Perspectives in Plant Ecology, Evolution and Systematics 15 (2013) 328–337

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Perspectives in Plant Ecology, Evolution and Systematics

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Research article

Conservatism of responses to environmental change is rare under

natural conditions in a native grassland

∗

Jonathan A. Bennett , James F. Cahill Jr.

Department of Biological Sciences, University of Alberta, Edmonton, AB T6G 2E9, Canada

a r t i c l e i n f o a b s t r a c t

Article history: Whether or not niche conservatism is common is widely debated. Despite this uncertainty, closely related

Received 27 April 2013

species are often assumed to be ecologically similar. This principle has led to the proposed use of phyloge-

Received in revised form

netic information in forecasting species responses to environmental change. Tests of niche conservatism

23 September 2013

often focus on ‘functional traits’ and environmental tolerances, but there have been limited tests for con-

Accepted 16 October 2013

servatism in species’ responses to changes in the environment, especially in the ﬁeld. The prevalence

Available online 24 October 2013

of functional convergence and the likelihood of functional trade-offs in a heterogeneous environment

suggest that conservatism of the response niche is unlikely to be detectable under natural conditions. To

Keywords:

test the relevance of evolutionary information in predicting ecological responses, we tested for conser-

Phylogenetic community ecology

vatism (measured as phylogenetic signal) of grassland plant population responses to 14 treatments (e.g.

Phylogenetic signal

Phylogenetic niche conservatism light, nutrients, water, enemies, mutualists), each manipulated for 2–3 years, and 4 treatment categories

Belowground ecology (aboveground, belowground, resource, and herbivory) at a single site. Individual treatment responses

Grazing showed limited evidence of conservatism, with only weak conservatism in plant responses to mycorrhi-

Mycorrhizae

zae and grazing. Aspects of the response niche were conserved among monocots both aboveground and

belowground, although the pattern varied. Conservatism was limited to grazing aboveground, but below-

ground responses were conserved as a group, suggesting fundamental differences in how selection has

led to niche conservatism in aboveground and belowground environments. Overall, our results suggest

that conservatism of the response niche is not common, but is actually rare. As such, evolutionary rela-

tionships are likely to be of limited relevance for predicting species responses under ﬁeld conditions, at

least over the short time scales used in this study.

Introduction many ecological factors differentially affect certain lineages within

the community, causing phylogenetic clustering (Helmus et al.,

Plant populations often respond idiosyncratically to changes in 2010; Verdú and Pausas, 2007). This suggests that phylogeny can be

their environment (Tilman, 1987; Turkington et al., 2002). Efforts used as a tool to predict species responses to changes in their envi-

have been made to identify species characteristics that can be ronment, but for phylogeny to be a useful predictor of ecological

used to develop a predictive framework for changes in the relative responses, the niche must be conserved. However, the prevalence

abundance of plant populations (e.g. Grime, 1977; Westoby, 1998). of niche conservatism has been questioned (Knouft et al., 2006;

Based upon the idea that related species are more ecologically Lavergne et al., 2010; Losos, 2008; Silvertown et al., 2006b).

similar (Darwin, 1859), hypothesized patterns of descent (e.g. a Niche conservatism can have multiple deﬁnitions. Here, we

phylogeny) have been used with some success in determining how deﬁne niche conservatism broadly as the tendency of related

species respond to both biotic (Burns and Strauss, 2011; Reinhart species to respond similarly to abiotic or biotic environmental

et al., 2012) and abiotic (Niinemets and Valladares, 2006; Prinzing, conditions (Wiens et al., 2010; Wiens and Graham, 2005). This def-

2001; Willis et al., 2008) elements of their environments. Further, inition is more liberal than other deﬁnitions that consider niche

conservatism to require species being more similar than expected

under a model of Brownian evolution (Losos, 2008). While phy-

logenetic relatedness is often considered an integrative measure

∗

Corresponding author at: B715 Biological Sciences Building, University of of functional similarity (Mouquet et al., 2012; Webb et al., 2002),

Alberta, Edmonton, AB T6G 2E9, Canada. Tel.: +1 780 492 1577;

for plants, ecologically relevant traits are often labile (Cavender-

fax: +1 780 492 9234.

Bares et al., 2006; Grime, 2006) or environmentally plastic (Berg

E-mail address: [email protected] (J.A. Bennett).

J.A. Bennett, J.F. Cahill Jr. / Perspectives in Plant Ecology, Evolution and Systematics 15 (2013) 328–337 329

and Ellers, 2010; Burns and Strauss, 2012). Further, there are many tested for niche conservatism (as measured by phylogenetic sig-

ways to respond to different aspects of the environment. For exam- nal) in responses to each individual treatment and in responses

ple, defensive compounds are produced using different pathways, to four categories of ecological treatments representing resource,

but all reduce herbivory (Howe and Jander, 2008) and competitive herbivory, aboveground, and belowground treatment groupings.

response is associated with many traits representing different ways

of coping with reduced resource availability (Wang et al., 2010).

