Using functional traits to assess the role of hedgerow corridors as environmental filters for forest herbs

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Using functional traits to assess the role of hedgerow corridors as environmental filters for forest herbs Vale´rie Roy, Sylvie de Blois* Department of Plant Science and the McGill School of Environment, McGill University, Macdonald Campus, 21 111 Lakeshore Road, Ste. Anne de Bellevue, Que., Canada H9X 3V9

A R T I C L E I N F O

A B S T R A C T

Article history:

Linear habitats such as hedgerows can constitute important refuges for native flora and

Received 23 September 2005

fauna, possibly providing connectivity between landscape elements. The effectiveness of

Received in revised form

these functions, however, depends on the ability of linear habitats to benefit a significant

7 January 2006

proportion of the local species pool and their functional attributes. This study aims to iden-

Accepted 25 January 2006

tify life-history traits that appear to either limit or facilitate survival or colonization of for-

Available online 23 March 2006

est herbs in hedgerows. The distribution patterns of 47 native forest herbaceous species and their associated traits were compared in a system of hedgerows and attached forest

Keywords:

patches of southern Quebec. Although 83% of the species surveyed in forest patches were

Connectivity

present in hedgerows, significant differences in abundance suggest the existence of a

Conservation outside reserve

selective pressure on forest species in linear habitats. Early spring flowering was negatively

Forest fragmentation

associated with hedgerows, possibly because of unfavourable microclimatic conditions.

Fourth-corner statistic

Seed dispersal phenology partly mirrors results for flowering phenology with early summer

Life-history traits

dispersal and late fall dispersal being less common in hedgerows than in forests. Slow dis-

Linear habitat

persal mainly through myrmecochory was also less common in hedgerows compared to forest sites, suggesting a selective pressure on slow dispersers in linear habitats. The capacity for vegetative propagation was positively associated with hedgerows, possibly because it provides an alternative strategy to survive and expand when conditions are less favourable for sexual reproduction. Our approach highlights traits that can help determine the vulnerability of native forest species in linear habitats or their likelihood to benefit from the maintenance of wooded corridors in an inhospitable matrix.  2006 Elsevier Ltd. All rights reserved.

1.

Introduction

Plant diversity at a site appears to be largely determined by abiotic and biotic filters that select, from a regional pool, a subset of species with appropriate traits to disperse to and survive at this site. Focusing not only on species but also on sets of traits that are conserved or filtered out in particular conditions can bring about a better understanding of the adaptive responses of organisms to environmental changes

(Lavorel et al., 1997; Lavorel and Garnier, 2002; Hooper et al., 2005). It also has the potential to lead to generalization of these responses across landscapes and taxa (Verheyen et al., 2003; Deckers et al., 2004b; Kolb and Diekmann, 2005). Among plants, temperate forest herbs exhibit functional attributes normally associated with a relatively stable environment. They have been described by several authors as poor dispersers and recruiters because of their slow growth rate, long pre-reproductive phase, low reproductive output,

* Corresponding author: Tel.: +1 514 398 7581; fax: +1 514 398 7897. E-mail address: [email protected] (S. de Blois). 0006-3207/$ - see front matter  2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2006.01.022

