Disturbance by an endemic rodent in an arid ...

Annals of Botany Page 1 of 12 doi:10.1093/aob/mcw258, available online at www.aob.oxfordjournals.org

Disturbance by an endemic rodent in an arid shrubland is a habitat filter: effects on plant invasion and taxonomical, functional and phylogenetic community structure Vıctor M. Escobedo1, Rodrigo S. Rios1, Cristian Salgado-Luarte1, Gisela C. Stotz2 and Ernesto Gianoli1,3,* 1

Departamento de Biologıa, Universidad de La Serena, Casilla 554 La Serena, Chile, 2Department of Biological Sciences, University of Alberta, Edmonton, Canada T6G 2E9 and 3Departamento de Bot anica, Universidad de Concepci on, Casilla 160C Concepci on, Chile *For correspondence. E-mail [email protected] Received: 9 September 2016 Returned for revision: 4 October 2016 Editorial decision: 9 November 2016

Background and Aims Disturbance often drives plant invasion and may modify community assembly. However, little is known about how these modifications of community patterns occur in terms of taxonomic, functional and phylogenetic structure. This study evaluated in an arid shrubland the influence of disturbance by an endemic rodent on community functional divergence and phylogenetic structure as well as on plant invasion. It was expected that disturbance would operate as a habitat filter favouring exotic species with short life cycles. Methods Sixteen plots were sampled along a disturbance gradient caused by the endemic fossorial rodent Spalacopus cyanus, measuring community parameters and estimating functional divergence for life history traits (functional dispersion index) and the relative contribution to functional divergence of exotic and native species. The phylogenetic signal (Pagel’s lambda) and phylogenetic community structure (mean phylogenetic distance and mean nearest taxon phylogenetic distance) were also estimated. The use of a continuous approach to the disturbance gradient allowed the identification of non-linear relationships between disturbance and community parameters. Key Results The relationship between disturbance and both species richness and abundance was positive for exotic species and negative for native species. Disturbance modified community composition, and exotic species were associated with more disturbed sites. Disturbance increased trait convergence, which resulted in phylogenetic clustering because traits showed a significant phylogenetic signal. The relative contribution of exotic species to functional divergence increased, while that of natives decreased, with disturbance. Exotic and native species were not phylogenetically distinct. Conclusions Disturbance by rodents in this arid shrubland constitutes a habitat filter over phylogeny-dependent life history traits, leading to phylogenetic clustering, and drives invasion by favouring species with short life cycles. Results can be explained by high phenotypic and phylogenetic resemblance between exotic and native species. The use of continuous gradients when studying the effects of disturbance on community assembly is advocated. Key words: Disturbance gradient, habitat filtering, phylogenetic signal, short life cycle, exotic species, functional divergence, phylogenetic structure, Spalacopus cyanus.

INTRODUCTION Disturbance events (e.g. fire, grazing, mowing activity of fossorial mammals) remove plant biomass and thereby create opportunities for plant species colonization (Davis et al., 2000; Shea and Chesson, 2002; Mouillot et al., 2013). Colonizing plants, such as non-native (hereafter: ‘exotic’) species, are usually adapted to exploit transient increases in resource availability by a rapid completion of their life cycle (r-strategists; Grime, 1977). Consequently, plant community structure should vary in a rather predictable manner following disturbance. The ‘Intermediate Disturbance Hypothesis’ (Connell, 1978) states that moderate levels of disturbance prevent competitive exclusion, generating a mixture of colonizing and slow-growing plant species that increase diversity and taxonomic composition. This pattern, however, is not always confirmed because the effects of disturbance on diversity may vary with environmental conditions (Hughes et al., 2007). In this regard, Huston

(1979, 2004) proposed a ‘Dynamic Equilibrium Model’, which predicts that the effects of disturbance on species diversity should reverse from productive to unproductive environments. That is, in productive environments, increased disturbance causes an increase in species diversity by reducing the biomass of dominant species and creating an opportunity for plant colonization, e.g. establishment of exotic species (Davis et al., 2000; Shea and Chesson, 2002). Conversely, in unproductive environments, an increase in disturbance beyond natural (or historic) levels causes failure of native plant populations to persist, resulting in a decrease in species diversity together with an increase in the probability of a successful invasion by exotics (Alpert et al., 2000; Huston, 2004). The failure of native plant populations to persist occurs because only those species with traits associated with short life cycles or tolerant to non-natural (or new) harsh conditions can establish successfully (Kraft et al., 2015). Finally, under intermediate conditions of

