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Carex ornithopoda*. Carorn. Trifolium pratense†. Inula salicina. Inusal. Sesleria caerulea*. Leontodon hispidus. Leohis. Sesleria caerulea*. Succisa pratensis.

Journal of Ecology 2013, 101, 1313–1321

doi: 10.1111/1365-2745.12127

Plants are least suppressed by their frequent neighbours: the relationship between competitive ability and spatial aggregation patterns Marina Semchenko*, Maria Abakumova, Anu Lepik and Kristjan Zobel Department of Botany, Institute of Ecology and Earth Sciences, University of Tartu, Lai 40, Tartu 51005, Estonia

Summary 1. Previous studies have concluded that spatial aggregation of conspecifics should benefit weak competitors and put stronger competitors at a disadvantage, thus promoting plant species coexistence. However, if competitive ability is viewed as a behavioural trait, it becomes evident that traits determining spatial patterns and competitive ability could co-evolve, resulting in greater dispersal in stronger competitors and reduced competitive ability in spatially aggregated species. 2. To test this prediction, we combined spatial data from a field survey of seven temperate grassland communities with the results of a common-garden competition experiment involving 28 focal species. 3. We found that species exhibiting strong conspecific aggregation and infrequent heterospecific encounters in the field maintained greater growth in competition with conspecifics than with heterospecifics. In contrast, species that mostly encountered heterospecific neighbours in the field achieved greater growth when surrounded by heterospecific than conspecific neighbours, indicating greater competitive ability. The observed patterns of conspecific aggregation were related to variation in clonal dispersal characteristics and there was a direct positive relationship between clonal dispersal distance and competitive ability. 4. Synthesis. Our study demonstrates that viewing competitive ability as a behavioural trait that imposes different costs and benefits on an individual depending on the identity of its neighbours can provide new insights into the long-debated topic of mechanisms promoting plant species coexistence. Key-words: competitive response, dispersal ability, growth form, intraspecific aggregation, plant– plant interactions, spatial patterns, species coexistence

Introduction Community spatial structure has been identified among the main factors determining the likelihood of stable plant species coexistence (Amarasekare 2003; Bolker, Pacala & Neuhauser 2003). Theoretical and empirical studies show that spatial aggregation of conspecifics can promote coexistence, as frequent within-species interactions improve the performance of inferior competitors but put superior competitors at a disadvantage (Pacala 1997; Stoll & Prati 2001; Turnbull et al. 2007; Wassmuth et al. 2009). While spatial competition models identify conditions under which species coexistence is possible, they give little insight into the way in which traits

*Correspondence author. E-mail: [email protected]

determining the intensity and frequency of interactions could evolve to benefit individuals. Competitive ability can be viewed as a behavioural trait that imposes different costs and benefits on an individual plant depending on the identity of its closest neighbours. It can therefore be considered in the context of evolutionary game theory, which has proved to be one of the most powerful tools used to study trait evolution in organisms ranging from bacteria to humans (Rankin, Bargum & Kokko 2007) and is being increasingly employed in plant studies (Gersani et al. 2001; Anten 2002; Falster & Westoby 2003; Dudley & File 2007; O’Brien, Brown & Moll 2007; Semchenko, John & Hutchings 2007; Dybzinski et al. 2011; Hikosaka & Anten 2012). Game-theoretic models predict that the presence of neighbours should trigger increased investment into competitive organs (roots in conditions of nutrient limitation and/or stems

© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society

1314 M. Semchenko et al. where light is limiting) at the expense of reproduction, as such behaviour ensures high competitive ability through capture of additional resources that would otherwise be acquired by competitors (Gersani et al. 2001; Anten 2002; Falster & Westoby 2003). Increased allocation to competitive organs is a selfish trait that ensures the highest pay-off to an individual in a competitive environment. If all individuals exercised cooperative restraint in the use of common resources (in this case, limited allocation to competitive organs), higher fitness would be achieved compared with a group of selfish individuals (Pepper & Smuts 2002; Kerr et al. 2006; Nahum, Harding & Kerr 2011). However, when faced with selfish individuals, a cooperative strategy will result in poor competitive ability. Cooperative behaviour can only spread in a population if it is primarily directed towards other cooperators. This condition can be fulfilled in a number of ways, but maybe the most relevant and empirically demonstrated for plants is through spatial aggregation of genetically closely related individuals due to limited dispersal (Doebeli & Hauert 2005; also known in the context of inclusive fitness or kin selection theory, Hamilton 1964; Gardner, West & Wild 2011). If individuals frequently encounter both close relatives and unrelated competitors, kin discrimination ability and selective avoidance of competition with kin should be favoured, but the evolution of such ability in plants may be constrained (File, Murphy & Dudley 2012; Lepik et al. 2012). Some perennial plant species mainly reproduce through clonal propagation and place offspring at very close proximity, resulting in groups of genetically identical individuals (Turkington & Harper 1979; Lovett Doust 1981; McLellan et al. 1997). In such species, indiscriminate avoidance of competition with all neighbours can be favoured since interactions with unrelated individuals are rare while kin selection is particularly strong as clonally produced individuals are genetically nearly identical (Semchenko, John & Hutchings 2007; Cornwallis, West & Griffin 2009). The selective advantage of competition avoidance is also reinforced by the facts that it precludes intense sibling competition, which would otherwise counteract kin selection, and it confers a direct fitness benefit, as fewer resources are invested into competitive organs and more is dedicated to reproduction (Griffin & West 2002). Thus, just as competition theory predicts that spatial aggregation of conspecifics should aid weak competitors and species coexistence, aggregation through limited dispersal is also likely to promote the evolution of cooperative traits, with avoidance of competition by restraining production of competitive organs (i.e. low competitive ability) being one of its manifestations. Competitive ability may in turn have a feedback effect on dispersal ability: stronger competitors may evolve greater dispersal ability due to selection for avoidance of encounters with highly competitive conspecifics, while short distance dispersal will be favoured in weak competitors because it will maximise the benefits of cooperative restraint in production of competitive organs. Indeed, theoretical models that allow the simultaneous evolution of altruism and dispersal behaviour have found that, while altruists should maintain short distance dispersal, individuals adopting selfish

behaviour should evolve longer distance dispersal (van Baalen & Rand 1998; Koella 2000). The incompatibility of strong competitive ability and limited dispersal is also corroborated by a theoretical model showing that, in the absence of co-evolution of competitive and dispersal abilities, the spatial structure generated by localised dispersal could actually drive a stronger competitor to extinction (Murrell 2010). In this study, we combined spatial occurrence and dispersal data from a field survey of seven temperate grassland communities with the results of a common-garden competition experiment that included 28 focal species. Since many plant traits are known to be determined by species growth form, we included representatives of different growth forms (legumes, graminoids and forbs) in our data set. We predicted that a high degree of conspecific aggregation due to limited dispersal (offspring are placed in close proximity) should be associated with a weaker competitive ability. Alternatively, conspecific aggregation may not be shaped by dispersal ability but by environmental filtering in a heterogeneous environment (different species being most successful in habitat patches with different environmental conditions, e.g. Seabloom et al. 2005). In such a case, no relationship between spatial patterns observed in the field and competitive ability measured in a common-garden experiment (homogenous light and mean-field soil conditions) should arise. It is also possible that competitive and dispersal abilities form a trade-off, so that plants cannot simultaneously be good competitors and dispersers due to associated costs (Holmes & Wilson 1998; Bolker, Pacala & Neuhauser 2003; Jakobsson & Eriksson 2003). In this case, a positive relationship between conspecific aggregation and competitive ability should be observed: most aggregated species should be the strongest competitors. To test these predictions, conspecific aggregation of each focal species was assessed in the field using nearest neighbour analysis. Numerically, the vast majority of individuals in temperate grasslands are a result of clonal propagation, with only a small percentage of individuals originating from seeds (Rusch & van der Maarel 1992; Zobel et al. 2000; Benson & Hartnett 2006). Clonally propagated offspring (ramets) are placed at a widely varying, species-specific distance from the mother plant, and this distance has been shown to explain betweenspecies variation in the degree of conspecific aggregation (Turkington & Harper 1979; Lovett Doust 1981; McLellan et al. 1997; Benot et al. 2013). Therefore, mean dispersal distances of clonal offspring were measured for a subset of focal species to ascertain how well the degree of conspecific aggregation described dispersal ability. Competitive ability was assessed by comparing the degree to which growth of focal plants was suppressed by conspecific and heterospecific competitors in a common-garden pot experiment. In focal species with low competitive ability, conspecific competition should suppress focal plant growth less than competition with heterospecifics, which on average should be stronger competitors. In highly competitive focal species, competition with conspecifics (i.e. similarly competitive neighbours) should result in greater suppression of growth than competition with heterospecifics, which on average should be weaker competitors.

© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology, 101, 1313–1321

Competitive ability and spatial patterns 1315 (n = 8–75 per species). For species in which clonal propagation could not be detected (Carlina vulgaris and Pimpinella saxifraga) or was very rare (under 5% of examined individuals, Filipendula vulgaris), the distance between the nearest conspecifics was recorded (n = 37–52).

Materials and methods STUDY SITES AND SPECIES

We examined seven semi-natural grassland communities in Estonia representing a gradient of species richness and differing in soil characteristics, age and management history (Table 1). Twenty-eight focal species were examined in total: seven graminoid species (i.e. Poaceae, Cyperaceae, Juncaceae), four legumes and 17 non-leguminous forbs (Table 2). All species used in this study are perennials (Carlina vulgaris may be biennial).

FIELD SURVEY

Between mid-June and mid-August, one hundred individuals of each focal species were selected randomly within the study site, and the species identity of the nearest neighbour was recorded. The nearest neighbour was defined as the shoot with the rooting point closest to that of a focal shoot. Species abundances and composition of each study community were assessed by surveying randomly placed 10-mlong transects and recording the species identity of the shoots with rooting points closest to metal poles inserted every 33 cm along the transect. The number of shoots recorded by random sampling varied depending on species richness: 913 plants at Site 1, 677 at Site 2, 596 at Site 3, 565 at Site 4, 330 at Site 5, 351 at Site 6 and 242 at Site 7. Three soil cores (diameter 2.5 cm, depth 15 cm) were taken from random locations in each study community. Plant roots and larger stone particles were removed from the samples, and the soil was airdried. Soil pHKCl, Ca, N (Kjeldahl method) and available P and K contents were determined from these samples according to methods in Moore & Chapman (1986). The same parameters were calculated for three samples of commercial soil that was used in the pot experiment. The seeds of focal and potential neighbour species were collected from each study site on several occasions during the vegetation season. These seeds were air-dried and stored at 4°C for several months. They were used in a common-garden pot experiment that was carried out in the following year. To test the role of clonal dispersal in spatial pattern formation, clonal fragments of focal species from Sites 1 and 2 were excavated, and the distance between the closest connected ramets was measured

COMMON-GARDEN EXPERIMENT

Each focal species surveyed in the field was subjected to a combination of two treatments: (i) neighbour identity (conspecific or heterospecific) and (ii) neighbour density (0, 1, 2, 3, 4, 6 or 8 neighbours). In the heterospecific treatment, each focal species was coupled with a species that it commonly encountered as its nearest neighbour in the field. Inevitably, highly aggregated species did not encounter any of the heterospecific neighbours at a high frequency. The choice of heterospecific neighbour was based on the frequency of encounters as far as possible, but it was occasionally limited due to the lack of seeds or poor germination; in such cases, the next most frequent neighbour was used. In general, the chosen neighbour species were encountered by the focal species as frequently as would be expected based on its abundance in the study community (Fig. S1). Each species9treatment combination was replicated twice. Due to poor seed germination and seedling mortality, a total of 757 pots were measured at the end of the experiment instead of the planned 784 pots (28 focal species 9 2 neighbour identities 9 7 neighbour densities 9 2 replicates). To perform the competition experiment in realistic soil conditions, we prepared mixtures of commercial soil, sand and lime powder to match the N content and pH of the soil at each study site as closely as possible. In addition, natural soil from each study site was added to the corresponding soil mixtures to introduce natural soil biota. Seed germination was initiated between 27 April and 8 May, and seedlings were transplanted into pots between 22 May and 2 June. Each of the 28 focal species and its neighbours were transplanted into pots on the same day. Since the studied communities differed greatly in productivity and average plant size, we used three pot sizes, assigning larger pot volumes to communities in which plants had larger individual sizes. We used 3.5-l pots for plants from Sites 2 and 7, 5-l pots for Sites 1, 3 and 4, and 7.5-l pots for Sites 5 and 6. The distance between the focal plant and its neighbours was 5.7 cm in the 3.5-l pots, 6.8 cm in the 5-l pots and 7.8 cm in the 7.5-l pots. These dis-

Table 1. The location and characteristics of the studied grassland communities Soil properties No

Location

General description

Dominant species

S

pH

N%

P mg/kg

K mg/kg

Ca g/kg

1

58°35′03″N 23°34′09″E 58°38′31″N 23°30′55″E 58°25′28″N 26°31′05″E 58°06′36″N 27°04′15″E 58°30′47″N 23°40′19″E 58°25′32″N 26°30′40″E 58°44′20″N 23°39′26″E