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and generally short dispersal distances (Bierzychudek, 1982; Matlack, 1994; Cain et al., 1998; Hermy et al., 1999). These traits are likely to make them vulnerable to edge effects and distance effects associated with fragmentation as several species appear to have difficulties surviving or recolonizing after disturbances (Bossuyt et al., 1999; McLachlan and Bazely, 2001; Honnay et al., 2005; Matlack, 2005). An interesting system in which to test such effects on forest herbs is found in hedgerows connected to forest patches in an agricultural landscape. In forested hedgerows, we expect the conditions generally associated with edge effects to be somewhat extreme. Yet, there is evidence that hedgerows may serve as refuges for forest herbs that have been excluded from the agricultural matrix (Boutin and Jobin, 1998; McCollin et al., 2000; de Blois et al., 2002a; Freemark et al., 2002). Moreover, it has been suggested that hedgerows could act as movement corridors that facilitate biotic exchanges among forest patches, alleviating the effect of population isolation and fragmentation at the landscape scale even for sensitive organisms such as forest herbs (Corbit et al., 1999; Deckers et al., 2004a). Obviously, the effectiveness of these habitat and corridor functions depends on the ability of a hedgerow to retain a significant proportion of the local species pool and their functional attributes. Assessing not only which forest plant species but also which traits are associated with or filtered out by hedgerows compared to adjacent forest patches can help us evaluate the conservation potential of linear habitats and their ability to provide connectivity at the landscape scale (de Blois et al., 2002b). This study examines the distribution of forest herb species, and their associated functional attributes, in a system of hedgerows and attached forest patches of southern Quebec. It aims to identify species-specific traits that appear to either limit or facilitate survival or colonization of forest herbs in hedgerows. Our analysis is based on the assumption that the species that are significantly less abundant in hedgerows compared to forest patches may possess traits that make them vulnerable in this system and are therefore ultimately less likely to benefit from the habitat or corridor function provided by hedgerows. We used the fourth-corner method (Legendre et al., 1997; Hooper et al., 2004; Urban, 2004) to directly relate attributes acting on the reproduction, survival and dispersal of forest herbs to habitat types (forest or hedgerow). We also examined whether a trait-based classification of forest herb species in emergent groups (Lavorel et al., 1997) is possible and informative in this system and whether emergent groups can be related to habitat types. Our results provide insights into processes that may be important for the conservation of forest plant diversity in fragmented habitats and anthropogenic landscapes.

2.

Methods

2.1.

Study area

The study was conducted in Mirabel and Deux-Montagnes (4540 0 N, 741 0 W), two regional county municipalities located west of Montreal, Que., Canada. This area is located within the St. Lawrence Lowlands Ecoregion (Ecoregions Working Group, 1989) which is marked by moist summers and cold,

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snowy winters; it receives 1065 mm of precipitation per year with an average temperature of 5 C, ranging from 12 C in January to 19.5 C in July (Environment Canada 2005). Mature deciduous forests are dominated by Acer saccharum Marsh, in association with Carya cordiformis (Wang.) K. Koch., Fagus grandifolia Ehrh., and Fraxinus pennsylvanica Marsh (Grandtner, 1966). The St. Lawrence Valley has undergone extensive clearing for agriculture, industrial and urban development in the past two centuries. Forest cover in the region comprising our study area is around 25% (Be´langer and Grenier, 2002). Most remaining forest patches within the agricultural matrix are highly fragmented forests measuring 19 ha on average (Be´langer et al., 1998). Agricultural land-uses occupy 45% of the landscape and include dairy farming (hay fields, pasture, fallow lands) as well as more intensive cultivation (corn and specialized crops) (Be´langer et al., 1999).

2.2.

Sampling

Data were collected in May and June of 2004 when both early spring and late summer flowering species were present. In order to identify the most suitable hedgerow habitats for forest herbs, we selected field sites based on the following structural and biological criteria: (1) Natural hedgerow P200 m long and P5 m large, connected, or with a gap no more than 10 m, to a forest patch >2 ha; connection to a forest patch is believed to facilitate dispersal into hedgerows (Corbit et al., 1999). (2) The hedgerow has mature deciduous trees in the canopy layer; the forest patch is a mature mesophytic forest characterized by dominance of Acer saccharum. (3) The hedgerow is located between two agricultural fields and does not have pronounced drainage ditches. (4) Forest herb populations are established in the hedgerow and the attached forest. A total of 35 hedgerows meeting the structural criteria were identified from panchromatic aerial photographs (1:40,000) of the region. Each potential hedgerow and its adjacent forest were then visited to determine if they met the biological criteria. The majority of hedgerows were species-poor, so only 13 of the 35 hedgerows visited met the biological criteria and were therefore sampled. Each selected hedgerow was attached to a forest patch, though in three cases, two hedgerows were connected to the same forest leaving a sample size of 10 forest patches. Eight hedgerows were bordered on one or both sides by intensive agriculture and the remaining ones by hay fields. The attached forests were all mature Acer saccharum stands. Although the forest stands may have been cut repeatedly, edaphic conditions suggest that they may never have been cleared for agriculture. All hedgerows have originated on land that was previously forested but it is not possible from the historical and site data to infer the exact origin of the forest herb populations. In this system, both remnant populations and colonization are possible and we thus assumed that selection would operate both on traits related to survival and dispersal. Historical data obtained from aerial photos show that five of our hedgerows