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Escobedo et al. — Disturbance by rodents drives phylogenetic clustering and plant invasion

productivity, an increase in disturbance produces the unimodal response originally proposed by Connell (1978). Although a global study concluded that disturbance is a weak predictor of plant invasion (Moles et al., 2012), a recent meta-analysis demonstrated that exotic species benefit from disturbance (Jauni et al., 2015). Thus, the species diversity and abundance of exotic species are higher at disturbed sites compared with undisturbed sites, while native species are not affected by disturbance (Jauni et al., 2015). Disturbance may increase resource availability, thus providing the opportunity for exotic species to invade (Davis et al., 2000; Shea and Chesson, 2002). Exotic species have faster growth, more efficient seed dispersal and higher resource-use efficiency and fecundity than native species (Van Kleunen et al., 2010, and references therein); thus they can rapidly colonize and establish at disturbed sites (Tierney and Cushman, 2006). Increased species richness and abundance of exotic species at disturbed sites can change community composition as a consequence of their impact on the performance and population dynamics of resident species (Vila et al., 2011). Importantly, disturbance often shows continuous variation in nature, but for operational reasons it is commonly studied as a categorical or dichotomous factor (Sousa, 1984; Jauni et al., 2015). If native or exotic species richness and abundance vary with disturbance in a non-linear fashion, it would be overlooked by a dichotomous approach (‘veiled gradient’; McCoy, 2002). For example, the metaanalysis conducted by Jauni et al. (2015), based on a categorical approach, showed that the species diversity and abundance of exotic species is higher at grazed sites compared with ungrazed sites. However, Moles et al. (2012) through a continuous approach showed that the increase in grazing intensity was not significantly associated with either abundance or species richness of exotic species. An accurate estimation of the relationship between disturbance and native/exotic species richness and abundance is not only important for a better understanding of the dynamics of ecological communities, it is also essential to avoid misleading recommendations for management of invasive species (Daehler, 2003). Community patterns are thought to be largely driven by the simultaneous action of two processes: (1) ‘limiting similarity’, where only species with dissimilar combinations of traits related to resource acquisition and/or use would coexist; and (2) ‘habitat filtering’, where only species with particular traits or strategies can establish and persist, leading to similar combinations of traits in coexisting species (Pausas and Verdu, 2010; Mouillot et al., 2013). Generally, increased disturbance reduces fitness of resident plant species, and by reducing the number of dominant species and releasing space and resources it may lessen the importance of interspecific competition in the community (Huston, 1979; Dinnage, 2009). Thus, disturbance is likely to tip the balance in favour of habitat filtering and against limiting similarity as the main process driving community structure (Mouillot et al., 2013; Laliberte´ et al., 2013). In unproductive environments where only plants with particular traits or strategies can establish and persist, we expect habitat filtering to become the dominant assembly process under the influence of disturbance (Kraft et al., 2015). The relative importance of habitat filtering in community assembly can be inferred from patterns of plant functional convergence or divergence (Pausas and Verd u, 2010), where convergence (species are

more functionally similar to each other than expected by chance) is typically associated with habitat filtering (Pausas and Verdu, 2010). Plant–plant interactions may also influence assembly processes in stressful environments (McIntire and Fajardo, 2014). For instance, it has been shown that facilitation may promote functional divergence in the resource-poor alpine tundra (Spasojevic and Suding, 2012). However, this pattern is opposite to what we expected to find assuming a habitatfiltering process: disturbance promoting functional convergence (Mouillot et al., 2013; Laliberte´ et al., 2013). Disturbance is a major agent of selection in the evolution of life history traits in plants (Grime, 1977; Sousa, 1984). At the community scale, previous studies have shown that species sharing functional traits associated with disturbance are more closely related than expected by chance (phylogenetic signal for r-strategy; Brunbjerg et al., 2012). If there is a phylogenetic signal for life history traits, we expect consistency between the phylogenetic and the functional structure, and thus an increase in disturbance may result in non-random phylogenetic community structure (Webb et al., 2002; Pausas and Verd u, 2010). In other words, if plant life history traits show phylogenetic signal and only species adapted to disturbance can persist and establish, then communities where these species are common should show phylogenetic clustering. Conversely, if closely related species are not functionally more similar than expected by chance (no phylogenetic signal), then habitat filtering may produce a phylogenetically overdispersed community structure. Evaluations of whether increased disturbance leads to phylogenetic clustering have not found consistent results (reviewed by Zhang et al., 2014). This inconsistency has been explained, at least in part, by the use of incomplete disturbance gradients, which probably miss disturbance levels where patterns might emerge (McCoy, 2002; Zhang et al., 2014). The nature of the effects of increased disturbance on species richness and abundance of both native and exotic species, as well as the relationship between disturbance and phylogenetic community structure, are still unresolved issues (Cadotte et al., 2010; Brunbjerg et al., 2012). Our understanding of the interplay between disturbance and exotic species in determining the phylogenetic structure of plant communities would benefit from an integrative analysis, which should include a continuous gradient of disturbance, patterns of functional structure (convergence or divergence) with the relative contribution of native and exotic species, and the underlying type of evolution (existence of phylogenetic signal). In the present study we evaluated the species richness and abundance of native and exotic herbs in 16 local communities along a natural gradient of soil disturbance in an arid shrubland of central Chile. We also determined the changes in community composition along the disturbance gradient and identified which species were most strongly associated with these changes. Finally, we measured community functional divergence using life history traits and the relative contribution to functional divergence of native and exotic species, as well as the phylogenetic structure of all 16 communities. We focused at the local scale, where soil disturbance by an endemic fossorial rodent (Spalacopus cyanus; Octodontidae) is a conspicuous element of the system (bare soil mounds). We chose this scale to avoid habitat differences that may be confounded with the disturbance gradient at larger scales (Dinnage, 2009). We tested

