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Climate Change, Aboveground-Belowground Interactions, and Species Range Shifts
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Wim H. Van der Putten
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Department of Terrestrial Ecology
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Netherlands Institute of Ecology (NIOO-KNAW) / Laboratory of Nematology, Wageningen
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University
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P.O. Box 50, 6700 AB / PO Box 8123, 6700 ES
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Wageningen, The Netherlands
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Email w.vanderputten@nioo.knaw.nl
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Details :
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Abstract 150 words
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Main text : 7087
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Figure legends 300 words
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References 108
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No. Figures 2
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No Tables or photographs : 0
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No pages : 37
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Abstract
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Changes in climate, land use, fire incidence, and ecological connections all may contribute to
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current species range shifts. Species shift range individually, and not all species shift range at the
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same time and rate. This will cause community reorganization in both the old and new range. In
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terrestrial ecosystems, range shifts will alter aboveground-belowground interactions, influencing
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species abundance, community composition, ecosystem processes and services, and feedbacks
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within communities and ecosystems. Thus, range shifts may result in no-analog communities
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where foundation species and community genetics play unprecedented roles, possibly leading to
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novel ecosystems. Long-distance dispersal can enhance the disruption of aboveground-
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belowground interactions of plants, herbivores, pathogens, symbiotic mutualists, and decomposer
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organisms. These effects most likely will be stronger for latitudinal than for altitudinal range
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shifts. Disrupted aboveground-belowground interactions may have influenced historical post-
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glacial range shifts as well. Assisted migration without considering aboveground-belowground
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interactions could enhance risks of such range-shift induced invasions.
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Key words: climate warming, extinction, invasiveness, geographic range, multitrophic
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interactions, no-analog communities
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Introduction
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A range, or distribution, is the geographical area where a species can be found. The range is
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determined by a large number of environmental factors, including climate, soil type and species
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interactions. Over geological time scales, adaptive radiation, speciation and plate tectonics can
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also influence the range of a species. A species range can shift by one or more changes in the
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environmental conditions, for example climate warming, land use change, new ecological
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connections, or artificial introduction in a new environment. Nevertheless, many reports on
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current massive range shifts of species towards higher altitudes and latitudes suggest that climate
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warming is a key driving factor (Grabherr et al. 1994, Walther et al. 2002, Parmesan & Yohe
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2003, Parmesan 2006, Walther 2010). When land use change would have been the main driver,
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species range shifts should have occurred in more directions.
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Compared to historical geographic range shifts, such as those that have taken place
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during glaciation-deglaciation cycles over the past 2 million years (Bush 2002), the rate of current
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climate warming is unprecedented (Walther et al. 2002). The first reports suggested that many
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species fail to keep up with climate warming (Warren et al. 2001, Thomas et al. 2004, Thuiller et
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al. 2005). However, more recent studies suggest that at least some species might respond
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adequately to climate warming by shifting their ranges (Chen et al. 2011) and that a number of
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species can reach enhanced dominance in the new range (Walther et al. 2002, Tamis et al. 2005,
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Engelkes et al. 2008). Thus far, most predictions on range shifts have been made independent of
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species interactions and the question is whether including species interactions may change the
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outcome of the model predictions (Lavergne et al. 2010, Van der Putten et al. 2010).
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Species abundance can be influenced by resource availability, predation, propagule
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availability, symbioses, competition and facilitation. As all these factors may vary between the
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old and new range, species that can move may not necessarily encounter suitable circumstances
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for establishment, growth and reproduction. Moreover, these factors may also vary during time
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since introduction, which can affect community composition in a dynamic way. Species
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interactions can drive, or be subject of evolution, such as can be seen in highly specialized
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pollination or parasitism patterns, or in other symbiotic mutualisms. These evolutionary processes
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may also be disrupted by climate change, whereas new evolutionary processes may be initiated
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(Lavergne et al. 2010).
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Besides range shifts, species may also respond to climate warming and other
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environmental changes via adaptation of local populations to changing environmental conditions.
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For example, there is scope for genetic adaptation of plants to climate warming, but there are also
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limitations that may contribute to diversity loss (Jump & Peñuelas 2005). Climate warming is
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highly multi-dimensional. Local effects of climate warming may be due to changes in
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temperature, precipitation, or length of growing season. Species that shift range also will be
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exposed to different day length (Jump & Peñuelas 2005). It is not well known how adaptation and
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migration interact during range shifts (Lavergne et al. 2010).
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Terrestrial ecosystems are composed of aboveground and belowground subsystems,
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which have been examined separately for many years, whereas the different subcomponents
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clearly interact with each other (Wardle 2002). Plants connect the aboveground and belowground
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subsystems and interactions belowground can, directly or indirectly, influence aboveground
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interactions vice versa. Species in these aboveground and belowground subsystems are differently
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susceptible to climate warming (Berg et al. 2010), leading to – at least temporarily – new species
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combinations in the new range. As aboveground-belowground interactions have the potential to
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impose selection on plants (Schweitzer et al. 2008), range shifts may influence selection and
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adaptation. In spite of the rapidly increasing interest in the subject of aboveground-belowground
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interactions, climate warming-induced range shift effects have been poorly studied thus far
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(Bardgett & Wardle 2010). In this article, I will combine reported knowledge on range shifts with
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information on the functional role of aboveground-belowground species interactions in
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community organization and ecosystem processes.