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(H4, H5, H6, H10, H13) had a tree cover since at least 1930; four others (H2, H3, H7 and H9) also show a mature tree cover as far back as our photos would allow us to go in time (1954). In these hedgerows, forest herb populations either survived hedgerow conditions for a significant period of time after forest clearing (perhaps more than 100 years) or had time to recolonize from adjacent forest patches. Hedgerow 11 had a well-developed structure in 1930 but was clear-cut in 1970. Hedgerows 1, 8 and 12 were visible as uncultivated field margins from 1930 until 1964, when a patchy tree cover was detected on aerial photographs. In these recent hedgerows, remnant forest herb populations would have had to survive an extended period without a tree cover or recolonization from adjacent forest patches would have had to occur in about 40 years. Given hedgerows’ history, we hypothesized that the species that were significantly less abundant in hedgerows compared to forest patches were possessing traits that made them more vulnerable to hedgerow conditions if they were remnant populations, or were unable or comparatively slow to recolonize after disturbances compared to the most abundant species. For this study, ‘forest herbs’ were defined as perennial, herbaceous, vascular plants characteristic of the interior of temperate deciduous forests’ understory and described as such by Marie-Victorin (1995), a local authority (Table 1). Forest herb populations were characterized by occurrence and abundance. We used a semi-quantitative measure of abundance from 1 to 5 based on the number of rooted stems (including seedlings). Exploratory analysis of species–area curves for a subsample of forest patches and hedgerows allowed us to determine an adequate sample size to capture the diversity of forest herbs in both habitat types. In forest patches, the abundance of forest herbs was noted in 1 m2 quadrats located every 5 m along 100 m transects set up at 3 m, 25 m and 35 m parallel to the forest edge, for a total of 42 interior quadrats and 21 edge quadrats. These distances were chosen to include species of the forest edge and forest interior, and were biased toward forest populations that would have been most likely to colonize hedgerows. In hedgerows, sampling was done to take into account the spatial segregation of forest herbs in the different microhabitats (‘edge’ and midline) of a hedgerow (de Blois, unpublished data) and to mirror edge and interior conditions found in forests. A transect was established along the midline as well as along both edges. Side transects were set up where the limit between the managed field and the unmanaged hedgerow was detectable, which was often distinguished by the start of woody vegetation. Data were collected in 1 m2 quadrats located every 5 m in the midline starting at the forest connexion, for a total of 42 quadrats. Both edges of a hedgerow were sampled alternatively every 10 m starting at 2 m from the forest connexion on one side and at 4 m on the other side for a maximum of 21 quadrats in hedgerow edges to match the number of quadrats in forest edges. We sampled a total of 1449 quadrats in this system.

2.3.

Species attributes

We focused our study on relevant demographic attributes describing mostly dispersal, reproductive strategies and phe-

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nology. Demographic attributes can be seen as a component of functional response traits (sensu Walker et al., 1999). We classified each species with respect to 11 attributes categorized into several traits (Table 2). The selected attributes were ones that did not require specific measurements in the field and for which information was available from an extensive search of the scientific literature (Appendix 1). To retain an attribute for analysis, information for that attribute had to be available for the majority of species.

2.4.

Data analysis

2.4.1.