Materials and methods

Additionally, traits may be associated with multiple functions, yet

multiple traits may determine a species’ functional response to a Site description

given factor. High volumes of ﬁne roots can increase both nitrogen

and water uptake (Craine et al., 2003), but periodic drought tol- All experiments occurred at the approximately 5000 ha Univer-

◦

erance also requires that the plant be able to store water for later sity of Alberta research ranch at Kinsella, Alberta, Canada (53 05 N,

◦

use, which is not an adaptation related to nitrogen uptake (Craine, 111 33 W). Research occurred in three ﬁelds located in two sep-

2009). This suggests that conservatism of a trait does not mean arate sections of the ranch totalling 100 ha. Field 1 was located

that a plant’s response to one factor related to that trait can predict in the northern part of the ranch, whereas ﬁelds 2 and 3 are in

its response to other related factors. Many of the traits necessary the southern part of the ranch, with the two sites separated by

to respond to environmental conditions also involve functional approximately 6 km. The ﬁelds used are unseeded and unbroken

trade-offs, such as those between shade and drought tolerance and represent a savannah habitat with mixed grass prairie (pri-

(Niinemets and Valladares, 2006). As a consequence, plant species marily Hesperostipa curtiseta (Hitchc.) Barkworth, Poa pratensis L.

may be suited to cope with certain environmental conditions, but and Festuca hallii (Vasey) Piper) interspersed with stands of aspen

not others. Thus, for many reasons, ecological responses are often (Populus tremuloides Michx.). Though historically lightly grazed by

less conserved than morphological or physiological traits (Losos, cattle, grazing was halted for the duration of each experiment.

2008; Prinzing, 2001). This suggests that evolutionary informa- As is true for many grasslands (Foster et al., 2004; Silvertown

tion may be of limited use for predicting how species respond to et al., 2006c; Tilman, 1996), plant community structure and func-

environmental conditions in nature. tion varies spatially and temporally. Soils at the site have a thin

When suites of traits appear to confer speciﬁc functioning, they topsoil layer over glacial till (Lamb, 2008), but are spatially vari-

have often been grouped into plant functional strategies (Reich able in texture, chemistry, and topography (Bennett et al., 2013).

◦

et al., 2003; Westoby, 1998). Most commonly, plant strategies are The site has an average annual temperature of 2.8 C and receives

associated with responses to resource availability and disturbance, approximately 430 mm of precipitation in an average year, but is

where some species are adapted to quick growth and rapid resource subject to periodic drought (Cahill, 2003). Fig. 1 shows the vari-

acquisition, while others are adapted to disturbances such as her- ability in species richness, productivity, and phylogenetic diversity

bivory (Craine, 2009; Grime, 1977; Reich et al., 2003). Responses to over the duration of the experiments. These data were taken from

both resources and herbivory are often consistent within broad, un-manipulated plots at the ﬁeld site, with species richness and

phylogenetically distinct functional groups (Coughenour, 1985; phylogenetic diversity data derived from cover estimates (0.25 m )

Lavorel et al., 1997; Niinemets and Valladares, 2006; Turkington and productivity estimates from live biomass clipped in small plots

et al., 2002), yet the evidence for conservatism of traits represent- (0.10 m ), dried, and weighed. Phylogenetic diversity was calcu-

ing these plant strategies is mixed (Brunbjerg et al., 2012; Diaz lated using the constructed phylogeny (see below) as abundance

et al., 2004). While there are a few experimental tests for conser- weighted mean phylogenetic distance (Webb et al., 2002) using the

vatism of plant strategies, to our knowledge, no studies have tested independent swap null model (Gotelli, 2000) in the picante package

whether population responses to multiple treatments related to in R (Kembel et al., 2010). Species richness and productivity were

these strategies are conserved. variable among years and across ﬁelds, with ﬁeld 1 having higher

Plant strategies require coordinated responses to multiple envi- species richness and productivity than ﬁelds 2 and 3. Phyloge-

ronmental factors, both above- and belowground. This requires netic diversity was much more consistent across ﬁelds, with limited

that root and shoot traits co-vary. There is evidence for such interannual variation (Fig. 1), suggesting greater consistency in the

covariance (Craine et al., 2001, 2002), although root and shoot phylogenetic structure of the community.

traits may have evolved independently (Kembel and Cahill, 2011).