Calcareous grassland, managed for ca 200 years Alvar grassland, managed for ca 200 years

88

6.7

0.60

30

72

3.2

61

6.9

0.54

24

103

2.4

Mesophytic meadow, probably has been ploughed and forested in the past Mesophytic meadow, probably has been forested in the past Islet, disturbed by ice and water

Carex tomentosa Sesleria caerulea Sesleria caerulea Carex tomentosa Festuca rubra Dactylis glomerata Festuca rubra

46

6.4

0.27

27

74

1.7

32

5.2

0.16

16

46

0.4

Urtica dioica

30

6.7

0.68

442

279

2.7

Flood-meadow, disturbed by ice and water

Deschampsia caespitosa

23

6.3

0.74

27

49

4.0

Coastal meadow, disturbed by ice and water

Juncus gerardii Plantago maritima

8

6.2

0.61

72

350

1.4

2 3 4 5 6 7

S – Chao estimator of species richness (Chao 1987). See Materials and methods for details on soil sampling and analysis. © 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology, 101, 1313–1321

1316 M. Semchenko et al. Table 2. The list of focal species and species used as neighbours in the heterospecific treatment

No

Focal species

Focal species abbreviation

1

Briza media* Carex ornithopoda* Inula salicina Leontodon hispidus Succisa pratensis Trifolium montanum† Antennaria dioica Carlina vulgaris Filipendula vulgaris Galium verum Lotus corniculatus† Pilosella officinarum Pimpinella saxifraga Sesleria caerulea* Achillea millefolium Centaurea jacea

Brimed Carorn Inusal Leohis Sucpra Trimon Antdio Carvul Filvul Galver Lotcor Piloff Pimsax Sescae Achmil Cenjac

Medicago lupulina† Phleum pratense*

Medlup Phlpra

Trifolium repens† Festuca rubra* Knautia arvensis Rumex acetosa Veronica chamaedrys Urtica dioica Deschampsia caespitosa* Lychnis flos-cuculi

Trirep Fesrub Knaarv Rumace Vercha Urtdio Descae

Peucedanum palustre

Peupal

Juncus gerardii*

Junger

2

3

4

5 6

7

Lycflo

Neighbour species Festuca rubra* Trifolium pratense† Sesleria caerulea* Sesleria caerulea* Carex flacca* Festuca rubra* Lotus corniculatus† Sesleria caerulea* Sesleria caerulea* Filipendula vulgaris Sesleria caerulea* Sesleria caerulea* Sesleria caerulea* Pilosella officinarum Festuca rubra* Anthoxanthum odoratum* Festuca rubra* Anthoxanthum odoratum* Poa pratensis* Poa angustifolia* Poa angustifolia* Festuca rubra* Rumex acetosa Artemisia vulgaris Peucedanum palustre Deschampsia caespitosa* Deschampsia caespitosa* Agrostis stolonifera*

Nomenclature: Tutin et al. 1964–80. *Graminoids. †Legumes.

tances were equivalent to two-third of the pot radius in each case. Pots were arranged randomly in a single block on an outdoor-paved area. During the first 2 weeks of the experiment, seedlings that failed to survive after transplantation were replaced. The position of pots was re-randomised twice during the experiment. Plants of 27 species were harvested after 11–14 weeks of growth in the pots. Due to very slow growth in the first season, the remaining species, Knautia arvensis, was left over winter and harvested in August of the next year. The longer growth period for this species did not cause it to be an outlier in our data. The above-ground biomass of each focal plant and of its neighbours was harvested separately, oven-dried at 70°C for 48 h and weighed. In addition, we selected pots representing plants from Site 2 as a representative subsample of the whole data set and estimated root densities as follows. Each pot was frozen at 18°C and sliced horizontally at depths of 5 cm and 10 cm below the soil surface. The surface of the frozen soil slices was then slightly cleared to expose cut-root tips, and the number of root tips present in the area between the focal plant and its neighbours was recorded. The examined species had different root colours in the heterospecific treatment, allowing the roots of focal plants and neighbours to be distinguished.