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Belowground subsystems include biota that interact with plants directly (herbivores,
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pathogens and symbionts), or indirectly (natural enemies of the directly interacting species and
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components of the decomposer subsystem). These direct and indirect interactions with plant roots
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can influence aboveground biota, and can result in effects that feed back to the soil subsystem
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(Wardle et al. 2004). Expanding from a previous review where it was argued that trophic
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interactions need to be taken into account when predicting consequences of climate warming
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(Van der Putten et al. 2010), here I will focus on how range shifts may influence community
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organization and ecosystem processes. I do not pretend to be complete in my review, and part of
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my conclusions will be speculative, but I hope to encourage thinking about species range shifts
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from a more complex (and realistic) ecological perspective.
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I will discuss recent work on aboveground-belowground interactions in relation to
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climate warming-induced species range shifts. I will compare altitudinal gradients, where
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dispersal distances may not have been a major limitation, with latitudinal gradients where range
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shifts may disrupt aboveground-belowground interactions more severely owing to larger dispersal
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distances and differences in dispersal rates. I will also provide a brief paleoecological view and
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discuss how aboveground-belowground interactions in the past may have been influenced during
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deglaciation periods. In the next sections, community and ecosystem consequences of range shifts
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will be reviewed from the perspective of aboveground-belowground interactions. I will discuss
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community assembly processes, including species loss and species gain, from an aboveground-
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belowground perspective while discussing their roles in no-analog communities (and novel
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ecosystems), foundation species and assisted migration.
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Species range shifts
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Patterns along altitudinal gradients
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The earliest signals showing that the current rapid climate warming of the past decades is leading
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to plant range shifts result from work along altitudinal gradients in Alpine ecosystems (Grabherr
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et al. 1994, Walther et al. 2002, Parmesan & Yohe 2003). Alpine vegetation responses to climate
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warming may depend on plant type and altitude. For example, along an elevation gradient, shrubs
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expanded 5.6 per cent per decade between 2400 and 2500 m above sea level. However, above
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2500 m there were unexpected patterns of regression, which were associated with increased
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precipitation and permafrost degradation (Cannone et al. 2007).
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At lower altitudes in mountains effects of climate warming are difficult to be
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disentangled from those of changes unrelated to climate, such as land use change. At high
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altitudes, where land use does not play a major role, effects of climate warming are revealed more
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clearly (Cannone et al. 2007). Nevertheless, even in low-altitude areas like the Jura (France),
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effects of warming could be detected over a 20 years period (Lenoir et al. 2008, Lenoir et al.
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2010). At a sub-Arctic island, analyses of 40 years of species data revealed an average upward
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elevation shift of half the plant species (Le Roux & McGeoch 2008). Both here and in the Jura
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not all plant species, but a subset responded to climate warming. Remarkably, although the
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species that determined the pattern of upslope expansion may be considered highly responding
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species, the response was still lower than expected based on the rate of warming (Le Roux &
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McGeoch 2008). Such species-specific range shift responses may result in no-analog
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communities at higher elevations, existing of the original plant species and range expanders.
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Downhill species shifts can also be observed, for example in California, where water deficit at
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higher elevations increased over time (Crimmins et al. 2011).
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While focusing on patterns of altitudinal range shifts, less work has been done on
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consequences for altered species interactions in relation to climate warming. In general, high
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altitude plant communities may be structured more by facilitative than by competitive interactions
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(Callaway et al. 2002). However, plant facilitation could also be influenced by aboveground and
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belowground multitrophic interactions, which may need more attention when understanding
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consequences of climate warming in high altitude habitats. As range shift distances are relatively
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short in altitudinal gradients, dispersal may be less limited. However, aboveground-belowground
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interaction patterns may still be altered in highly complex ways. For example, the development of
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bare soil surface at higher altitudes (Walther et al. 2002) will have considerable influence on
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belowground decomposition processes (Wardle et al. 1999). In contrast, ecosystem regression
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towards pioneer stages can affect the outcome of plant community interactions by a shift from
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symbiotic (arbuscular) mycorrhizal fungi towards a more prominent role for soil-borne pathogens
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(Kardol et al. 2006). In general, global change effects on soil biota are relatively well predictable
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(Blankinship et al. 2011), but interactive consequences of climate warming, such as altered frost
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incidence, rainfall patterns, plant types, and plant cover may complicate predictions of responses
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of soil biota and their feedback effects to plants and aboveground interactions.
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Patterns along latitudinal gradients
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Initially patterns of latitudinal range shifts have been predicted based on altitudinal shifts
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(Walther et al. 2002). Climate effects of one meter in altitudinal range shift may be considered
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equal to 6.1 km latitude (Parmesan & Yohe 2003). However, these conversion factors do not
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account for dispersal limitations that may arise, for example due to poor dispersal capacity,
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effects of habitat fragmentation, or limitations of vector organisms. In north-western Europe, for
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example, there are clear patterns in seed dispersal limitations as some vectors, especially large
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vertebrates, are much more limited in migration now than in the past (Ozinga et al. 2009). Such
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limitations also may apply to insect range shifts. In a study in the UK, habitat specialist butterflies
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were constrained in range expansion following climate warming due to lack of connections
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between the specific habitats. Only habitat generalists could keep up with climate warming,
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because their dispersal was less limited by unsuitable corridors (Warren et al. 2001).