Escobedo et al. — Disturbance by rodents drives phylogenetic clustering and plant invasion the hypothesis that the disturbance gradient generated by the burrowing activity of S. cyanus acts as a habitat filter that favours closely related herb species with traits associated with short life cycles, thus driving increased abundance and species richness of exotic species and modifying community composition. Specifically, we predicted that: (1) abundance/richness of native species and exotic species would decrease and increase with disturbance, respectively; (2) compositional change along the disturbance gradient would be mainly linked to exotic species for the more disturbed communities and to native species for the less disturbed communities; (3) functional divergence would decrease as disturbance increases (changing from divergence to convergence); (4) the relative contribution to functional divergence of exotic species and native species would increase and decrease with disturbance, respectively; and (5) phylogenetically dependent life history traits associated with increased disturbance would change phylogenetic community structure from overdispersed to clustered. MATERIALS AND METHODS Study site

Research was conducted at Las Cardas Experimental Station (5436 ha; Universidad de Chile) in North-Central Chile (30 150 S–71 170 W). The study area is an arid shrubland (aridity index ¼ 54; De Martonne, 1926) with a mean annual precipitation of 138 mm, low productivity (Pe´rez-Quezada et al., 2012) and homogeneous soil textural properties (Verbist et al., 2013). The study site has 18 ha of fenced area from which livestock and anthropogenic activities have been excluded for 34 years. The enclosure lies on flat land, so it does not extend over slopes, which would result in contrasting exposure to solar radiation. The dominant vegetation is an open shrubland (main woody species: Gutierrezia resinosa, Flourensia thurifera, Acacia caven and Senna cumingii) with a temporally active herbaceous stratum (winter and beginning of spring) dominated by native species such as Bromus berteroanus, Conanthera campanulata and Plantago hispidula (see species abundance ranking in Supplementary Data Fig. S1). Despite unnoticeable human impact, within the enclosure there is a substantial presence of exotic species such as Medicago polymorpha and Herniaria cinerea (Fig. S1). Exotic species established in Las Cardas arrived in central Chile on average 140 years ago (range: 170–56 years; Fuentes et al., 2013). Currently, 21 out of 106 plant species in the site are exotic (C. Salgado-Luarte et al., unpubl. data). Occurrence of exotic species within the enclosure may be linked to the intensive use of surrounding habitats for goat raising (C. Salgado-Luarte et al., unpubl. data). Disturbance gradient

The main disturbance regime within the enclosure is generated by the burrowing activity of the fossorial rodent Spalacopus cyanus (Octodontidae). Spalacopus cyanus is an endemic herbivorous rodent, distributed from 27 S to 37 S along the coastal range, which forms colonies of 16–26 individuals that maintain a system of connected tunnels (Contreras et al., 1993). Soil disturbance by S. cyanus generates

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conspicuous above-ground oval bare soil mounds (004– 025 m2 area, 10–20 cm height) that are distributed in clusters (Contreras et al., 1993). In areas free from enclosures of North-Central Chile, disturbance by this rodent promotes the recruitment of the exotic species Mesembryanthemum crystallinum and native geophyte species (its main food source) without changing diversity or composition (Contreras and Gutie´rrez, 1991). In areas relatively free from human impact such as our study site, however, mounds of S. cyanus do not promote colonization of M. crystallinum (Contreras et al., 1993). We verified that M. crystallinum is absent from Las Cardas, supporting the idea of a habitat with low human disturbance. It has been suggested that mounds of S. cyanus may drive the expansion of exotic species through an increase in soil nutrient availability (Torres-Dıaz et al., 2012). However, soil from S. cyanus mounds and soil from microsites without the influence of S. cyanus showed no difference in pH, electrical conductivity, nitrogen, phosphorus, potassium or organic matter (Contreras et al., 1993; Whitford and Kay, 1999). This suggests that the effects of disturbance by S. cyanus are mainly mediated by physical phenomena (i.e. plant removal by burial) rather than via changes in soil nutrient content or plant consumption (Contreras et al., 1993). At Las Cardas, the only noticeable gradient within the enclosure is the density of mounds, which in turn is associated with a decrease in total plant abundance (see Table 1). Mound density, however, was not associated with the abundance of Bromus berteroanus, the most abundant native species [Generalized Linear Models (GLMs): v2ð1Þ ¼ 148, P ¼ 0224]. The abundance of B. berteroanus was not included in the statistical model (see below) because it did not affect any of the response variables of this study (Supplementary Data Table S1). Sampling design