STATISTICAL ANALYSIS

The observed probability of conspecific encounter was calculated for each focal species as the proportion of times the nearest neighbour was conspecific. The abundance of a species in the study community, calculated as the proportion of times it was recorded in the random survey, was used as the expected probability of encountering a conspecific in the absence of spatial structure. The degree of conspecific aggregation was calculated for each focal species as the difference between the observed and expected probabilities of conspecific encounters. In addition, the probability of encountering the species used as a neighbour in the heterospecific treatment was calculated as the proportion of times the nearest neighbour in the field belonged to that species. Linear mixed models were performed with ln-transformed aboveground dry mass of focal plants as a response variable and the following predictors: neighbour density (continuous variable), neighbour identity (fixed factor with two levels: conspecific or heterospecific) and one of the parameters calculated for each of the focal species (degree of conspecific aggregation, probability of encountering species used as neighbour in the heterospecific treatment or mean distance between adjacent ramets as continuous variables, or growth form – grass, legume or non-legume forb – as a fixed factor). Species, nested within community, was included in the models as a random factor. In addition, the same models were run for each community separately, excluding two communities where only one focal species was examined (Sites 5 and 7). A significant three-way interaction was interpreted as evidence for a role of the calculated focal species parameters (conspecific aggregation, distance between adjacent ramets, heterospecific encounters or growth form) in determining the difference in competitive response to conspecific vs. heterospecific neighbours (i.e. how focal plant growth was suppressed by increasing densities of conspecific vs. heterospecific neighbours). To illustrate the three-way interaction, the difference in competitive response was calculated as the difference between the regression slopes of the relationship between neighbour density and ln-transformed focal plant mass in the heterospecific and conspecific treatments (Fig. 1 for further details and an example). The difference in slopes was then plotted against the focal species characteristic involved in the interaction term (Fig. 2). To test whether a similar relationship between competitive response and spatial aggregation would be observed if below-ground data were used instead of above-ground biomass, ln-transformed root density from focal plants representing Site 2 was used as the response variable in linear mixed models with neighbour density, neighbour identity and degree of conspecific aggregation (or the probability of encountering the species used in the heterospecific treatment) included as predictor variables and species as a random factor. Data analyses were performed using R 2.15.0 (R Development Core Team 2012). Mixed models were implemented using R package nlme (Pinheiro et al. 2012).

Results The effects of neighbour density and identity on focal plant mass in the competition experiment were dependent on the degree of conspecific aggregation recorded in the field (significant three-way interaction F1,723 = 9.0, P = 0.0028; Fig. 2a). Species with a low degree of conspecific aggregation achieved greater growth with heterospecifics than with conspecifics, while species with a high degree of conspecific aggregation exhibited greater growth when surrounded by conspecifics than by individuals of other species (Fig. 2a). The degree of

© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology, 101, 1313–1321

Competitive ability and spatial patterns 1317 (b)

0.5

ln(focal plant mass, g)

ln (focal plant mass, g)

(a)

0.0 –0.5 –1.0 –1.5

8

–2.0

–1.0 –2.0 –3.0 –4.0 –5.0

–2.5 0

1

2

3

4

5

6

7

8

Neighbour density

0

1

2

3

4

5

6

7

8

Neighbour density

Fig. 1. An example of the effects of neighbour density and identity on the dry mass of focal plants. (a) Pilosella officinarum as a focal species grown with conspecifics or surrounded by Sesleria caerulea (n = 28). (b) S. caerulea as a focal species grown with conspecifics or surrounded by P. officinarum (n = 27). The closed symbols and unbroken line denote the conspecific treatment, and the open symbols and dashed line represent the heterospecific treatment. The red squares on the photos are 2 9 2 cm and are provided for scale. The difference in competitive response to heterospecifics vs. conspecifics shown in subsequent figures in this paper was calculated as the difference between the slopes of the regression lines in the heterospecific and conspecific treatments (heterospecific–conspecific). A positive difference between slopes (panel a) indicates that the growth of the focal species is suppressed more by conspecifics than by heterospecific neighbours (i.e. higher-than-average competitive ability). A negative difference between slopes (panel b) indicates that the growth of the focal species is suppressed by heterospecific neighbours more than by conspecifics (i.e. lower-than-average competitive ability).