Species richness and composition

Values of overall species richness at each site (H1, H2, etc.) for a given habitat type, (H)edgerow or (F)orest, were submitted to a one-way ANOVA through Systat (1998) in order to determine whether mean species richness in hedgerows was significantly different from mean species richness in forests. We conducted a principal component analysis (PCA) and a redundancy analysis (RDA) with Canoco (ter Braak and Smilauer, 1997) in order to illustrate differences in species composition between sites and to detect species preferences to a given habitat type. We used the sum of abundances for all quadrats for a given species at a site as response variable for both ordinations, and the habitat type as binary environmental variables for the RDA. A chord transformation was used previous to the RDA to eliminate the problem normally associated with the use of the Euclidean distance for comparing sites on the basis of species data containing double-zeros and to reduce the weight of rare species allowing for a more accurate interpretation of distribution patterns (Legendre and Gallagher, 2001).

2.4.2.

Formation of emergent groups

The term emergent group refers to ‘‘a group of species that reflect natural correlation of biological attributes’’ (Lavorel et al., 1997). In this study, emergent groups were created by calculating a similarity matrix based on Gower’s coefficient (Legendre and Legendre, 1998) from the species · attributes matrix. The similarities were transformed to distances in order to perform a PCoA on them. We used K-means clustering to divide objectively the species into emergent groups, based on the eigenvectors calculated for the PCoA. This clustering method was preferred over hierarchical clustering because it was able to handle missing values and semi-quantitative data.

2.4.3.

Relationship of species attributes to habitat types

We used a multivariate analysis known as the fourth-corner method (for a complete description of the analysis refer to Legendre et al., 1997; for other examples see Hooper et al., 2004; Urban, 2004) to assess how the measured traits (or the emergent groups) relate to habitat types in this system. This would normally require analysing data tables by pairs, i.e., relating the species at a site to the matrix of species traits, then to the type of habitat at a site. If we consider the matrix of species abundances (rows) observed at sites (columns), the fourth-corner approach uses matrix multiplication to provide a direct assessment of the relationships between supplementary variables associated with the rows (species attributes in this case) and the columns (habitat types in this case) of our

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Table 1 – Woodland herb species included in the study and their membership to one of the six emergent groups Species 1. Actaea pachypoda Ell. 2. Actaea rubra (Ait.) Willd. 3. Allium tricoccum Ait. 4. Aralia nudicaulis L. 5. Arisaema triphyllum (L.) Schott 6. Asarum canadense L. 7. Cardamine diphylla (Michx) Wood 8. Carex blanda Dewey 9. Carex cephaloidea (Dewey) Dewey 10. Carex deweyana Schwein 11. Carex intumescens Rudge 12. Carex leptonervia (Fern.) Fern. 13. Carex pallescens L. 14. Carex rosea Schkuhr ex Willd. 15. Caulophyllum thalictroides (L.) Michx. 16. Circaea lutetiana L. 17. Cypripedium pubescens Willd. 18. Dicentra cucullaria (L.) Bernh. 19. Dryopteris carthusiana (Vill.) H.P. Fuchs 20. Dryopteris goldiana (Hook. ex Goldie) Gray 21. Epifagus virginiana (L.) W. Bart. 22. Epipactis helleborine (L.) Crantza 23. Erythronium americanum Ker-Gawl. 24. Gymnocarpium dryopteris (L.) Newman 25. Hepatica nobilis Schreb. 26. Hydrophyllum virginianum L. 27. Impatiens capensis Meerb. 28. Maianthemum canadense Desf. 29. Maianthemum racemosum (L.) Link 30. Matteuccia struthiopteris (L.) Todaro 31. Onoclea sensibilis L. 32. Orthilia secunda (L.) House 33. Phegopteris connectilis (Michx.) Watt 34. Polygonatum pubescens (Willd.) Pursh 35. Prenanthes alba L. 36. Pteridium aquilinum (L.) Kuhn 37. Ranunculus abortivus L. 38. Sanguinaria canadensis L. 39. Streptopus lanceolatus (Ait.) Reveal 40. Thalictrum dioicum L. 41. Tiarella cordifolia L. 42. Trillium erectum L. 43. Trillium grandiflorum (Michx.) Salisb. 44. Uvularia grandiflorum Sm. 45. Viola canadensis L. 46. Viola pubescens Ait. 47. Viola sororia Willd.