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Poor dispersal capacities of certain soil biota, especially soil fauna, have been mentioned
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in a number of studies. For example, the highest nematode diversity occurs in temperate zones,
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where there are more root feeders of higher plants than in the tropics. The lower nematode
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diversity in the Antarctic than in Arctic zones suggests that dispersal limitations are, at least in
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part, causing the latitudinal zonation of nematodes (Procter 1984). Also within latitudes, there
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may be gradients, but these are more related to community similarity than to community richness.
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For example, in a comparison of nematodes and microbial assemblages among 30 chalk
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grasslands in the UK, roughly scattered across a west-east gradient of 200 km long, similarity in
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both nematodes and bacteria declined with distance (Monroy et al. 2012). Therefore, soil
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communities may vary with distance, irrespective of orientation (Fierer et al. 2009). Hence range
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shifts in any direction can cause that plant species may become exposed to novel soil biota, while
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becoming disconnected from the specific biota with which they usually have been interacting.
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Applications of findings from altitudinal shifts for range shift predictions in lowlands
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may also be complicated for other reasons. In a study of 44 years (1965-2008) of climate
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warming of lowland and highland forests in France, latitudinal range shifts were expected in the
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lowland forests. However, temperature response lags in lowland forests were 3.1 times stronger
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than altitudinal range shifts in highland forests (Bertrand et al. 2011). There are several possible
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explanations: lowland forests may have proportionally more species that are persistent to
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warming, there may be fewer opportunities for short-distance escapes, and the greater habitat
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fragmentation in lowlands may prevent range shifting.
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Range shifts can be limited by the availability of sites for establishment. This has been
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shown for butterflies (Warren et al. 2001), but also for plants. For example Leithead et al. (2010)
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showed that range-shifting tree species from temperate forest in Canada, such as red maple (Acer
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rubrum) can only establish in boreal red pine (Pinus resinosa) forest if there are large tree-fall
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gaps. Native red pine forest species, on the other hand, were not influenced by gap size or gap
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age. Interestingly, pine dominance in red pine forest is maintained by wildfires, which selectively
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omit competitors and re-set succession. Fire incidence can be altered by climate warming. As
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southern tree species establish faster in tree-fall gaps than wild fires are occurring, these
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combined effects may result in enhanced colonization of northern forests by southern tree species.
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Tropical lowlands, on the other hand, may be especially sensitive to climate warming, because
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the tropical climate now is warmer than at any time in the last 2 million years (Bush 2002). The
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spread of species from tropical forests to cooler areas may be constrained by long dispersal
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distances and poor colonization sites along the dispersal routes. Therefore, it has been suggested
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that tropical regions may be sensitive to species loss due to climate warming. Moreover, lowland
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tropics lack a species pool to provide new species that may favor the new climate conditions
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(Colwell et al. 2008). Range shifts of species from tropical lowlands to tropical highlands are
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possible, but they may result in depauperate lowland plant communities, which will be
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increasingly dominated by early successional species (Bush 2002, Colwell et al. 2008).
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Aboveground-belowground interactions have been investigated in relation to latitudinal
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range shifts. A comparison of range expanding plant species from Eurasia and other continents
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with phylogenetically related species from the invaded range showed that both types of range
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expanders develop less pathogenic activity in their soils than related natives. Moreover, the range
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expanders on average were more tolerant of, or better defended against two polyphagous
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invertebrate aboveground herbivores, which coincided with induced levels of phenolic
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compounds, which are general secondary metabolites used for plant defense (Engelkes et al.
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2008). Therefore, successful range expanding plant species may have invasive properties
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irrespective of their origin. Interestingly, although belowground and aboveground effect sizes
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were additive, there was no correlation between aboveground and belowground effect strengths
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(Morriën et al. 2011). Thus, plant species that resisted, or tolerated, belowground enemy effects
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in the new range are not necessarily well protected against generalist aboveground herbivores.
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Analysis of soil samples along a latitudinal gradient of a range expanding plant species
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(Tragopogon dubius) showed soil pathogen effects in a number of sites in the native range, but
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not in the part of the range where this species had shifted into recently (Van Grunsven et al.
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2010). Thus, range shifts enable plants to escape from their original soil pathogens, whereas
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successful range shifters were well defended against aboveground polyphagous herbivorous
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insects (Van Grunsven et al. 2007, Engelkes et al. 2008). These results have been based on
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growth trials in greenhouse mesocosms. The next step should be to determine the consequences
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of altered belowground and aboveground biotic interactions under field conditions.
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Historical patterns of range shifts
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Species range shifts have occurred throughout the Earth’s history. For example, it is well
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documented that glacial cycles have caused species range shifts (Jackson & Overpeck 2000,
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Williams et al. 2007, Willis et al. 2010). There have been approximately 20 cycles of glaciation
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and deglaciation during the Quaternary (the last 2.58 mln years), especially on the northern
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Hemisphere (Dawson et al. 2011). The last ice age occurred about 10,000 years ago. Based on
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pollen records from late Quaternary Europe paleo-vegetation maps have been constructed at the
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level of formations. As these vegetation maps are not analogue with contemporary vegetation,
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Huntley (1990a) concluded that the macroclimate in the late Quaternary may have been
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completely different from the present one. However, a complication of comparing paleobiology
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data with contemporary ecosystems is that current vegetation in Europe has been strongly
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influenced by human activities and that the continent is highly heterogeneous (Huntley 1990a). In
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spite of these uncertainties, it is still quite likely that communities have become reorganized over
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and over again during cycles of warming and cooling (Jackson & Overpeck 2000).