Individual root and shoot traits show varying degrees of conser-

Data selection

vatism (Anderson et al., 2011; Comas et al., 2012; Diaz et al.,

2004; Grime and Mackey, 2002; Kembel and Cahill, 2005, 2011), Data were taken from six separate multi-year multi-factorial

as do plant responses to various above- and belowground factors experiments, containing a total of 14 treatments (Table 1). Within

(Niinemets and Valladares, 2006; Prinzing, 2001; Silvertown et al., each independent experiment, interactions among the treatments

2006b). However, it is unclear whether plant responses to either were included in the original study. However, we do not have data

aboveground or belowground factors as groups would be phylo- testing the interactive effects of all treatments, so we limit our anal-

genetically conserved and there are no experimental tests of this yses to main effects, though we recognize complex interactions

concept. among this number of treatments can occur. For each treatment,

To test whether related species responded similarly to changes we only used plots where a single treatment was applied and

in their environment, and thus if response niches were conserved, compared those treatment plots to a control plot with no treat-

we synthesized the results of six short-term (2–3 years) experiments applied within the same block. Grazing was simulated by

ments conducted in a single grassland system within the Aspen clipping plants at either low intensity (7 cm stubble height) or

Parkland eco-region of Canada. In total, 14 abiotic and biotic treat- high intensity (3 cm stubble height; White et al., 2012). Fertilizers

ments were manipulated: aboveground insecticide; belowground were applied either as ammonium nitrate (5.4 g N/m ) for nitro-

insecticide; contact fungicide; drought; ﬁxed interval watering; gen only (Lamb, 2008) or as a slow-release fertilizer for NPK at

2 ®

high intensity clipping; litter removal; low intensity clipping; 5.2 g NPK/m (applied as 14:14:14 Osmocote Classic, Scotts, Ben-

nitrogen addition; nitrogen, phosphorus and potassium (NPK) nett et al., in preparation). Fixed interval watering increased total

addition; shading; systemic fungicide; variable interval watering; precipitation by 50% through weekly water addition (Lamb, 2008).

and warming. From population responses to these treatments, we Drought treatments decreased precipitation by 60% using rainout

330 J.A. Bennett, J.F. Cahill Jr. / Perspectives in Plant Ecology, Evolution and Systematics 15 (2013) 328–337

decrease nutrient availability (Sardar and Kole, 2005) and can

be harmful to other organisms (vandenBrink et al., 1996). Beno-

myl is commonly used to suppress arbuscular mycorrhizal fungi

(e.g. Hartnett and Wilson, 1999), but it also has effects on non-

target organisms and can increase available nitrogen (Allison et al.,

2007). Rovral has also been used to suppress mycorrhizal fungi

(Gange et al., 1990), but has fewer documented effects on non-

target organisms (Ganade and Brown, 1997) and no detectable

effects on soil nutrient availability (J.A. Bennett, unpublished data).

Detailed methods for each treatment can be found in the origi-

nal manuscripts. Additional methods details for the unpublished

experiment are found in Table 1.

Relative abundance was estimated as percent vegetative cover,

a commonly used method to assess relative change within herba-

ceous plant communities (Lamb and Cahill, 2008; Tilman, 1987).

Most experiments were 2–3 years long, but some experiments ran

for longer than 3 years and only percent cover estimates were col-

lected in the interim as destructive harvesting was unfeasible. To

minimize the variation in experimental duration, we chose to limit

experimental duration to 3 years. Across all experiments, we calcu-

lated the responses of 54 different species to at least one treatment,

with an additional six species included when calculating aggregate

responses to treatment categories (see below). For most species,

we were able to calculate responses to approximately half of the 14

treatments (mean 7.1, standard deviation 4.19), although species

did vary in how often we were able to calculate responses (see

Figure A1). Our abundance estimates were the mean of three cover

estimates taken over the growing season (late spring, mid-summer,

and late summer) from 0.25 m sub-plots within each larger con-

trol or treatment plot. Changes in relative abundance for each

species were calculated as the log response ratio of abundances

(ln(treatment/control)) for each pair of treatment and control plots.

The log response ratio was used instead of percent change to nor-

malize responses (Hedges et al., 1999). As many experiments were

multi-factorial, control plots within a given block were used in

the calculation of responses to multiple treatments. For exam-

ple, when calculating responses to aboveground and belowground

insect suppression, the control plot where no treatments were

applied was used to calculate responses to both aboveground insect

suppression and belowground insect suppression. However, plots

where insects were suppressed above- and belowground were not

Fig. 1. Inter-annual variability in (B) species richness, (C) phylogenetic diversity,

included in any calculations. From these measurements, we calcu-

calculated as abundance weighted mean phylogenetic distance, and (D) standing

lated the average response of a species to each treatment and the

biomass over the course of the 14 experimental manipulations. Panel A shows the

standard error of that estimate. By using the average response of

time frame over which each of the manipulations was conducted. In panels B–D,

empty circles show conditions in ﬁeld 1, grey circles in ﬁeld 2, and black circles a species, we ignore the potential variation in how individuals of

in ﬁeld 3. Experimental manipulations abbreviated as follows: AI – aboveground a given species respond to a treatment due to neighbour compo-

insecticide, BI – belowground insecticide, CF – contact fungicide, D – drought, FW –

sition or local environmental conditions. Given that we are testing

ﬁxed interval watering, HC – high intensity clipping, LC – low intensity clipping, LR

the generality of niche conservatism and the utility of evolutionary

– litter removal, N – nitrogen addition, NPK – NPK addition, S – shade, SF – systemic

fungicide, VW – variable interval watering, and W – warming. Error bars in panels information for informing ecology under natural conditions, the

B–D represent standard error. particular set of conditions under which related species respond

similarly is not of interest in the current study.