Code Aru Atc Anu Atp Aca Cbl Cde Cle Cpa Cth Clu

Dca

Eam Hno Hvi Mca Mra Mst Osn

Ppu Pal

Sca Sla Tco Ter Tgr Ugr Vpu Vso

Emergent group #

Hedgerow

4 4 4 4 4 2 1 5 5 5 5 5 5 5 4 4 6 2 3 3 6 6 2 3 2 1 6 4 4 3 3 6 3 4 6 3 2 2 2 5 1 2 2 2 2 2 2

x x x x x x x x x x x x x x x

x

x x

x x x x x x x x x x x x x x x x x x x x x

Presence in at least one hedgerow is indicated. Notes: Nomenclature follows the Integrated Taxonomic Information System (ITIS) on-line database, http://www.itis.usda.gov. Codes of the species are those used in Fig. 3. a Non-native but not invasive.

multivariate table and to test the significance of these relationships. The supplementary variables can be qualitative or quantitative. Qualitative variables are expanded to binary variables and the estimated parameter crossing two states corresponds to frequencies in a contingency table from which a v2 statistic can be computed using Wilk’s (G statistic) formula. For quantitative variables, the fourth-corner statistic corresponds to a Pearson product-moment correlation. The estimated parameters of the association between habitat types and species traits are tested by permutations. In our

case, values were permuted in such a way as to simulate the absence of habitat control over individual species (permutation model 1 sensu Legendre et al., 1997). Rejecting the null hypothesis supports the ecological hypothesis that species and their associated traits are distributed individually at locations where they find adequate conditions. The resulting probabilities were adjusted for multiple testing using Holm’s procedure. In a first analysis, we tested the relationship between habitat types and each of the individual species traits (Table 2). In a second analysis, we examined the relationship

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Table 2 – Results of the fourth-corner analysis where species occurrence and abundance data in forests and hedgerows are related to species traits (A) Nominal attributes

p(G) Presence

a

Vegetative phenology Spring green Summer green Late summer green Winter green

0.1700

Seed dispersal phenology May to mid-June End of June and July August to mid-September Late September and later

0.0100

Pollination mode Abiotic pollination Biotic pollination

0.0700

Flowering phenology Early spring Mid-spring Late spring Summer/Fall

0.0001

Breeding system Hermaphrodite flowers Dioecious flowers Monoecious flowers Spores

0.1700

Dispersal mode Endozoochory Barochory Autochory Myrmecochory Anemochory

0.0001

Hedgerow Abundance

Presence

0.1342 6 95 26 21

– – – –

7.19 84.62 24.54 60.53

38 11 57 20

– *** – – –**

29.35 – * 9.85 – 75.29 + à 5.51 – **

0.0436 5.81 –* 171.06 –

0.0001 26 – 44 – 54 + 18 –

*** **

20.33 – ** 28.76 – 104.15 +* 22.44 +

0.0830 123 10 9 6

– – – –

164.33 6.83 4.52 1.19

– + – –

0.0012 73 – 22 – à 12 + 28 –*** 13 –**

r(I,j) Presence

Abundance

Vegetative propagation No clonal propagation Propagation at the parent stem Propagation equivalent to the plant’s height Longer propagation distances

+ 0.0537

+ 0.3306***

Seed mass Less than 1 mg 1.0 mg to 5 mg 5.1 mg to 10 mg More than 10.0 mg

+ 0.0627

+ 0.0548

Self-compatibility Self-incompatible Self-compatible/predominantly outcrossing Facultatively self-compatible Self-compatible/rarely outcrossing

0.0073

+ 0.0199

Height of the plant 0–20 cm 21–40 cm 41–60 cm 61–80 cm 81–100 cm More than 100 cm