To assess how variation in natural disturbance by S. cyanus relates to herb community structure, we sampled and compared sixteen 025 ha plots randomly established within grazing-free sites to minimize confounding factors. Each plot embodied a single independent plant community with its specific level of rodent disturbance (¼ number of mounds) and was located on average 100 m apart from each other (range: 30–200 m). Accordingly, there was a disturbance gradient that ranged from two to 14 mounds per plot. Within each plot, 25 quadrats of 03 03 m were placed along five parallel 25 m transects. In each quadrat, every individual was recorded and identified to species or genus level, and the abundance was estimated as the sum of occurrences in the 25 quadrats within each plot (frequency). For each species, following standard references (Cornelissen et al., 2003; Pe´rezHarguindeguy et al., 2013) and regional floras (Squeo et al., 2001; Zuloaga et al., 2008), we determined three categorical life history traits: growth form (rosette plant/elongated/ extensive-stemmed herb/tussock/bambusoid/herbaceous vine/scrambler), plant life span (annual/biennial/perennial) and life form (therophyte/hemicryptophyte/geophyte/phanerophyte). We also recorded species origin (OR) as ‘native’ or ‘exotic’ (Fuentes et al., 2013).

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TABLE 1. Linear (D), quadratic (D2) and averaged (between linear and quadratic models) relationships between disturbance and community parameters: richness, abundance, standardized effect size (SES) of overall and single trait (growth form, life span and life form) functional dispersion, relative contribution of native and exotic species to overall and life span functional divergence, SES of mean pairwise distance (MPD) and SES of mean nearest taxon distance (MNTD) Parameter

Richness for groups Total Native Exotic Abundance for groups Total Native Exotic

Model

Slope parameter

Pseudo-R2

d.f.

logLik

AICc

DAICc

wi

D

D2

Linear Quadratic Linear Quadratic Linear Quadratic *Average

–0090 0126 –0407 –0945 0317 1071 0524

– –0015 – 0036 – –0051 –0014

0008 0010 0260 0270 0244 0301 –

3 4 3 4 3 4 –

–43245 –43225 –37410 –37137 –34044 –33200 –

94491 98085 82820 85910 76089 78036 –

0 3595 0 3091 0 1948 –

0858 0142 0824 0176 0726 0274 –

Linear Quadratic Linear Quadratic Linear Quadratic

–0018 0024 –0033 –0015 0019 0131

– –0003 – –0001 – –0007

0476 0561 0786 0791 0426 0181

2 3 2 3 2 3

–70181 –68770 –76535 –76336 –66457 –63613

145286 145541 157993 160672 137836 135225

0 0255 0 2679 2611 0

0532 0469 0792 0208 0213 0787

– –0004 – 0019 – –0014 – –0022

0245 0235 0001 0064 0359 0374 0002 0079

3 4 3 4 3 4 3 4

–18983 –18942 –21244 –20636 –18767 –18332 –21556 –20814

45966 49521 50488 52908 45535 48300 51111 53265

0 3555 0 2420 0 2765 0 2154

0855 0145 0770 0230 0799 0201 0746 0254

– 0072 – –0131

0366 0364 0286 0322

3 4 3 4

–50826 –50626 –51430 –50789

109653 112889 110860 113214

0 3235 0 2355

0834 0166 0764 0236

– 0197 0087 – 0197 –0087

0157 0286 – 0157 0286 –

3 4 – –

–51123 –49537 – –51123 –49537 –

110246 110710 – 110246 110710 –

0 0464 – 0 0464 –

0558 0442 – 0558 0442 –

– 0037 0009 – 0043 0021

0203 0280 – 0084 0233 –

3 4 – 3 4 –

–27480 –26452 – –26599 –24939 –

62959 64540 – 61197 61514 –

0 1581 – 0 0317 –

0688 0312 – 0540 0460 –

Functional divergence OverallSES

Linear –0124 Quadratic –0058 Linear –0004 Growth formSES Quadratic –0293 Linear –0161 Life spanSES Quadratic 0051 Linear –0012 Life formSES Quadratic 0313 Relative contribution to overall functional divergence Native Linear –1209 Quadratic –2280 Exotic Linear 1046 Quadratic 3006 Relative contribution to life span functional dispersion Native Linear –0700 Quadratic –3639 *Average –1999 Exotic Linear 0700 Quadratic –3639 *Average 1999 Phylogenetic structure Linear –0187 MPDSES Quadratic –0736 *Average –0332 Linear –0106 MNTDSES Quadratic –0753 *Average –0427