conspecific aggregation was negatively correlated with the probability of encountering the species used in the heterospecific treatment (Pearson’s r = 0.75, P < 0.0001, n = 28). Similarly to the effect of conspecific aggregation, the probability of encountering in the field, the species used in the heterospecific treatment had a significant effect on the way focal plant mass was affected by neighbour density and identity (three-way interaction F1,723 = 3.9, P = 0.0477). Focal species that frequently encountered the species used as their heterospecific neighbour were more suppressed by conspecific competition than by competition with the heterospecific neighbour. In contrast, the growth of species that rarely encountered the heterospecific neighbour was more suppressed by heterospecific than by conspecific competition (Fig. 2b). At sites where clonal dispersal data were available (Sites 1 and 2), the degree of conspecific aggregation was negatively correlated with the mean distance between adjacent, clonally propagated ramets or adjacent conspecifics if clonal propagation was very rare (Pearson’s r = 0.63, P = 0.0166, n = 14). Similarly to conspecific aggregation, species competitive ability was also dependent on clonal dispersal distance: species that placed clonal offspring at a very short distance achieved greater growth with conspecific than heterospecific neighbours, while the growth of species with greater distances between adjacent ramets was more suppressed by conspecific than by heterospecific competition (three-way interaction between neighbour density, identity and mean inter-ramet distance, F1,355 = 6.7, P = 0.0101; Fig. 2c). The strength and direction of the relationship between the competitive response and the degree of conspecific aggregation differed between the groups of species representing different study communities. Among the five communities of which more than one focal species was examined, the most pronounced dependence of competitive response on intraspecific aggregation was detected in plants representing Site 1 (three-way interaction between neighbour density, identity and intraspecific aggregation, F1,147 = 8.2, P = 0.0048; Fig 2a). A significant relationship was also detectable in Site 2 (three-

way interaction, F1,202 = 4.1, P = 0.0444; Fig. 2a), while a similar but marginally non-significant relationship was found in Site 4 (three-way interaction, F1,97 = 3.3; P = 0.0745, Fig. 2a). The opposite trend – that is, the more the aggregated a species was, the more successful it was in competition with heterospecifics – was observed in Site 6, although the effect was not significant (three-way interaction, F1,75 = 1.9; P = 0.1728, Fig. 2a). The degree of intraspecific aggregation was significantly affected by species growth form (F2,25 = 6.7, P = 0.0048; Fig. 3a). Graminoids were characterised by the highest intraspecific aggregation. Forbs and legumes exhibited a similar degree of intraspecific aggregation that was significantly lower than that of graminoids. Competitive response to the density and identity of neighbours was also affected by species growth form: graminoids tended to be suppressed by competition with heterospecifics as much as or more than by competition with conspecifics, while forbs exhibited the opposite trend and legumes always achieved greater growth with heterospecific neighbours (three-way interaction between neighbour density, identity and focal plant’s growth form, F2,720 = 8.6, P = 0.0002; Fig. 3b). To ascertain whether the results obtained for above-ground mass were representative of the whole plants (i.e. including roots), competitive response was also calculated using root density data, which was available for Site 2. We found that the obtained relationships between conspecific aggregation, frequency of heterospecific encounters and competitive response were very similar to those observed in the analysis of above-ground biomass (Fig. S2).

Discussion We found that the frequency with which plants encounter conspecifics and heterospecifics as their nearest neighbours in the field was significantly correlated with their ability to compete with these species as neighbours in a controlled experiment. Species with a low degree of conspecific aggregation and a

© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology, 101, 1313–1321

0.3

Lotcor Pimsax Piloff Inusal Leohis Galver Cenjac 0.1 Achmil Fesrub Rumace Carvul Filvul Trimon

0.2

0.0

Greater growth with conspecifics

Trirep

Vercha Medlup

Peupal

Phlpra

–0.1

Descae

Lycflo Knaarv Antdio Sescae Brimed Junger Sucpra Urtdio

–0.2

Carorn

–0.3 –0.1 0.0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

Greater growth with heterospecifics

Degree of conspecific aggregation

Greater growth with conspecifics

(b)

0.3

Vercha Trirep

Medlup Lotcor

0.2

Piloff Pimsax Galver Inusal Leohis Cenjac Rumace Fesrub Achmil Trimon Filvul Carvul

Descae

0.1 0.0

Phlpra Antdio

Lycflo Knaarv

Peupal

Brimed SescaeSucpra

–0.1

Junger Urtdio

–0.2

Carorn

–0.3 –0.1

0.0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

Greater growth Greater growth with conspecifics with heterospecifics

arcsin[sqrt(probability of encountering neighbour species)]

(c)

Degree of conspecific aggregation

(a)

Greater growth Greater growth with conspecifics with heterospecifics

Greater growth with heterospecifics

1318 M. Semchenko et al. 0.8

(a)

0.6

Median 25%-75% Min-Max

0.4 0.2 0.0 –0.2

0.3

(b)

0.2 0.1 0.0 –0.1 –0.2 –0.3

Graminoids Non-legume forbs Legumes

Fig. 3. The relationship between species growth form and (a) The degree of conspecific aggregation (n = 28) and (b) The difference in competitive response to heterospecifics vs. conspecifics (n = 28). The difference in competitive response was calculated as the difference in slopes of the regression lines between neighbour density and ln (focal plant mass) in the heterospecific and conspecific treatments (Fig. 1 for details).