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Historic range shift data still cast doubts about the rate of plant dispersal. The proposed
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average of 1 km per year northward spread during deglaciation periods is most likely ten times as
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fast as the average dispersal capacity of individual plant species. This discrepancy in migration
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distances can be due to a hitherto undetected role of long-distance dispersal (Loarie et al. 2009). It
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is likely that long-distance dispersal has played an important role in pre-historic times. In a
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modeling study (K.M. Meyer and M. van Oorschot, unpublished results), long-distance dispersal
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turned out to be crucial for enemy release, in their case root-feeding nematodes. Long-distance
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dispersal of plants may also reduce their exposure to specialized aboveground enemies, because
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they may have difficulties reaching the new plant populations. Therefore, it can be expected that
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also during deglaciation range shifts plant species may have become exposed to different
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aboveground-belowground interactions.
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It is also possible that (aboveground or belowground) enemies have promoted tree range
shifts (Moorcroft et al. 2006). In a modeling study, natural enemies were able to influence the
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spread of tree species into ecosystems where equally strong competitors were present. Adding
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host-specific pathogens to the model resulted in dispersal distances equal to the ones that have
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been reported by paleo-ecologists based on pollen patterns (Moorcroft et al. 2006). Obviously, the
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issue of long-distance dispersal needs more emphasis in relation to range shifts and relationships
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with aboveground and belowground natural enemies and their antagonists. This might also
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provide a different view on evolution during glaciation-deglaciation cycles.
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In a review of range post-glacial expansion effects on the evolution of insects, it was
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concluded that that rapid evolution of dispersal may be promoted in the expansion zones (Hill et
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al. 2011). This suggests a positive feedback between range expansion and the evolution of traits
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(in this case dispersal) that accelerate range expansion capacity. Thus, the feedback between
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ecology and evolution will be strongest at range boundaries where selection will be strongest and
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where population bottlenecks are common (Hill et al. 2011). These data may, however, not be
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translated to present day range shifts, because of the unprecedented rate of the current warming.
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Moreover, modern landscapes are much more fragmented than the original post-glacial
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landscapes, which may lead to loss of genetic variation, rather than enabling trait evolution (Hill
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et al. 2011).
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Current insights in aboveground-belowground species interactions may be used to assess
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how they have been operating and changing during pre-historical changes in vegetation types. For
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example, in a flood plain in Pakistan, isotope records reveal shifts from C3 to C4 grass-dominated
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ecosystems (Barry et al. 2002). There were also pulses in (vertebrate) fauna turn-over resulting in
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a loss of biodiversity and the pace of extinction from this region accelerated once C4 vegetation
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occurred on the flood plain. Over all, species composition was relatively steady, with brief,
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irregularly spaced temporal spikes of species turnover and ecological change, however, time
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intervals of the assessment were minimally 100,000 years (Barry et al. 2002). Opposite to these
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aboveground changes in vertebrate fauna, selective plant removal studies in New Zealand
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(Wardle et al. 1999) and sampling under C3 and C4 grasses in the United States (Symstad et al.
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2000, Porazinska et al. 2003) suggest that conversion of C3 into C4 grasslands will have had very
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little effects on soil fauna or aboveground arthropod diversity. However, C4 grass vegetation may
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have been a response to warming and drier conditions, which could have had a much stronger
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effect on soil community composition and the resulting ecosystem functioning (Blankinship et al.
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2011).
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Another example concerns the last post glacial period in Europe, during which mixed
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deciduous forests received their current distribution around 8,000 B.P. Relative tree abundance
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changed in those forests over the past 13,000 years, as they were dominated first by Pinus, then
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by Tilia and during the last millennia by Fagus species (Huntley 1990b). How exactly these
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vegetation changes have taken place and at what rate is difficult to explain, because these data are
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amongst others based on chord-distance maps that have intervals of 1000 years (Huntley 1990a).
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Nevertheless, litter composition is known to influence decomposition (Hättenschwiler & Gasser
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2005) and it will also have influenced soil organisms, such as earthworms (Muys & Lust 1992)
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and microbes (Ayres et al. 2009, Strickland et al. 2009). These examples show that responses of
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plant communities to climate changes and consequences for ecosystem processes in the (late)
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Quaternary may have been quite dynamic. Over these long time periods, climate will be the
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overarching driver. Belowground-aboveground interactions may have driven community
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responses at shorter spatial and temporal scales.
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Other drivers of range shifts
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There are some, though not many, examples of range shifts that have been caused by other factors
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than climate warming or cooling. For example, intensified grazing and fire regimes enabled range
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expansion of shrubs in Colorado (Archer et al. 1995), whereas El Niño-Southern Oscillation
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influences frequency and extent of wildfires, which influences tree stand composition in southern
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USA (Swetnam et al. 1999). Further, there are examples on bird range expansion due to land use
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change. Improved feeding or nesting sites can drive such range shifts. For example, the black-
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shouldered Kites (Elanus caeruleus) has shifted range into Spain, because the last half of the
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previous century similarity increased between cultivated Dehesa systems with African savannahs,
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from where this species originates (Balbontín et al. 2008).