+ 0.0073

+ 0.0827

b

– – – +

0.0009

16 – 132 –

(B) Semi-quantitative attributes

Abundance

81.20 + 58.93 + 11.22 + 23.47 –** 2.08 –**

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Table 2 – continued (B) Semi-quantitative attributes

r(I,j) Presence

Number of seeds per fruit 1 or 2 3–10 11–20 More than 20

0.0677

Abundance 0.1397

(A) Results for nominal attributes. The second and third columns report the global test of significance for an attribute p(G) and the fourth and fifth columns report the observed values for each trait resulting from the matrix multiplications. Sign indicates whether the statistic is above (+) or below () the estimated expected value. Significant values in bold. (B) Semi-quantitative attributes. Fourth-corner correlation statistics r(I,j) for the attribute reported for hedgerows. Significant and nearly significant values in bold (* – p 6 0.05, ** – p 6 0.01, *** – p 6 0.001, à – p 6 0.058) adjusted using Holm’s procedure. 9999 permutations following model 1 (sensu Legendre et al., 1997). a Categories as defined by Mahall and Bormann (1978). b Categories as defined by Matlack (1994).

between habitat types and species membership to the emergent groups (Table 1). A revised version of the original program (Dray and Legendre, in preparation) allowed us to perform the analyses using species abundance data as well as presence–absence data.

3.

Results

3.1.

Species richness and composition

A total of 47 forest herb species were surveyed in this study, among which 39 were sampled in hedgerows (Table 1). All species unique to forest habitats were also rare in surveyed patches (e.g. Cypripedium pubescens, Dicentra cucullaria, Epifagus virginiana) with the exception of Hepatica nobilis. No sampled forest herb species was unique to hedgerows. The average number of forest herb species varied significantly between habitat types (p < 0.05) (Fig. 1). The first two axis of the PCA explain 40.7% of the variance (Fig. 2). The ordination reveals variations in species composition and abundance both between and within habitat types.

Fig. 1 – Mean number of forest herbaceous species in forests (n = 10) and hedgerows (n = 13). One-way ANOVA: F = 5.544, p = 0.028. Characters above bars indicate the results of Bonferroni multiple comparisons, p < 0.05.

Some hedgerows tend to group with their adjacent forest patches (e.g., H4, F4, H2, F2-3), although this pattern is not consistent throughout, and not consistent for hedgerows with similar history in this system. The first canonical axis resulting from the redundancy analysis is significant (p = 0.007) and displays a strong species–habitat correlation (r = 0.772). The variance explained represents 11.2% of the variance in species composition between sites. Many species were relatively infrequent in this system and did not contribute in the characterization of habitats. The ordination is based on the 29 most common species after Chord transformation. The distance biplot (Fig. 3) shows that more than half of the most common species tend to be more abundant in forest patches. Species such as Trillium grandiflorum and Caulophyllum thalictroides are highly associated with a forest habitat, while others such as Maianthemum

Fig. 2 – PCA ordination of sampling sites based on species abundances.  = hedgerow (n = 13), e = forest patch (n = 10). Forest patches are given the number(s) of the hedgerow(s) attached to it.

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ory) were marginally less present in hedgerows than in forest patches (p = 0.0528). Regarding pollination mode, abiotic pollination tended to be less represented in hedgerows than in forest habitats. Finally, the capacity for vegetative propagation was highly positively associated with hedgerows.

3.3.

Emergent groups and habitat relationships

The K-means partitioning resulted in the formation of 6 emergent groups (Table 1). Ferns (group 3) and wind-pollinated species (group 5) formed two easily describable clusters. The four other groups contained more variation in traits. Group 2 enclosed mostly species dispersing their seeds early in the season. Group 4 had many plants dispersing their seeds by August with the help of animal vectors and members of group 6 exhibited a late flowering phenology. Group 1 was more heterogeneous. The fourth-corner analysis revealed that both emergent groups 2 and 3 were under-represented in hedgerows.

Fig. 3 – Redundancy analysis (RDA) ordination biplot illustrating species preferences to a given habitat type. The ordination is based on the 29 most common species following Chord transformation. Habitat variation was significantly related to the first canonical axis (999 Monte Carlo simulations; p = 0.007), explaining 11.2% of the total variance.

racemosum and Maianthemum canadense are associated with hedgerows.

3.2.