For each treatment, the mean change in abundance across

shelters (White et al., 2012). This water was collected and added to populations and its 95% conﬁdence intervals were estimated

plots within 24 h following rainfall for the variable interval water- using the average response of each species to each treatment in a

ing treatment (White et al., 2012). Shade cloth was used to reduce mixed model in SPSS (v. 19.0). We only included species for which

light by 73% (Lamb, 2008), open-top chambers were used to warm we could calculate the standard error for a given treatment and

◦

plots by approximately 3 C (White et al., 2012), and litter was weighted species responses by the inverse of that standard error.

removed by raking (Bennett et al., in preparation). Insects were We also attempted to account for additional sources of variation by

suppressed using chlorpyrifos with Lorsban 4E (Dow) used for including a number of random factors, including year of data col-

aboveground insects and Lorsban 5G (Dow) for belowground lection and experimental duration. As experiments at the site were

insects (Clark et al., 2012; Coupe et al., 2009). Fungi were sup- spatially distinct, we included experimental identity to account for

pressed using both a systemic fungicide (Benomyl, Dupont Inc.; spatial variability among and within ﬁelds, but nested it within year

Cahill et al., 2008a) and a contact fungicide (Rovral , Bayer; Ben- as data from multiple experiments was collected in most years.

nett et al., in preparation). As with all pesticides, each of the Species identity was also included as a random factor to account

pesticides used has non-target effects. Chlorpyrifos is known to for differences in species pool across factors. Thus, we included

J.A. Bennett, J.F. Cahill Jr. / Perspectives in Plant Ecology, Evolution and Systematics 15 (2013) 328–337 331

Table 1

Meta data for each treatment included in the analysis.

a b c d e

Treatment Category Harvested Length (years) Field Species N Dir. Methods

Aboveground insecticide A,H 2003, 2005 2, 3 1, 2 48 22 + Clark et al. (2012) and Coupe et al. (2009)

Belowground insecticide B,H 2005 3 1 41 10 + Coupe et al. (2009)

Contact fungicide U,U 2010 3 1 41 20 ? Bennett et al. (in preparation)

Drought B,R 2010 3 3 10 5 − White et al. (2012)

Fixed watering B,R 2005 3 1 46 22 + Lamb (2008)

High clipping A,H 2010 3 3 15 5 − White et al. (2012)

Litter A,U 2010 2 1 41 20 ? Bennett et al. (in preparation)

Low clipping A,H 2010 3 3 15 5 − White et al. (2012)

Nitrogen B,R 2005 3 1 45 22 + Lamb (2008)

NPK B,R 2010 2 1 41 20 + Bennett et al. (in preparation)

−

Shading U,U 2005 3 1 45 22 Lamb (2008)

Systemic fungicide U,U 2005 3 1 38 20 ? Cahill et al. (2008a)

Variable watering B,R 2010 3 3 12 5 + White et al. (2012)

Warming U,U 2010 3 3 16 5 ? White et al. (2012)

High and low refer to the intensity of clipping; above and below refer to aboveground and belowground; ﬁxed and variable refer to the interval of watering.

Treatments are classiﬁed as aboveground (A) or belowground (B) and herbivory (H) or resource-based (R). Treatments we could not classify are categorized as unknown (U).

Species refers to the number of species for which we could calculate the standard error of their response to that treatment, allowing us to estimate their response to that treatment.

N refers to the number of paired treatment and control plots in the experiment where the treatment was applied.

Treatments were classiﬁed as having a positive (+), negative (−) or unknown (?) hypothesized direction of effect.

f ® 2

Rovral (Bayer) was applied to half the plots at a rate of 0.36 g/m active ingredient (iprodione) every two weeks. Litter was raked each spring in all plots, replaced in

control plots and disposed of in litter removal plots. Fertilizer was added as 3- to 4-month slow release 14:14:14 nutrient pellets (Osmocote , Scotts) each spring at a rate

of 5.22 g NPK/m .

treatment as a ﬁxed effect and the calendar year the data was present except amongst close relatives within Poaceae and Aster-

collected, the duration of the experiment, experiment identity aceae (Fig. A1). Polytomies at the tips of a phylogenetic tree are

nested within year and species identity as random effects in the unlikely to inﬂuence analyses of phylogenetic signal (Münkemüller

model. In the ﬁnal model, we retained only species identity among et al., 2012; Swenson, 2009).

the random effects as the other random effects explained no

additional variation, resulting in a Hessian matrix that was not Niche conservatism

positive deﬁnite.