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Habitat fragmentation, such as caused by intensified land use, can limit the capacity of
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species range shifts. Currently, this is considered as one of the major constraints for species
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responses to climate warming (Warren et al. 2001). Habitat fragmentation may also have limited
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range shifts in post-glacial periods under specific conditions. In Finland, recolonization of former
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islands after land ice retreat during the Holocene may have been hampered by poor connectedness
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to the surrounding main land (Heikkilä & Seppä 2003). One possibility to determine if climate
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warming is the key factor leading to range shift is to determine if the pattern is one-directionally
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correlated with the warming gradient. However, terrestrial range shifts often cause mosaic-like
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patterns, rather than wave-like phenomena, which may also be due to the velocity of climate
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change on land that is far more patchy than in oceans (Burrows et al. 2011).
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Conclusions on species range shifts
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Patterns of individual species range shifts as a response to climate change are less uniform than
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general averages suggest, for example because there are fast and slow responding species, time
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lags, downhill instead of uphill range shifts, and long-distance dispersal. Some range shifts are
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due to other factors than climate, for example changing land use or altered fire incidence. Uphill
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range shift is better correlated with warming than lowland range shifts towards the poles,
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probably due to shorter dispersal distances along altitudinal gradients and less constraints such as
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habitat fragmentation at high elevations. Lowland tropical systems may be highly sensitive to
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warming, because temperatures are already higher than in the past 2 million years, and dispersal
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distances to cooler areas are generally large, except in tropical lowland-mountain areas where
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uphill range shifts are possible. Range contractions have been less well studied than range
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expansions and in some cases downhill range shifts have been recorded, for example more water
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is more available or microclimate is cooler due to forest regrowth downhill.
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Aboveground,
plants might also be released from their natural enemies, especially in the
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case of long distance dispersal. This phenomenon is also supposed to have played a role in
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recolonization during post-glacial range shifts. Therefore, although very little information exists
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on this subject, disassembly of aboveground-belowground interactions during range shift may
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influence ecology and evolution during climate warming-induced range shifts. This may happen
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now, but it can also have played a role during prehistoric range shifts. Such disruptions of
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aboveground and belowground interactions have the potential of influencing community
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assemblage processes, as well as the evolution of the species involved.
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Community consequences of altered aboveground-belowground interactions during range
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shifts
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Understanding species range shifts requires addressing a key question in ecology: how will
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biodiversity and ecosystem functioning be influenced by the disappearance of existing species
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and the arrival of new species (Wardle et al. 2011)? The research on range shifts initially has been
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dominated by reports on species extinctions due to climate warming (Warren et al. 2001, Thuiller
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et al. 2005), whereas later the emphasis has also included consequences of climate warming for
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range shifts of exotic invaders (Walther et al. 2009). Other studies have shown that the number of
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species from warm climate regions in temperate areas is increasing (Tamis et al. 2005), so that
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there is a group of species that may shift range to higher altitude or latitude in accordance with
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the rate of climate warming (Chen et al. 2011).
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Patterns of species gains and losses
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Which species will be lost and gained following climate warming depends on a large number of
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aspects, including the tolerance of species to the environmental change (warming or an associated
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change, for example drought or extreme weather events), the time needed for species to disperse
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and the time needed by other species to be lost from communities, sensitivity to habitat
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fragmentation, habitat specialization, dispersal mode, etc. The net effect of species gains and
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species loss can be that total biodiversity remains constant, but it can also decrease, or even
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increase (Jackson & Sax 2010). When time proceeds, net effects of gains and loss of species may
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vary, so that the total number of species in communities may temporarily go up or down.
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Although net effects of species gain and loss can be positive locally, worldwide biodiversity will
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decline, and communities across the world, in the same climatic zones, will appear more similar
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because of sharing an increasing number of species.
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The traits of the species coming in and going out will strongly influence their role in
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ecosystem processes. For example, novel chemistry may influence ecological relationships, as
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herbivores and decomposer organisms from the invaded range may not be capable of dealing with
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those compounds (Callaway & Ridenour 2004). Phylogenetic non-relatedness with other species
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that are native in these communities can play an important role in predicting the success of
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species introductions (Strauss et al. 2006). Loss or gains of dominant species should have more
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impact on ecosystem processes (Grime 1998), although some low-abundant species might have
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disproportional effects. For example, microbial pathogens or endophytes have low abundance, but
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they can substantially influence plant community composition (Clay & Holah 1999) and,
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therefore, ecosystem functioning.
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In general, new species most likely will have characteristics of early successionals,
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because such species have good dispersal abilities. Long-distance dispersal may enable them to
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escape from natural enemies, to which early successional plant species can be sensitive (Kardol et
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al. 2006). For example, range shift of Tragopogon dubius has not yet led to the establishment of
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specific soil-borne pathogens in the new range (Van Grunsven et al. 2010). Although it is known
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that not all species will respond to climate warming by range shift (Le Roux & McGeoch 2008),
388
little is known about which species will stay behind, what traits they have and what will be their
389
fate on the longer term.
390
391
Assessing ecological consequences
392
393
An increasing amount of studies has assessed how aboveground and belowground interactions
394
may change in relation to plant species gains (Maron & Vilà 2001, Agrawal et al. 2005, Parker &
395
Gilbert 2007, Peltzer et al. 2010) and plant species loss (Wardle et al. 1999, Scherber et al. 2010).