For each community parameter, the log-likelihoods (logLik), a corrected Akaike Information Criterion (AICc), the difference between the AICc value for a given model and that with the lowest AICc (DAICc) and Akaike weights (wi) are shown. All models were fitted using a GLM, and the significance of their parameter estimates are based on LRTs (P < 005). Significant coefficients are shown in bold. Slope parameters of abundance are log-transformed. *Averaged parameters are shown for cases where both linear and quadratic models had substantial support (DAICc 8 mounds (see Fig. 3; Supplementary Data Fig. S3). In addition, the analysis of preference showed that 20 species (14 native and six exotic) had a significant association with communities with a given disturbance level (Supplementary Data Table S3). All but one of the six exotic species were associated with communities with 9 mounds (Fig. 3; Table S3; Supplementary Data Fig. S3). In contrast, 64 % of the 14 native species were associated with communities with 8 mounds (Fig. 3; Table S3; Fig. S3), showing that exotic species are mostly associated with the more disturbed communities and, conversely, native species are mostly associated with the less disturbed communities. Functional divergence

The SES of FDis for overall traits and plant life span showed a significant relationship to disturbance; neither growth form nor life form showed associations with disturbance (Table 1; Fig. 4A, B; non-significant relationships are not shown). For overall FDis, increased disturbance resulted in a change from functional divergence to functional convergence (Fig. 4A), a pattern typically associated with habitat filtering. Thus, species with traits poorly suited to local disturbance by S. cyanus cannot establish or occur at very low abundance. The SES of a plant life span changed from functional divergence to functional convergence as disturbance increased. Therefore, species at more disturbed communities were more similar than expected in terms of life span, while at less disturbed communities they were more different than expected (Fig. 4B). We found a significant interaction between disturbance and OR for the relative contribution to both overall (Overallcontribution: G21,28 ¼ 57940, P < 001) and life span functional divergence (Life spancontribution: G21,28 ¼ 22331, P < 005). The proportional variation in both overall and life span functional divergence contributed by the FDis of native species was significantly higher than that contributed by exotic species (Fig. 4C, D). The overall functional divergence contribution

Escobedo et al. — Disturbance by rodents drives phylogenetic clustering and plant invasion Life history traits

Number of mounds

GF PL LF

2 2 3 3 4 4 6 8 8 9 9 9 10 11 13 14

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Stachys truncata Plantago hidpidula Solanum gaudichaudii Galium aparine Diplolepis boerhaviifolia Pectocarya dimorpha Cryptantha glomerata Cryptantha linearis Gamochaeta suffruticosa Helenium urmenetae Helenium sp Sonchus oleraceus Sonchus asper Moscharia pinnatifida Calendula tripterocarpa Cyclospermum laciniatum Eryngium coquimbanum Gilia laciniata Herniaria cinerea Cistanthe longiscapa Montiopsis trifida Lastarriaea chilensis Medicago polymorpha Sicyos baderoa Viola pusilla Oxalis rosea Oxalis micrantha Malva parviflora Clarkia tenella Camissonia dentata Erodium malacoides Erodium cicutarium Crassula closiana Fumaria parviflora Aristolochia chilensis Aristida adscensionis Aristida sp1 Aristida sp2 Avena sative Lamarckia aurea Bromus berteroanus Bromus catharticus Oziroe biflora Gethyum cuspidatum Leucocoryne sp Pasithea coerulea Olsaynium junceum Conanthera campanulata Trichopetalum plumosum Dioscorea humifusa 10 15 20 25

50 MYR

Number of individuals

FIG. 1. Phylogenetic tree showing all 50 studied species (exotic and native species are shown in bold and grey, respectively). Life history traits for each species are shown as follows. growth form (GF) categories are: rosette plant (black square), tussock (grey square), elongated (light-grey square), extensive-stemmed herb (white square), bambusoid (black circle), scrambler (grey circle) and herbaceous vine (white circle). Plant life span (PL) categories are: annual (white), biennial (grey) and perennial (black). Life form (LF) categories are: therophyte (white), geophyte (light grey), hemicryptophyte (grey) and phanerophyte (black). Species abundance along the disturbance gradient (where each column is a plot with its respective number of mounds) is shown as the number of individuals in a 025 ha plot scaled by the size of the black circles.

