e). For example, species with low competitive abilities, but a wide potential distribution along the elevation gradient associated with a high degree of plasticity (Fig. 2c) might be already present downwards as remnant populations living at environmental extreme sites where the competitive species are excluded by abiotic factors (Eriksson 2000). In this latter case, downslope mid-range shifts might simply result from an increasing abundance of the species with these outlier populations acting as “expansion foci”. Finally, we note that downslope range shifts under this model would be likely to be temporary, as the importance of competition may become reasserted if climate change slows down or come to a halt, while species will eventually be forced upwards in elevation if climate change continues and conditions at lower elevations shift beyond the fundamental climatic niche of the species. Species may also shift downslope as a direct consequence of habitat modification, with or without involving competitive release, either following natural disturbances (windthrows, fires, and avalanches), human-induced disturbances or permanent habitat changes (recreational activities, land use changes, and management practices), or due to other local changes in habitat suitability. For example, in the Swiss Central Alps, Hättenschwiler and Körner (1995) have suggested that the cessation of forest cattle grazing and the high level of nitrogen deposition may have led to denser and more exuberant ground vegetation, thereby enhancing the replacement of Pinus sylvestris seedling populations by those of P. cembra below the present lower margin of P. cembra adult trees. Similarly, Archaux (2004) has suggested that the increase of conifer areas at the expense of broad-leaved trees due to changes in forest management might cause both coniferous- and deciduous-forest bird species to shift their mean elevation downwards. We note that habitat modification in conjunction with climate warming may explain upslope range shifts as well. As an illustration, in the Swiss Alps, Gehrig-Fasel et al. (2007) have reported that >90% of upslope shifts in the local tree line are due to ingrowth and the filling of gaps indicating that land use is the primary driver over climate warming in many instances, although the two drivers may also act in combination. In a conceptual model involving climate change and herbivory pressure, Cairns and Moen (2004) have highlighted a potential pathway for the interaction of both climate change and herbivore on tree line fluctuations leading to upslope a or of tree Hence, habitat modification has often been to be an important driver of elevational range shifts, acting in with climate warming or even it (Hättenschwiler and Körner 1995, Archaux Cairns and Moen Gehrig-Fasel et al. 2007, Vittoz et al. 2009). Nevertheless, habitat modification may increased disturbance levels and thereby cause release from competition of climate warming, but with effects on species’ elevational distributions. disturbances are likely to be more in lowland areas, however, a generally increasing degree of habitat modification towards lower elevations of most mountainous settings et al. the reduction in the importance of competition due to disturbances should be more important range expansions of the realised distribution of species towards lower elevations as as climatically suitable sites are down below their lower Therefore, species that fill only part of their potential distribution areas along the elevation gradient (Fig. 2c) are more likely to shift downwards in response to habitat modification alone, especially if their potential distribution areas do not shift For example, it has been suggested that destruction and the from competitive from below, has alpine and species in to increase their elevational distributions downwards and Let us now a more of the effects of climate warming and habitat the one habitat modification may act in with climate warming to cause a reduction in the importance of competition at the lower margin of a species’ elevational distribution and to allow a potential downslope shift in its mid-range position due to potential expansions at the margin (Fig. 2e). This is especially for species that fill only part of their potential distribution areas along the elevation gradient (Fig. 2c). the other habitat modification may upslope range expansions due to climate warming or even cause at the higher margin of a species’ elevational distribution (Fig. 2e). For example, species may to climatically suitable areas at the higher margins of their elevational distributions if they are by habitat et al. 2002). Additionally, other factors such as towards (Colwell et al. limited dispersal et al. et al. and 2006), and/or may or at warming-induced upslope shifts. Finally, natural habitat modification may warming-induced upslope shifts through unexpected of at the higher margins of species’ elevational distributions (Fig. 2e). For example, et al. (2007) have suggested that warming-induced permafrost degradations at high elevations may habitat in the of and unexpected of in m. This that upslope migrations to species (Cannone et al. 2007). to upslope migrations are with in species extinctions at the lower margins of species distributions have been reported to be more than at the higher margins et al. 2005, 2007, Kelly and Goulden 2008, Moritz et al. 2008, Lenoir et al. 2009). This may result in no upslope but rather in local changes in species abundance over and 2009). In such shifts may more than do shifts associated with both and The resulting is a transient upslope et al. The of a species towards higher elevations may to for the at lower elevations leading to transient in species or biotic attrition not only at lower elevations (Colwell et al. but the elevation gradient (Fig. 2 in Wilson et al. This is transient and, is likely to a of for highly and species that might shift either upslope or downslope to fill the gaps either by climate warming or habitat a communities with reduced of species, and by more and species et al. frequency of windthrows during the (Usbeck et al. in is one of disturbances that is likely to of for species with a high degree of Thus, habitat strongly with climate warming and to competitive