396
However, few such studies have focused explicitly on plant range shifts (Engelkes et al. 2008,
397
Morriën et al. 2010, Van Grunsven et al. 2010, Meisner et al. 2012). Interestingly, plant species
398
that shift range and are successful in their new range have invasive properties with respect to
399
aboveground and belowground enemy effects similar to intercontinental exotic invaders
400
(Engelkes et al. 2008). In Figure 1, different scenarios of aboveground-belowground range shifts
401
are worked out and consequences for plant biomass are presented. It is shown that depending on
402
how fast plants, herbivores and carnivores may shift range, in the new range plants can produce
403
more or less biomass than in the native range.
404
Further studies using aboveground and belowground surveys and manipulations along a
405
range expansion gradient are needed in order to tease apart the ecological and evolutionary
406
consequences of individual effects. Whereas studies on invasive plants have shown contrasting
407
relationships for the amounts of natural enemy exposure (Mitchell & Power 2003, Van Kleunen
408
& Fischer 2009), ecological responses are not necessarily in line with the assumed enemy release
409
effects (Parker & Gilbert 2007). Long-term experiments and studies along latitudinal or elevation
410
gradients (Sundqvist et al. 2011) are needed in order to determine extended effects of plant range
411
shifts on decomposition, nutrient cycling and consequences for plant performance under field
412
conditions. Transplantation studies, for example, may reveal to what extent there is specificity in
16
413
litter decomposition along latitudinal or altitudinal gradients. This specificity has been described
414
as a ‘home field advantage’ (Ayres et al. 2009, Strickland et al. 2009), as the soil communities of
415
some plant species decompose own litter faster than soil communities from other plant species.
416
This home field advantage has also been established to be plant genotype-specific (Madritch &
417
Lindroth 2011).
418
It is important to include negative controls in experiments when testing species responses to
419
climate warming. For example, in aboveground-belowground interaction studies successful range
420
expanders may be compared with unsuccessful ones in order to test aboveground-belowground
421
interaction effects (Morriën et al. 2011) and consequences for plant abundance (Klironomos
422
2002). Besides effects of species gains, consequences of species loss due to climate warming
423
need to be tested experimentally. This will yield information on the traits of species that are under
424
threat by extinction under climate warming, their ecological relationships and the amount of
425
generalist and specialist relationships with other plants and multitrophic organisms. These
426
integrated and field-based approaches may help to further conceptualizations of species loss and
427
gain (Jackson & Sax 2010) from a multitrophic perspective. Ultimately, those approaches will
428
learn how foodwebs are being influenced by global changes (Tylianakis et al. 2008) and how
429
trophic networks may function under dynamic restructuring.
430
431
Long-term perspectives on range shifts
432
433
Aboveground and belowground interactions of range shifting plants will not be static over time,
434
as has been demonstrated for host-parasite interactions (Phillips et al. 2010). When time proceeds,
435
the natural enemies, symbionts and decomposer organisms and their antagonists may colonize the
436
expanded range, but it is not yet known how fast this process may develop and how complete the
437
original communities may become re-assembled. Historical data from paleobiology do not
438
provide such detailed information. Range shifting plants that arrive without their naturally co-
17
439
evolved insects, microbes and nematodes may or may not establish interactions with species from
440
the new range. Provided that suitable conditions exist, natural selection may cause changes in the
441
genetic structure of the range shifted plants. For example, when exposure to natural enemies is
442
diminishing, selection against the production of costly defenses is to be expected (Müller-Schärer
443
et al. 2004), which could lead to a trade-off between defense and growth (Blossey & Nötzold
444
1995). This process has been tested for cross-continental introductions of exotic plant species,
445
although these costs are difficult to be quantified and experimental tests sometimes show opposite
446
results (Wolfe et al. 2004).
447
There are spectacular studies where introduced exotic species lose their capability to
448
produce high defense levels. For example, in a chronosequence representing over 50 years of
449
Alliaria petiolata introduction in North America, phytotoxin production turned out to decrease
450
when time since introduction increases (Lankau et al. 2009). Variation in allelochemical
451
concentrations also influenced soil microbes, including fungi that had mutualistic interactions
452
with a native tree species (Lankau 2011). Over time, introduced plants may become less resistant,
453
or native biota may develop higher aggressiveness. For example, in New Zealand plant species
454
that varied in time since being introduced until maximally 250 years were experimentally
455
exposed repeatedly to soil biota. This study showed that the longer ago the plant species had been
456
introduced, the stronger the pathogenic effects from the soil community were (Diez et al. 2010).
457
These studies suggest that introduced exotic species may become less invasive over time, due to
458
natural selection of the introduced species themselves, or the belowground or aboveground
459
species from the new habitat. Possibly, these temporal processes may contribute to the sudden
460
population crashes that have been observed for a number of introduced species (Simberloff &
461
Gibbons 2004). A possible long-term scenario for such a boom-bust pattern has been worked out
462
in Figure 2.