0.3 Lotcor

0.2

Piloff

Inusal

Galver Leohis

0.1

Pimsax

Carvul Trimon

Filvul

0.0 Antdio

–0.1 Sescae Brimed Sucpra

–0.2 Carorn

–0.3 –0.2

0.0

0.2

0.4

0.6

0.8

1.0

1.2

1.4

ln(mean distance between adjacent ramets, cm)

Fig. 2. Relationship between the difference in competitive response to conspecific and heterospecific neighbours and (a) The degree of intraspecific aggregation (n = 28), (b) The probability of encountering the species used in the heterospecific treatment (n = 28) and (c) The mean distance between adjacent ramets (n = 14). The difference in competitive response was calculated as the difference in slopes of the regression lines between neighbour density and ln (focal plant mass) in the heterospecific and conspecific treatments (Fig. 1 for details). Different symbols are used to highlight different sampled communities: filled squares, Site 1; filled circles, Site 2; open squares, Site 3; open triangles, Site 4; open circle, Site 5; crosses, Site 6; open diamond, Site 7 (descriptions in Table 1). Abbreviations of focal species are provided in Table 2.

high frequency of encounters with the species used in the heterospecific treatment were more suppressed by conspecific than by heterospecific competition, reflecting higher-than-

average competitive ability in these species. Species with a high degree of conspecific aggregation and, consequently, a low frequency of heterospecific encounters maintained greater growth when surrounded by conspecifics than by individuals of another species, reflecting low competitive ability. In other words, plants were least suppressed by competition with the neighbour type that they encountered most frequently in nature. Temperate grasslands are predominantly composed of perennial species possessing an ability to reproduce clonally, and most of the individuals in such communities are a result of clonal propagation (Rusch & van der Maarel 1992; Klimes et al. 1997). It has been shown that variation in spatial aggregation of conspecifics can be explained by the species-specific distance between clonally propagated offspring (Turkington & Harper 1979; Lovett Doust 1981; McLellan et al. 1997; Benot et al. 2013). Our results conform to the observations reported in previous studies – the observed patterns of conspecific aggregation were strongly related to variation in clonal dispersal distances. Moreover, we found a direct link between clonal dispersal and competitive ability: species that placed clonal offspring at a very short distance, and were therefore highly likely to interact with genetically identical individuals, exhibited lower competitive ability against heterospecifics than species with longer dispersal distances. This finding supports the hypothesis that a high degree of conspecific aggregation due to limited dispersal should be associated with a weaker competitive ability. Spatial aggregation of conspecifics and the relative intensity of intra- and interspecific competition have both been central

© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology, 101, 1313–1321

Competitive ability and spatial patterns 1319 to the theories explaining species coexistence (Bolker, Pacala & Neuhauser 2003; Silvertown 2004), but the possibility of co-evolution between dispersal and competitive abilities has not been considered previously in studies on plants. Our results are consistent, however, with the predictions of models examining the role of dispersal in the evolution of cooperation. According to game-theoretic models and kin selection theory, limited dispersal should strongly promote the evolution of cooperative traits, because it ensures that cooperators interact with each other more frequently than would be expected based on their abundance, and thus, the exploitation of cooperators by selfish individuals is reduced (Hamilton 1964; Doebeli & Hauert 2005). Furthermore, theoretical models show that, if dispersal distance and investment in altruism are allowed to co-evolve, altruists maintain short dispersal distances while individuals adopting a selfish strategy evolve towards greater dispersal ability (van Baalen & Rand 1998; Koella 2000). Weak competitive ability (measured as greater suppression of focal plant growth by heterospecifics than by conspecifics in our study) can be viewed as an expression of cooperative restraint in the use of common resources, while strong competitive ability (greater suppression of focal plant growth by conspecifics than by heterospecifics in our study) probably results from selfish, inefficient resource consumption (Pepper & Smuts 2002; Kerr et al. 2006; Nahum, Harding & Kerr 2011). Since we found that the degree of conspecific aggregation was related to clonal dispersal ability, the relationship between conspecific aggregation and competitive response to conspecifics vs. heterospecifics detected in this study can be viewed as the first empirical evidence that competitive restraint and dispersal ability might be co-evolved in plants. We detected a significant overall relationship between the degree of conspecific aggregation and competitive response to conspecific vs. heterospecific neighbours, but the strength and direction of the relationship varied between groups of species representing different study communities. The dependence of competitive response on conspecific aggregation was most pronounced in plants from calcareous grasslands, where the least-aggregated species were the strongest competitors against heterospecifics. The opposite trend, although statistically not significant, was observed in plants from a flooded meadow community: the dominant grass in this community (Deschampsia caespitosa) exhibited the highest degree of spatial aggregation and the strongest competitive ability against subdominant forbs. Calcareous grasslands examined in this study are characterised by high species richness and a long history of continuous management by grazing or mowing (Poska & Saarse 2002; P€artel et al. 2007). The flooded meadow is, on the other hand, species poor, more productive and subject to frequent disturbance due to flooding. Investigating the importance of community history, productivity and other community properties could give further insight into the processes determining the relationship between spatial patterns and competitive ability. We also found that species growth form had a significant impact on both conspecific aggregation in the field and