release even towards lower downslope range shifts of some species more likely than with climate warming downslope range shifts could be driven by changes in other of climate than mean e.g. water or in climate These of climate variability may influence species range margins (Zimmermann et al. 2009), and more interactions are likely to cause unexpected range shifts in response to climate warming. high for example, warmer temperatures may decrease the and may cause damage at the higher margin of a species’ elevational which in may the competitive effect of this species on other ones towards lower elevations (Fig. 2c). the competitive that this species on the distributions of the species will likely become less Additionally, the towards areas by upslope competitive species is likely to occur both from and This should result in some species upslope and and even towards both without changing in their mid-range position (Fig. 2e). Therefore, interactions may also cause downslope range shifts, but before other competitors to our null the proportion of random downslope mid-range shifts despite an average upslope trend of z m is dependent on the range of random variation shifts (Fig. 1). We data from a on the shifts in the elevational position of plant species’ of et al. to this range of random variation shifts and then the proportion of random downslope mid-range shifts despite an average upslope trend of z m. found an average upslope trend of plant species, between a 1905–1985 and a 1986–2005 for To the range of random variation shifts, we two random by forest from the 1905–1985 by Lenoir et al. the increasing trend in mean annual temperature and the have since the et al. we to our two random from the first to potential strong in climatic conditions between the two Indeed, it was important that the two represented an range of environmental We then the same as in Lenoir et al. (2008) to species elevation for of the species in of the two The elevational position was between the lowest and the elevations in the 1905–1985 However, of the in species elevation between two we the in species elevation between two from the same to the distribution of in expected from We this the and in 2009). the we found a mean in species elevation of m and a for mean at from m to m Finally, to the proportion of downslope mid-range shifts expected at random despite an average upslope trend of m in forest plants, we simply for of the the distribution of random in m i.e. to the by m to the of shift (Fig. We then the expected proportion of random downslope shifts, despite an average upslope trend of as the proportion of shifts in the of the at m shift gray in Fig. the (Fig. we found a proportion of of species expected to have below the 1905–1985 elevational by chance alone, which is the proportion of downslope shifts we found between 1905–1985 and 1986–2005 et al. Thus, the of species found to move downwards along the elevation gradient is as high as expected by chance under the observed general upward We note that this proportion of species the is higher than the of species with significant downslope shifts found species elevation tested for significant from a constant species elevation expectation (Table S2 in Lenoir et al. (2008)). However, this the of the we for testing in species along the elevation gradient et al. of (a) observed and random in along the elevation gradient for plant species published data from et al. the distribution of random in a single illustrative of the and (b) distribution of the proportion of random downslope mid-range shifts despite an average upslope trend of m for the gray represent the observed shifts in species elevation between 1905–1985 and represent the distribution of random shifts in species by two from the 1905–1985 after this distribution m upslope, i.e. to the for gray represent the proportion of downslope mid-range shifts expected at despite an average upslope trend of m. The vertical broken line displays the average upslope trend of m. The vertical broken line displays the proportion of random downslope mid-range shifts despite an average upslope trend of m for the single illustrative of the The forest plant species displaying significant downslope shifts despite an average upslope trend of m are and of these species have by and the of are and with the while is by et al. Hence, four of these species have dispersal most likely an important for downslope range shifts despite climate warming. has low dispersal abilities and a distribution between and it also in the down to m in et al. Thus, might represent a species strongly limited by competitors from below (Fig. 2c). Additionally, and to a and are highly to i.e. by we do not to our conceptual model with these we note that these downslope species have a of them likely to respond to climate change in a way by our model. However, a much more empirical testing of this model is We that downslope range shifts of species may an biotic response to both climate warming and habitat modification rather than random effects due to stochastic fluctuations in population distributions or observer The concept should become part of a general for studies of changes in species distributions in response to climate warming. In our conceptual model, we on a for change, that downslope shifts primarily occur for species that are strongly limited by competition at their lower elevation range margin, and therefore have a realised distribution that do no fill their potential distribution areas along the elevation To this hypothesis, one could two of one set of species that have shifted downslope and set of species that have shifted One could then their realised distribution in their natural habitats with their potential distribution areas additionally by or In such an we would expect between the realised and the potential distributions along the elevation gradient for the set of species that have shifted downslope range shifts, particularly where driven by warming-induced competitive release, should be only we the to the hitherto downslope range shifts of species more explicitly of the effects of climate change on species distributions. We are to the numerous data and to and the for particularly and We and for and many and We from the for the of the to and and the to