463
464
Conclusions
18
465
466
Thus far, most work on pattern analyses of range shifts has been dedicated to understanding
467
consequences of species loss due to climate warming. Species gain effects have not received
468
much attention yet and the ecological consequences, as well as temporary developments of range
469
shifting species are only beginning to be explored. However, we can expect that successful range
470
shifting involves a gradual response of the available plant species and that aboveground and
471
belowground organisms expand their range subsequently, but at lower and variable rates. In the
472
meantime, aboveground and belowground organisms from the native range will establish
473
interactions with the new species, and may adapt to the new plants by natural selection. The biotic
474
interactions established in the new range, in return will also impose natural selection on the range
475
shifting species and this may reduce the invasive performance when time since introduction
476
proceeds further. The question is what may happen when the former natural enemies become co-
477
introduced as well: will they recognize their original host, or not (Menéndez et al. 2008), over-
478
exploit their former host, or will the novel biotic interactions completely alter priority effects
479
(Lau 2006). Considering all these possible changes, it is quite likely that the original host-
480
consumer interactions will not become restored as they were acting in the original range. The
481
outcome of this complex process might contribute to boom-bust patterns of abundance that have
482
been observed for some introduced exotic species, novel community composition and
483
functioning, or they may enable a ‘soft landing’ for the range shifting species in their novel
484
habitats following restoration of the original species interactions.
485
486
Ecosystem consequences of changed aboveground-belowground interactions during range
487
shifts
488
489
Until here, range shifts have been considered mainly from the perspectives of species response
490
patterns and community interactions. The question now is whether and how these altered species
19
491
assemblages and community interactions translate into ecosystem consequences. These
492
consequences may be expressed as altered ecosystem processes (nutrient cycles), resilience and
493
stability, and their influences on the provisioning of ecosystem services (for example, primary
494
production, control of greenhouse gas emissions, control of pests and pathogens) (Naeem et al.
495
2009). Few such analyses have been made of ecosystem consequences of range shifts, opposite to
496
biodiversity loss and exotic species invasions (Wardle et al. 2011).
497
In a comparative study of range-shifted plant species and phylogenetically related natives
498
from the new range, nutrient dynamics in the root zone (Meisner et al. 2011) and litter
499
decomposition (Meisner et al. 2012) were affected by plant (genus-related) traits, rather than by
500
plant origin. That is also analogous to work done on intercontinental invasive plant species, which
501
may enhance nutrient cycling dynamics, but there is no general pattern between natives and
502
exotics (Ehrenfeld et al. 2005, Vilà et al. 2011).
503
Interestingly, plant origin affected sensitivity to aboveground polyphagous insects
504
(Engelkes et al. 2008) and feedback effects from the soil community (Van Grunsven et al. 2007,
505
Engelkes et al. 2008) in similar phylogenetically controlled comparisons. Therefore, nutrient
506
cycling-related ecosystem services may be altered less by range shifts than biocontrol-related
507
services. Failing top-down control in the new range can be due to enemy release of the range
508
expanders (Van Grunsven et al. 2010), failing biotic resistance from the natural enemies present
509
in the new range, or a combination of the two (Keane & Crawley 2002). In a survey of
510
intercontinental invasive exotic plant species, exotic plants had fewer pathogen and virus species
511
in the new range than expected (Mitchell & Power 2003). Little is known whether this applies as
512
well to plant species that have shifted range intra-continentally.
513
Another ecosystem consequence of range shifts is related to the question if diversity
514
begets diversity (Whittaker 1972, Janz et al. 2006). Some plant species can have a disproportional
515
role in sustaining aboveground and belowground biodiversity. These so-called foundation species
516
(Ellison et al. 2005) strongly influence aboveground and belowground community composition
20
517
and species interactions, which can be considered as ‘extended phenotypes’. Little is known
518
about range shift potentials of such foundation species and how species assemblages aboveground
519
and belowground in the new range may be as extended as in the native range. Non-foundation
520
species may have less far-stretching effects on aboveground and belowground communities.
521
Nevertheless, many of those species may also have individual aboveground (Bukovinszky et al.
522
2008) and belowground (Bezemer et al. 2010) food webs, which could be altered by differential
523
range shift capacity (Berg et al. 2010). Therefore, ecosystem consequences of range shifts may be
524
that foundation species, as well as non-foundation species lose at least part of their extended
525
phenotypes (Figure 1). Consequences for ecosystem processes, resilience and stability are yet
526
unknown.
527
The altered community composition of range-shifted plant species potentially influences
528
community genetics (Hersch-Green et al. 2011). When range-shifting plant species have fewer
529
ecological interactions in the new than in the original range, patterns of community genetics and
530
evolutionary processes can be completely different in the new than in the original range. These
531
changes at the genetic level may have consequences at the level of ecosystem processes and
532
functioning (Whitham et al. 2006). Therefore, range shifts will provide interesting opportunities
533
for community genetics approaches by testing how micro-evolutionary processes may play a role
534
during disintegration and (re)assemblage of multitrophic interactions under climate warming. In
535
these studies, abiotic stress conditions should also be included, as they can change during climate
536
warming, both in the native and new range, and they can alter composition and functioning of
537
entire food webs below ground (De Vries et al. 2012).
538
It has been proposed that assisted migration and colonization (Hoegh-Guldberg et al.
539
2008) may help solving problems of species that are not able to shift range under climate
540
warming. However, assisted migration might also involve risks with consequences for the
541
composition, as well as functioning of ecosystems of the new range. Successful range expanding
542
plant species have invasive properties similar to intercontinental invaders (Engelkes et al. 2008).