Given that there is spatial and temporal heterogeneity in local

Our deﬁnition of niche conservatism – related species respond

community processes (Fig. 1), we explored the amount of variation

similarly to ecological factors – is broad and our approach is holis-

explained by year and experimental identity relative to the treat-

tic in its focus on population outcomes, rather than trait-focused

ments to evaluate our decision to exclude them from the model. We

measures of plant morphology or physiology. We used three sep-

ran a mixed model with year, experimental identity nested within

arate methods to test for phylogenetic signal as a proxy for niche

year, and treatment identity nested within experimental identity

conservatism: Blomberg’s K (Blomberg et al., 2003), Pagel’s (Pagel,

within year as ﬁxed factors. As in the previous model, species

1999), and the decomposition of trait variation (Pavoine et al.,

identity was included as a random effect and species responses

2010). The ﬁrst two methods assess whether the distribution of

were weighted by the inverse of the standard error. Only treat-

traits (or in this case population responses) among species fol-

ment identity (F = 2.73, P = 0.004) and not experiment identity

9,421 lows a Brownian motion model of evolution. The third method

(F = 1.34, P = 0.261) or year (F = 1.45, P = 0.236) explained

3,450 2,456 assesses response diversity among all the species descending from

signiﬁcant variation in species responses, supporting our decision

each branch of each node of the phylogenetic tree, measured as

to remove these random factors. We recognize that this does not

quadratic entropy (Rao, 1982). This information is used to gen-

account for potential differences in how species may respond to

erate both a visual display of where divergence occurred along

treatments in different years, but given the nature of the data such

the tree and uses randomization procedures to determine if there

a test is not feasible.

is signiﬁcant phylogenetic signal. The randomization tests for the

response decomposition analyses indicate whether response vari-

Phylogenetic information ation is skewed towards a single node, a few nodes, the root, or the

tips (Pavoine et al., 2010). Variation skewed towards the root or

Phylogenetic information was extracted from the molecu- towards one or few nodes can be used to infer niche conservatism or

lar phylogeny outlined in Bennett et al. (2013) that sampled at least differentiation, whereas variation skewed towards the tips

146 species across 35 families found at the study site (see suggests convergence. However, careful examination of how vari-

Fig. A2). The phylogeny was based on a 1400 bp section of the ation in responses is distributed across the nodes of the phylogeny

ribulose-biphosphate carboxylase gene (rbcL) and constructed is required to infer patterns of niche conservatism.

using standard techniques. Although the phylogeny only sampled Before quantifying phylogenetic signal, we created separate

one gene, sequence variation in rbcL was sufﬁcient to resolve rela- phylogenetic trees for each experimental treatment, for a total of

tionships with strong support. Deeper branching patterns were 14 trees. Each tree was created by pruning the full phylogenetic

consistent with published angiosperm phylogenies based on mul- tree to include only species for which we had a response value

tiple genes (Bremer et al., 2009; Soltis et al., 2011) and topology with an associated error measurement in that treatment. We cal-

within families were largely consistent with published phyloge- culated both K and and tested their signiﬁcance using the phylosig

nies for the Poaceae (Döring et al., 2007), Asteraceae (Selliah and function in the GEIGER package in R (Harmon et al., 2008). To

Brouillet, 2008), Rosaceae (Dobesˇ and Paule, 2010), and Brassi- decompose trait variation, we used an updated version of the R

caceae (Beilstein et al., 2008). In addition, few polytomies are scripts from Pavoine et al. (2010) provided by the author in the

332 J.A. Bennett, J.F. Cahill Jr. / Perspectives in Plant Ecology, Evolution and Systematics 15 (2013) 328–337

Fig. 2. Average change in relative abundance following manipulation of various individual treatments (above heavy solid line) and treatment categories (below solid line)

applied to a native grassland. Treatment and treatment category effects are arranged in descending order of the absolute value of the average response. Dots represent the

estimated marginal mean of the log response ratio with error bars showing the 95% conﬁdence intervals of that estimate. Numbers following treatment names represent

the number of species measured followed by the number of replicates for individual treatments and the number of species measured for treatment categories.

ade4 package in R (Chessel et al., 2004). Responses were considered availability and herbivory responses (Grime, 1977; Reich et al.,

to be conserved if the tests for phylogenetic signal indicated that 2003), while the second set of categories test whether the phyloge-

there was signiﬁcant variation at one or a few nodes that represent netic conservatism seen for many root and shoot traits (Anderson

deep branches within the phylogeny. A more thorough explanation et al., 2011; Cahill et al., 2008b; Comas et al., 2012; Kembel and

of these methods can be found in the online Appendix. Each test for Cahill, 2005, 2011) resulted in conservatism in species responses

phylogenetic signal was conducted for each individual factor with to aboveground and belowground treatments. Before estimating

both ultrametric and non-ultrametric trees. The results were simi- responses to treatment categories, we standardized the direction

lar, and thus we only present those using the non-ultrametric tree. of effect such that each treatment was expected to negatively affect