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Escobedo et al. — Disturbance by rodents drives phylogenetic clustering and plant invasion A

Abundance

Richness

B

Native Exotic

40 30 20 10 0

6

Native Exotic

5 4 3 2

2

4 6 8 10 12 14 Number of mounds

2


FIG. 2. Relationship between disturbance level (number of mounds) and expected richness (A) and abundance [ln (frequency of species)] (B) of native and exotic species. Solid lines represent significant relationships (GLM). Dashed lines represent the averaged GLMs (between linear nd quadratic models).

3 Oro Sba

Dbo

2

Fpa* Ctr Mpi

Gcu Tpl

Gap*

Sas Asa

Str*

Ach

Pco*

1

Dhu* NMDS 2

Sol

Oju

Lsp

Disturbance

Mpa Sga*

0

Ema* Aad*

Gsu* Eco*

Clo Hci*

–1

Lch Vpu Ccl Pdi

Hur* Hsp

Gla Cde*

–2

Mtr

–3 –3

–2

–1

0

1

2

3

NMDS 1 FIG. 3. Changes in species composition along the disturbance gradient generated by the fossorial rodent Spalacopus cyanus at an arid shrubland. Patterns are based on a non-metric multidimensional scaling (NMDS) analysis. Community composition at each level of disturbance and their centroids are represented with both grey ellipsoids (from light grey to dark grey) and numbers that indicate the numbers of mounds at each level. The vector represents the correlation between disturbance and community composition and represents the gradient in multidimensional space. Exotic species have bold labels, and an asterisk indicates a significant correlation index (rUg ). Species codes are given in Supplementary Data Table S2. Concordance between observed interobject distances and those predicted from the dissimilarities (final stress ¼ 0155).

of exotic species increased linearly with disturbance, while the contribution of native species showed a significant linear decrease (Table 1; Fig. 4C). The contribution to life span functional divergence of exotic and native species showed a concave and convex parabola along the disturbance gradient, respectively (Fig. 4D). In both cases only the linear component/parameter (D) was statistically significant (Table 1, solid line in Fig. 4D), so the contribution to life

span functional dispersion by exotics increased, while that of natives decreased, along the disturbance gradient.

Phylogenetic signal and community structure

We found significant phylogenetic signals (i.e. traits are influenced by phylogeny) for all life history traits but not for

Escobedo et al. — Disturbance by rodents drives phylogenetic clustering and plant invasion B

A

Plant life spanSES

1 0 –1 –2 2

% Overallcontribution

C 100

Native Exotic

80 60 40 20 0 2

1 0 –1 –2 2

D

F

4

MNTDSES

0 –2 –4


100 80 60

Native Exotic

40 20 0


2 MPDSES

2

4 6 8 10 12 14 Number of mounds % Plant life spancontribution

OverallSES

2

E

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2


2


4 2 0 –2 –4

2


FIG. 4. Relationships between disturbance by a fossorial rodent (number of mounds) and functional divergence (A, B), relative contribution to overall and life span functional divergence by native and exotic species (C, D) and phylogenetic community structure (E, F) of herbaceous species found at the study site. Solid lines represent significant relationships (based on LRT) between parameters and number of mounds, and the dashed lines represent the averaged GLMs (between linear and quadratic models). Dotted lines are used to separate negative SES values, which indicate phylogenetic clustering (or functional convergence), from positive SES values, which indicate phylogenetic overdispersion (or functional divergence) (A, B, E, F).

OR: growth form (k ¼ 091, P < 0001), plant life span (k ¼ 072, P < 0001) and life form (k ¼ 1, P < 0001), OR (k ¼ 090, P ¼ 035). Thus, there is a relationship between the degree of phylogenetic relatedness and trait similarity for all life history traits. In the case of plant life span and growth form, the relationship is less than that expected under a Brownian motion model of evolution, whilst life form evolves according to a Brownian process. Our results indicate that, although there is weak phylogenetic signal, all functional traits analysed were less labile than expected under a random community phylogeny. On the other hand, the results suggest that there is no phylogenetic distinctiveness between exotic and native species at the studied shrubland. The regression analyses showed that phylogenetic structures of communities were significantly related to increased disturbance (Table 1; Fig. 4E, F). Standardized effect sizes of pairwise phylogenetic distance (MPDSES) decreased significantly and linearly with disturbance (Table 1; Fig. 4E). On the other hand, the relationship between mean nearest taxon distances (MNTDSES) and disturbance resembled a convex parabola (Fig. 4F), but only the linear component/parameter (D) was significant according to LRT (Table 1). These two lines of evidence indicate that increased disturbance changed phylogenetic