21
543
It is not known if these invasive properties are already intrinsic in the original populations,
544
whether they are selected during range shift, or whether they are due to rapid evolution in the new
545
range. Any of these options will be relevant to be considered when preparing assisted migration:
546
which genotypes to select for dispersal, how to test their ecological suitability to become
547
established in the new range and how to assess ecological consequences in case the assisted
548
species may do disproportionally well in their new range. There are already too many examples
549
from intentional or unintentional cross-continental invasions where taking species out of their
550
original community context has resulted in enemy release (Keane & Crawley 2002). Therefore,
551
before considering assisted migration and other climate warming mitigation activities, community
552
and ecosystem consequences of such actions need to be carefully assessed, including
553
consequences of aboveground or belowground enemy release (Engelkes et al. 2008), symbiont
554
availability (Hegland et al. 2009) and loss of home field advantage of decomposition (Ayres et al.
555
2009).
556
It is in this context that discussions on emerging ecosystems (Milton 2003) and novel
557
ecosystems (Hobbs et al. 2006) may need to be considered. As in restoration ecology, where the
558
role of soil communities and aboveground-belowground interactions have become acknowledged
559
(Harris 2009, Kardol & Wardle 2010), consequences at the ecosystem level of aboveground-
560
belowground interactions influenced by range shifts need to be considered as well. Most likely,
561
the concept of novel ecosystems may require considering species as tied in aboveground-
562
belowground interactions, rather than the considering presence or absence of species in isolation.
563
However, ecological novelty may change over time, because of the temporal dynamics of
564
dispersal of associated species, as well as community genetics processes to which both the new
565
and the resident species will be exposed. Therefore, by considering the interactions of
566
aboveground and belowground species from a combined ecological and evolutionary perspective,
567
ecosystem consequences of (climate warming-induced) range shifts may be more appropriately
568
predicted. This work could as well serve to better understand historical range shifts during
22
569
glaciation-deglaciation cycles, how those processes may have shaped current aboveground-
570
belowground communities in terrestrial ecosystems, and to predict the potential consequences of
571
the current unprecedented rates of warming for future ecosystem functions and services.
572
573
Summary points
574
575
576
577
578
579
1. Terrestrial ecosystems consist of aboveground and belowground subsystems and the species
in these subsystems all can interact.
2. Range shifts of plant species may result in temporary release from natural enemies or
symbionts, which might cause invasions or establishment failures in the new range
3. Decomposition-related processes have been supposed to be less specific, but recent work has
580
pointed at considerable – even up to the plant genetic level – specificity in decomposer
581
organisms.
582
583
4. Latitudinal range shifts will be more sensitive to disruption of aboveground-belowground
interactions than altitudinal range shifts.
584
5. No-analog communities have no-analog aboveground-belowground interactions, which may
585
change patterns of community organization, species abundance and biodiversity completely.
586
587
6. Landscape configuration may be important for range shifts, as it influences dispersal
capacities of plants, aboveground and belowground biota.
588
7. Range shifts will be crucial for maintaining ecosystem functioning and ecosystem services.
589
8. The role of foundation species and community genetics may change substantially due to
590
591
592
range shifts.
9. Assisted migration should be considered with care, as it might cause more problems than it
may solve.
593
594
Acknowledgements
23
595
596
I thank Tadashi Fukami for proposing me to write this review and for providing helpful
597
comments, Pella Brinkman for helping me throughout the writing process, Jennifer Krumins,
598
Annelein Meisner, Elly Morriën, Pella Brinkman and Martijn Bezemer for comments and
599
suggestions on previous versions of the manuscript. This is NIOO publication xxxx.
600
601
Figure captions
602
603
Figure 1. Scenarios for range shifts of plants, aboveground and belowground herbivores and their
604
natural enemies and consequences for plant size (or abundance). According to scenario A, plants
605
shift range faster than all aboveground and belowground biota and do not encounter biotic
606
resistance in the new range. This leads to enhanced biomass in the new range both aboveground
607
and belowground. In scenario B, aboveground herbivores shift range as fast as plants and are
608
released from their natural enemies. This leads to over-exploitation of the plants, aboveground
609
(n.b.: it is to be debated whether this may also result in reduced belowground biomass due to a
610
lack of photosynthesis products to support root and rhizome growth). In scenario C, aboveground
611
herbivores and carnivores shift range equally fast as plants, resulting in unchanged aboveground
612
biomass compared to the native range, whereas root biomass may be enhanced due to lack of
613
belowground herbivory (but see scenario B).
614
615
Figure 2. Hypothetical explanation for an introduction-boom-bust pattern of size (or abundance)
616
of a range-shifting plant species. Following introduction, there may be a benefit of release from
617
native enemies, absence of biotic resistance in the new range, and generalist symbionts
618
(pollinators, arbuscular mycorrhizal fungi) in the new range that weighs out poor home field
619
advantage. This benefit may further increase due to evolution of increased competitive ability and
620
the development of home field advantage due to specialization of decomposer organisms from the
24
621
new range. However, that benefit can turn into a major disadvantage when natural enemies from
622
the native range migrate as well, or enemies from the new range break through plant resistance. In
623
that case, plants are poorly defended and in spite their home field advantage, top-down control
624
becomes so severe that plant size or abundance is strongly reduced with a risk of extinction.
625
626
25
627
26
628
629
630
Figure 2. Aboveground-belowground scenario for a boom-bust pattern of
631
range-shifted plants in their new range
27
632
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