In addition to assessing niche conservatism in response to each population growth (Table 1). For example, the effects of water addi-

individual treatment, we also assessed conservatism of responses tion were made negative, whereas drought was left as is. We used

to broad categories of treatments (Table 1). The ﬁrst set of cat- these adjusted species responses to the individual treatments to

egories represent plant strategies for responding to resource estimate species responses to each of the treatment categories. For

Table 2

Phylogenetic signal in individual treatments and treatment categories.

d e *

Treatment type # Species Signiﬁcance of skewness (P) Blomberg’s K Pagel’s

a b c

Single node Few nodes Root/tip K P P

Aboveground insecticide 40 0.53 0.397 0.278 0.109 0.597 6.61E−05 1.000

Belowground insecticide 35 0.506 0.934 0.229 0.024 0.985 6.61E−05 1.000

Contact fungicide 33 0.788 0.621 0.469 0.132 0.651 6.61E−05 1.000

Drought 9 0.056 0.14 0.248 0.443 0.407 6.61E−05 1.000

Fixed interval watering 41 0.918 0.987 0.412 0.137 0.301 6.61E−05 1.000

High intensity clipping 12 0.913 0.894 0.847 0.349 0.169 0.010 0.976

Litter removal 34 0.952 0.445 0.553 0.160 0.170 6.61E−05 1.000

Low intensity clipping 13 0.635 0.042 0.278 0.366 0.181 0.093 0.723

Nitrogen addition 42 0.679 0.112 0.566 0.058 0.801 6.61E−05 1.000

NPK addition 33 0.521 0.737 0.508 0.136 0.649 6.61E−05 1.000

Shading 39 0.650 0.882 0.679 0.158 0.114 6.61E−05 1.000

Systemic fungicide 34 0.033 0.668 0.591 0.146 0.355 6.61E−05 1.000

Variable interval watering 10 0.968 0.906 0.309 0.433 0.168 0.407 0.373

Warming 10 0.884 0.989 0.254 0.253 0.771 6.61E−05 1.000

Aboveground (agg) 54 0.149 0.592 0.435 0.107 0.379 6.61E−05 1.000

Belowground (agg) 53 0.029 0.628 0.292 0.110 0.415 0.214 0.055

Herbivory (agg) 49 0.099 0.456 0.359 0.061 0.801 6.61E−05 1.000

Resource (agg) 50 0.188 0.244 0.590 0.091 0.567 0.100 0.319

Values signiﬁcant at ˛ = 0.05 are bolded.

Single node skewness refers to situations where a single node (branching point) on the phylogenetic tree accounts for most of the variation in plant responses.

Similarly, few nodes skewness refers to situations where a small number of nodes can explain variation in plant responses.

Root/tip skewness occurs when most of the variation in plant responses can be explained by either deep branches in the tree or by variation among the tips of the tree.

Responses to aggregated categories of treatments are denoted by (agg) and represent model estimated mean responses by individual species to all treatments that ﬁt in

that category (Table 1).

The number of species represents the number of species included in that analysis of phylogenetic signal and is limited to the species for which we could calculate a mean

response to that treatment or treatment category.

J.A. Bennett, J.F. Cahill Jr. / Perspectives in Plant Ecology, Evolution and Systematics 15 (2013) 328–337 333

this estimation, we used mixed models, one for each set of treat-

ment categories, with only species with at least three response

values in a category included in the models. Within these models,

we also included a number of random effects to account for other

potential sources of variation. We initially included treatment cat-

egory and species identity as ﬁxed effects with treatment identity

nested within treatment category, experimental duration, calen-

dar year of harvest, and experiment identity included as random

effects. However, we only retained one random effect in both ﬁnal

models, treatment identity nested within treatment category, as it

was the only random effect that explained any variation. From the

models, we estimated (as marginal means) both the mean response

to the treatment categories across species and the response of

the individual species to the same treatment categories. These

species-speciﬁc category means were then used in our phyloge-

netic analyses, following the same methods as described for the

individual treatments.

Results

As expected, species varied in their responses to the individ-

ual treatments, with only high intensity clipping and shading

causing signiﬁcant net change across populations (Fig. 2). Pop-

ulation responses to individual treatments were generally not

conserved (Table 2). We found no evidence of conservatism for

individual treatments as measured using Blomberg’s K or Pagel’s

, but population responses to 2 of 14 treatments (systemic fungi-

cide application and low intensity clipping (Fig. 3 and Table 2))

were similar among related species according to the skewness

tests. Variation in plant responses to systemic fungicide applica-

tion was skewed towards a single node differentiating Asterids,

which mostly responded negatively, from the other core eudicots,

which generally showed positive responses (Fig. 3A). Conversely,

variation in responses to low intensity clipping was skewed

towards multiple nodes representing variation within the Aster-

aceae, within the Poaceae, and between monocots and eudicots,

where monocots increased following clipping and eudicots were on

average neutral (Fig. 3B). This weak evidence of niche conservatism

suggests that evolutionary history does little to predict how species

respond to environmental conditions under natural conditions.