structures from overdispersed to clustered, as is expected for a habitat-filtering process driven by disturbance. DISCUSSION Our results are consistent with the hypothesis that disturbance by the burrowing activity of the native fossorial rodent S. cyanus operates as a habitat filter that favours plant invasion in herb communities of the studied arid shrubland. Thus, species richness and abundance of exotic and native species increased and decreased, respectively, with disturbance. Moreover, community composition changed significantly across the disturbance gradient, with exotic species being mainly associated with communities containing more mounds of S. cyanus. Disturbance by this endemic rodent is a habitat filter that favours species with short life cycle strategies, as verified by the particular increase in abundance of this group of species. Accordingly, the relative contribution to functional divergence of exotic species increased and the relative contribution of native species decreased along the disturbance gradient. The filtering effect imposed by disturbance on the measured traits could switch phylogenetic community structure from an overdispersed pattern to a clustered one, because we found a

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significant relationship between the degree of phylogenetic relatedness and trait similarity (phylogenetic signal). We cannot rule out, however, that other unmeasured traits might be involved in the response to increased disturbance (e.g. plant height or foliar nitrogen content; Laliberte´ et al., 2013), and consequently might change phylogenetic community structure. Earlier studies in arid and semi-arid environments have reported that natural disturbance by S. cyanus favours the dominance of annual plants (Contreras et al., 1993) and can promote invasion by exotic species despite the relatively stressful conditions (Contreras and Gutierrez, 1991; Torres-Dıaz et al., 2012). It has been suggested that natural soil disturbance by fossorial rodents may favour colonization of native species over that of exotic species (Karsten et al., 2007; El-Bana, 2009) because native species should be more adapted to historic natural disturbance regimes (Alpert et al., 2000; Daehler, 2003; Huston, 2004). In fact, the use of disturbance regimes at natural or historic levels has been proposed as a tool for management of exotic plant invasion (Alpert et al., 2000; Daehler, 2003; Huston, 2004). In contrast, our results of species richness and abundance support the idea that natural disturbance is favouring the invasion of exotic species (Jauni et al., 2015). It seems that in this arid ecosystem, disturbance is detrimental to native plant species, because both species richness and abundance decreased linearly with the number of mounds. This pattern supports predictions of the Dynamic Equilibrium Model (Huston, 1979) and probably arises because disturbance worsens the already harsh conditions beyond the tolerance limits of native plants (Grime, 1977; Walker, 1999). In contrast, disturbance favours species possessing traits associated with a short life cycle, and exotic plant species certainly represent this life history strategy (Pysek and Richardson, 2007). Likewise, we found that exotic species had greater preference for more disturbed communities, while native species showed the opposite pattern. Actually, ten native species showed a significant decrease in abundance with the disturbance gradient, and 70 % of these could eventually be absent from the original pool if high levels of disturbance prevail, because their abundance tends to approach zero after a certain level of disturbance captured by our gradient (see Supplementary Data Table S4). Interestingly, we detected a significant change in community composition, but total species richness did not change along the disturbance gradient. Therefore, ecological studies on disturbance not considering species origin (native vs. exotic) could be missing important phenomena at the community level. In the same vein, had we used a categorical approach, considering only low vs. high disturbance levels, we would have missed the non-linear relationship between disturbance and abundance of exotic species and, consequently, had wrongly concluded that exotic species were equally abundant along the disturbance gradient. This highlights the advantage of a continuous approach (or multilevel approach) over a categorical one when addressing the relationship between disturbance and plant community parameters. The analysis of the relationship between disturbance and community functional divergence provides further evidence that disturbance operates as a habitat filter in low-productivity environments (Pausas and Verdu, 2010; Laliberte´ et al., 2013). Increased disturbance changed the overall trait structure from functional divergence towards convergence, which is associated with habitat filtering (Pausas and Verdu, 2010; Kraft et al.,