competitive response in the common-garden experiment. The degree of conspecific aggregation was on average significantly higher in graminoids than non-leguminous forbs and legumes. The growth of graminoids was suppressed by competition with heterospecifics as much as or more than by competition with conspecifics, while non-leguminous forbs exhibited the opposite trend, and legumes always achieved greater growth with heterospecific neighbours than with conspecifics. As the three growth forms represent major phylogenetic splits in the plant kingdom, our results show that species characteristics examined in this study were significantly influenced by phylogenetic provenance. Similar results were obtained in a study examining the effect of phylogenetic distance on the strength of interspecific competition: variation in the intensity of competition was strongly influenced by the monocot–eudicot evolutionary split, with monocots being weaker competitors against forbs and forbs being stronger competitors against monocots (Cahill et al. 2008). Significant differences between growth forms have also been identified in the studies examining the strength of microbial feedbacks (Bartelt-Ryser et al. 2005; de Kroon et al. 2012), the effects of grazing (Deleglise, Loucougaray & Alard 2011), patterns of colonisation and extinction in experimentally established plant communities (Cadotte & Strauss 2011) and the ability of legumes to invade communities containing different growth forms (Turnbull et al. 2005). Although the importance of growth form has been demonstrated in many studies, there is still little understanding of the actual traits that contribute to these effects. Our results suggest that important traits may include the degree of conspecific aggregation and the relative ability to compete with conspecifics and heterospecifics. Previous studies have concluded that spatial aggregation should benefit weak competitors but should put stronger competitors at a disadvantage, thus promoting species coexistence. Our results show that weaker competitors indeed tend to form highly aggregated spatial distribution patterns in the field, probably aiding their persistence in the community, but stronger competitors seem to avoid frequent conspecific interactions. Spatial aggregation of conspecifics was closely related to dispersal ability via clonal propagation. This finding highlights a thus far overlooked connection between fundamental species properties that are central to the theories of species coexistence: species dispersal ability and the relative ability to withstand competition with conspecifics and heterospecifics covary, resulting in greater dispersal in stronger competitors and lower competitive ability in spatially aggregated species. While our results are in accordance with predictions of evolutionary models, further empirical research into the costs and benefits of different competitive and dispersal strategies is needed to improve our understanding of the mechanisms promoting species coexistence.

Acknowledgements We thank Siim Nettan, Aime Randveer, Sirgi Saar, Anette Sepp, Siim–Kaarel Sepp and Marge Thetloff for help in planting, harvesting and measuring plants.

© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology, 101, 1313–1321

1320 M. Semchenko et al. We are also grateful to John Davison, Mike Hutchings, Lindsay Turnbull and two anonymous reviewers for helpful comments that greatly improved the manuscript and to Lars G€ otzenberger for statistical advice. This work was supported by the University of Tartu (0119) and Estonian Science Foundation (Grant No. 9332).

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Additional Supporting Information may be found in the online version of this article: Figure S1. Relationship between the observed and expected probabilities of encountering the species used as a neighbour in the heterospecific treatment. Figure S2. Relationship between the difference in competitive response to conspecific vs. heterospecific neighbours and (a) the degree of conspecific aggregation and (b) the probability of heterospecific encounter.

Received 4 January 2013; accepted 5 June 2013 Handling Editor: James Cahill

Supporting Information

© 2013 The Authors. Journal of Ecology © 2013 British Ecological Society, Journal of Ecology, 101, 1313–1321

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