Similar to the individual treatments, there was no evidence of

conservatism in species’ responses to the factor groupings when

measuring Blomberg’s K, but there was some evidence of conser- Fig. 3. Phylogenetic signal in plant species’ responses to (A) contact fungicide appli-

vatism using Pagel’s and the skewness tests. Speciﬁcally, we cation and (B) low intensity clipping depicted graphically as response diversity

decomposed across a community phylogeny. TQE is the total quadratic entropy

found evidence for niche conservatism in population responses

(response diversity) and the size of the circle at a given node represents the pro-

to the group of belowground treatments, but not to groups of

portion of entropy concentrated at that node, which corresponds to the amount

aboveground, top-down, or bottom-up treatments (Table 2 and

of divergence at that node. The bar graphs on the right of each panel show the

Fig. 4A). Variation in species responses to belowground treatments response of species at that tip location to that treatment, with monocots and eudi-

cots separated by the bar on the left and the major plant families in boxes of each

was signiﬁcantly skewed towards a single node corresponding to

panel.

a split between monocots and eudicots (Fig. 4B), where monocots

declined strongly in response to belowground stresses and eudicot

responses were variable, but on average positive.

et al., 2004; Silvertown et al., 2006b). Some of this variability in

niche conservatism may be due to the spatial scale at which niche

Discussion conservatism is measured. Local scale niches (˛ niches) are thought

to be more labile than habitat niches (ˇ niches) (Silvertown et al.,

Plant species varied in their population responses to the dif- 2006a), and empirical ﬁndings suggest that niches are often

ferent individual treatments, but these responses showed only poorly conserved (Prinzing et al., 2008; Silvertown et al., 2006a,b).

occasional and weak evidence of niche conservatism. The results However, for our study region, trait conservatism is stronger within

˛ ˇ

of previous studies on ecological responses and environmental sites ( traits) than among sites ( traits) (Kembel and Cahill,

niches have been inconsistent as well, with some studies show- 2011). This suggests that other factors, besides scale, have led to

ing strong conservatism (Burns and Strauss, 2011; Prinzing, 2001; a lack of response niche conservatism at the site. Further, for sites

Reinhart et al., 2012; Willis et al., 2008), others weak conservatism where niches are not conserved at local scales (Prinzing et al., 2008;

(Niinemets and Valladares, 2006; Thuiller et al., 2011), mixed con- Silvertown et al., 2006a), responses to environmental change are

servatism (Cahill et al., 2008b), or no conservatism (Cavender-Bares even less likely to be conserved. There are many reasons for niche

334 J.A. Bennett, J.F. Cahill Jr. / Perspectives in Plant Ecology, Evolution and Systematics 15 (2013) 328–337

Fig. 4. Phylogenetic signal in plant species’ responses to (A) aboveground and (B) belowground treatments. The size of the circle at a given node represents the contribution

of that node to total diversity in responses. The bar graphs show the average response of the species at that tip location on the tree to either aboveground or belowground

stresses and disturbances. Monocots and eudicots are shown along the left hand side of panel A and the major grassland plant families are enclosed within boxes.

conservatism to be variable, including the niche axis considered, species abilities to take up different resources. Conversely, both

its relationship to local environmental conditions, the nature of shading and clipping had large effects on population abundances

the species pool, and the need to adapt to a diverse set of selective and there are known trade-offs between shade and herbivory tol-

forces (Grime, 2006; Losos, 2008; Prinzing et al., 2008). We suggest erance (McGuire and Agrawal, 2005), which could limit a species

that functional convergence needs to also be considered. There are ability to be respond to multiple aboveground treatments. This sug-

many ways to accomplish different ecological tasks (e.g. mycorrhi- gests that there may be different modes of selection inﬂuencing

zae or root traits for nutrient acquisition (Lambers et al., 2008)), how species are able to respond to aboveground and belowground

and thus there is a high likelihood of functional convergence even treatments.

if different sets of traits are conserved among lineages. Our ﬁnding Despite differences in conservatism of responses among mono-

of limited conservatism of responses, despite morphological trait cots in how they responded to belowground treatments and

conservatism at the site (Kembel and Cahill, 2011) supports this grazing, we did not ﬁnd a similar pattern for resource and herbivory

concept. responses. Selective forces related to resource capture are expected

In the current study, when evolutionary history explained any to cause convergent evolution (Grime, 2006) and there are known

of the variation in species responses, it was primarily related trade-offs between belowground resource capture (high root allo-

to differences between monocots and eudicots. This result is cation) and shade tolerance (high shoot allocation) (Valladares

consistent with the large differences between monocots and and Niinemets, 2008). Both mechanisms could limit the conser-

eudicots in belowground traits and root foraging (Grime and vatism of resource responses. However, trade-offs alone could