2015); however, only plant life span divergence showed a significant decrease. These results suggest that the combined effects of disturbance and aridity select species with short life cycles, regardless of the type of growth form or life form. Two lines of evidence suggest that a ‘live fast, die young’ life cycle strategy should be adaptive under drought and disturbance conditions (Bazzaz, 1979; Whitford and Kay, 1999). First, it has been demonstrated that in seasonally dry and variable environments, such as the studied arid shrubland, a drought escape strategy is favoured over drought avoidance (Franks, 2011). Secondly, Grime (1977) pointed out that high disturbance selects for species with features adapted to exploit transiently favourable conditions, the tendency for a short life cycle being the most consistent trait. The effect of disturbance on phylogenetic community structure depends on whether or not traits show phylogenetic signal (Webb et al., 2002; Pausas and Verdu, 2010). We found that trait evolution in the shrubland community is related to the degree of phylogenetic relatedness because all studied life history traits showed significant phylogenetic signal. Increased disturbance changed phylogenetic community structure from overdispersed (or random) to clustered. This provides additional evidence for habitat filtering as the main assembly process resulting from natural disturbance by burrowing activities of S. cyanus in this arid shrubland. At the most disturbed end of the gradient, however, communities showed a slight decrease in the degree of phylogenetic clustering. We propose two nonmutually exclusive explanations for this pattern. First, greater environmental heterogeneity generated by disturbance may allow functionally different species to occupy different microhabitats within a site, thus increasing overall functional divergence (de Bello et al., 2013; Kraft et al., 2015) and decreasing the degree of phylogenetic clustering, provided that life history traits show phylogenetic signal (Pausas and Verd u, 2010; de Bello et al., 2013). Actually, it has been shown that increased disturbance by fossorial mammals causes soil heterogeneity, because inter-mound microsites have higher cover of dominant species and different microclimatic conditions compared with mound microsites (Whitford and Kay, 1999). Secondly, competition or facilitation at the inter-mound microsites between closely related taxa might lead to reduced trait similarity (Cavender-Bares et al., 2009; Spasojevic and Suding, 2012; McIntire and Fajardo, 2014), hence reducing functional convergence. Further, this might result in phylogenetic overdispersion, provided that such traits show phylogenetic signal. Habitat filtering and limiting similarity are often viewed as alternative processes explaining community assembly (Webb et al., 2002; Cavender-Bares et al., 2009). However, both assembly processes can operate in a given community (Kraft et al., 2015), but their predominance is likely to vary with spatial scale and stress level, among other factors (Cavender-Bares et al., 2009; Spasojevic and Suding, 2012; de Bello et al., 2013; Laliberte´ et al., 2013). In our system, habitat filtering may have restricted species composition and functional divergence of communities, by species sorting, before interspecific interactions could limit the phylogenetic similarity between co-occurring species. Our results partially support these ideas because the degree of phylogenetic clustering decreased slightly at the most disturbed end of the gradient; however, the values were generally below zero along the disturbance gradient.

Escobedo et al. — Disturbance by rodents drives phylogenetic clustering and plant invasion Moreover, the functional divergence patterns of life form and growth form were random and the overall functional divergence was generally below zero along the disturbance gradient, which provides additional evidence for habitat filtering as the main assembly process in the studied shrubland. Increased species richness and abundance of exotic species can result in phylogenetic change of communities (Cadotte et al., 2010; Bennett et al., 2014), potentially leading to phylogenetically clustered communities (Winter et al., 2009). Our results illustrate a case of disturbance-driven increase in species richness and abundance of exotic species that led to phylogenetically clustered communities. These patterns arise because exotic plant species are not phylogenetically distinct from the native flora (no phylogenetic signal for species origin); this resemblance between exotic and native species has been reported at the country scale in Chile (Escobedo et al., 2011). Therefore, when the native fossorial rodent promotes the addition of exotic herbs closely related to the native herbaceous flora, it ultimately reduces the mean phylogenetic distance between taxa from the herb communities of the arid shrubland. Finally, we stress that an accurate and continuous estimation of the impact of disturbance on native/exotic species richness and abundance, as well as on community assembly processes, is not only essential for a better understanding of the dynamics of ecological communities, it is also important to avoid misleading recommendations for the management of invasive species. SUPPLEMENTARY DATA Supplementary data are available online at www.aob.oxfordjour nals.org and consist of the following. Figure S1: ranked species abundance curve. Figure S2: species accumulation curves. Figure S3: smooth surface added to the non-metric multidimensional scaling. Table S1: effect of the abundance of Bromus berteroanus on the response variables of the study. Table S2: species code. Table S3: association values of the correlation index (rUg ). Table S4: linear relationships between increased disturbance and abundance of all native species. ACKNOWLEDGEMENTS We thank Universidad de Chile for granting permits to work in Las Cardas Experimental Station, and Arancio G for plant ID. V.M.E. thanks CONICYT (Consejo Nacional de Investigaci on Cientıfica y Tecnologica) for a PhD fellowship CONICYT 21130035. This work was supported by CONICYT grant 21130035 awarded to V.M.E., FONDECYT grant 1140070 awarded to E.G., and a Rufford Small Grant 10015-1 and a DIULS Regular 2015 Grant both awarded to R.S.R. LITERATURE CITED Alpert P, Bone E, Holzapfel C. 2000. Invasiveness, invasibility and the role of environmental stress in the spread of non-native plants. Perspectives in Plant Ecology, Evolution and Systematics 3: 52–66. Anderson MJ, Walsh DC. 2013. PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: what null hypothesis are you testing? Ecological Monographs 83: 557–574. Bazzaz FA. 1979. The physiological ecology of plant succession. Annual Review of Ecology and Systematics 10: 351–371.

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