Mackey, 2002; Kembel and Cahill, 2005) and responses to her- have limited conservatism of herbivory responses. There are also

bivory (Coughenour, 1985). Further, it is consistent with broad resource allocation trade-offs between herbivory tolerance and

differences between monocot and eudicot crop species in how resistance (Agrawal and Fishbein, 2006) which could limit con-

they respond to belowground resources and stresses (Richmond servatism of responses to herbivory in general. Further, insect

and Sussman, 2003; Sadras and Milroy, 1996). However, mono- herbivory is variable in its form (Crawley, 1989) and although

cot, but not eudicot, responses to the treatments were conserved; grasses may be adapted to grazing (Coughenour, 1985), it seems

monocots decreased in abundance when experiencing below- unlikely that any species would be well adapted to all forms of her-

ground stresses, but increased following simulated herbivory. This bivory. However, more evidence is necessary before we can draw

response conservatism ﬁts with the general conservatism of traits any ﬁrm conclusions.

related to gathering soil resources (e.g. adventitious root growth Of the treatment responses which showed evidence of conser-

and high root allocation) and regrowth following grazing (e.g. basal vatism, only systemic fungicide, which suppressed mycorrhizae

meristem and high root allocation) across graminoids and many (Cahill et al., 2008a), was conserved among groups other than

monocots (Chase, 2004; Coughenour, 1985). However, it is inter- the monocots. Here, we found that Asterids generally decreased

esting that belowground responses were conserved as a group, following mycorrhizal suppression, whereas other core eudicots

but only grazing responses were conserved aboveground. In this mostly increased. Other recent studies found variation among grass

system, belowground insect suppression had minimal effect, caus- tribes in how they responded to mycorrhizae (Reinhart et al., 2012),

ing belowground responses to be driven by belowground resource but there were differences in both methodology (e.g. inoculation

responses. Having a large root system already in place is going to be vs. suppression, greenhouse vs. ﬁeld) and species pool between

advantageous following resource pulses, regardless of the nature of the two studies that make comparison difﬁcult without further

the resource. Given that we saw no evidence for conservatism in work. However, it does suggest that there are phylogenetic func-

species responses to individual belowground treatments, it sug- tional groups in mycorrhizal response, but that these groups vary

gests that niche differentiation among monocots may come from contextually.

J.A. Bennett, J.F. Cahill Jr. / Perspectives in Plant Ecology, Evolution and Systematics 15 (2013) 328–337 335

If niche conservatism is truly common (Wiens et al., 2010), belowground functions (e.g. nitrogen or water uptake), despite

then there should be an emergent pattern in how related species morphological and foraging similarities.

respond to certain conditions. Our results suggest that conser-

vatism of plant responses to environmental change, under natural Acknowledgments

conditions, is in fact rare. However, these results are limited to

short-term responses to each of the treatments and do not nec-

We would like to thank E.W. Bork, S.R. White, E.G. Lamb, B.H.

essarily reﬂect how species respond to long-term environmental

Shore, M.R. Clark, and M.D. Coupe for supplying the original data,

changes. Although most experiments are of similar length to those

A.E. Nixon and M.W. Cadotte for their helpful comments, and S.

used in this study, plant community responses to long-term manip-

Pavoine for providing updated versions of the R scripts. We would

ulations are often different than those witnessed over shorter

also like to thank Jack Welch, Barry Irving and the rest of the staff

intervals (e.g. Silvertown, 1980). Therefore, responses to long-

at the University of Alberta research ranch at Kinsella, for their

term changes may be conserved, resulting in the loss of some

help facilitating a decade of ﬁeld research. J.F.C. oversaw the devel-

lineages and the addition of others; however, we are unable to

opment and execution of all original datasets. J.F.C. originated the

address this issue with the current data. Plant responses to indi-

broader concept of comparing among all experimental treatments.

vidual factors can also vary spatially and temporally depending

J.A.B. developed the concepts of this particular study. J.A.B. con-

on soil conditions, neighbour identity, and climate (Bertness and

ducted all analyses. J.A.B. wrote the paper and J.F.C. edited the

Callaway, 1994; Knapp et al., 2002; Pennings et al., 2005; Pulliam,

manuscript. J.A.B. was supported by an NSERC PGS-D scholarship.

2000; Reader et al., 1994), but they can also be remarkably con-

This work was funded by a NSERC Discovery Grant and Discovery

sistent across sites with highly diverse conditions (Pennings et al.,

accelerator award to J.F.C. Funding sources for the original studies

2005). Although, site conditions and community properties var-

are listed within the associated manuscripts.

ied among the years over which the different experiments were

conducted, phylogenetic diversity, with few exceptions, remained

Appendix A. Supplementary data

relatively consistent among years and locations. Thus, we see no

reason we should expect a bias in how different lineages would

Supplementary material related to this article can be

respond to certain treatments or treatment categories depending

found, in the online version, at http://dx.doi.org/10.1016/j.ppees.

on current conditions. It is possible that under more controlled con-

2013.10.001.

ditions we would have found greater evidence of conservatism,

but such a requirement would limit its applicability to natural

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