Relationship of species attributes to habitat type

Based on the results of the fourth-corner analysis with presence–absence data, the relationship between habitat types and demographic attributes was globally significant for 3 of the 11 studied attributes: flowering phenology, seed dispersal phenology and dispersal mode. The same three attributes were globally significant when calculated from species abundance data, in addition to pollination mode and vegetative propagation capacity (Table 2). Regarding flowering phenology, early spring flowering was negatively associated with hedgerows both in terms of presence and abundance, while populations flowering in late spring tended to be more abundant in these linear habitats. Seed dispersal phenology partly mirrors results for flowering phenology with early dispersal being less common in hedgerows than forests and late summer dispersal being marginally more common in hedgerows (p nearly significant = 0.058). Populations that disperse their seeds in the fall also tended to be less abundant in hedgerows compared to forest habitats. Regarding dispersal mode, ant-dispersal (myrmecochory) and, to a lesser extent, wind-dispersal (anemochory) were strategies that were less common in hedgerows than in forest patches. Species with no specific means of dispersal (baroch-

4.

Discussion

4.1.

Species richness and composition

Significant differences in the composition and abundance of native forest herbs between forest habitats and hedgerows suggest the existence of a selective pressure on forest species in linear habitats. Although 83% of the species surveyed in forest patches were present in hedgerows, abundance patterns vary greatly among species and among habitats. The species that were not found in hedgerows tended to be also uncommon in our survey of forest patches, suggesting that limitations for these species could be related to microhabitat availability at the landscape scale. For instance, one such species, Epifagus virginiana, is a parasite on Fagus grandifolia, a tree rarely found in hedgerows and that has become less common in regenerating forests sites (Brisson and Bouchard, 2003). The loss of the less common or less tolerant species from disturbed communities is a pattern often reported in ecological studies, with possible consequences for functional diversity (Walker, 1992; Walker et al., 1999). Many species were found at relatively low abundances in hedgerows compared to forest patches (Fig. 2). For example, Caulophyllum thalictroides and Trillium grandiflorum were two of the most frequent forest herbs in forest patches but they were always found at low abundances in hedgerows. For such species, lower abundance in hedgerows may hide a long-term extinction debt (Honnay et al., 2005) that can only be assessed by careful monitoring of population dynamics in hedgerows and adjacent forest patches. Species like Maianthemum racemosum, or Actaea rubra, on the other hand, appear more tolerant of hedgerow conditions or may have been able to recolonize after disturbances. Such species are potentially more likely to benefit not only from the habitat function provided by hedgerows, but also from the corridor function which would necessitate continued reproduction and efficient dispersal within the hedgerow. We discuss below how the measured traits that were significantly related to habitat conditions could facilitate or limit the survival, reproduction or dispersal of forest herbs, acknowledging that

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the relations observed, while not necessarily causal, can nevertheless point to important ecological processes in this system.

4.2.

Relationship of species attributes to habitat type

Our results show that the selective pressures that act on the measured traits for forest herbs in these linear habitats are mostly related to the timing of reproduction and the modes or timing of dispersal. The differences observed in the distribution of the timing of flowering events, and consequently of seed dispersal events, suggest a link between microclimatic conditions in hedgerows and the survival and reproduction of forest herbs. It is possible that the under-representation of early flowering species and late seed maturing species in hedgerows is determined partly by the higher risk of late frosts in spring and early frosts in fall, damaging the reproductive organs before flowers or fruits have reached maturity. In fact, a preliminary comparison of spring temperatures between hedgerows and forest patches in order to assess differences in climatic conditions seems to support the hypothesis of lower night temperatures in hedgerows (Roy and de Blois, unpublished data). Lower temperatures early in the growing season in the exposed environment of hedgerows may also limit pollinator activities, as evidence from forest edge surveys tend to demonstrate (Jules, 1998). Flowering late in the spring when light intensity is still high before full competition from the dense shrub layer and ruderal species, but stressful climatic events less likely, might be a more efficient adaptation in hedgerows. Several studies demonstrated a link between dispersal mode and migration rate of woodland herbs in successional forests (Matlack, 1994; Brunet and Oheimb, 1998; Bellemare et al., 2002; Takahashi and Kamitani, 2004). In our system, very slow dispersal by myrmecochore and barochore seeds does not seem to be advantageous in hedgerow conditions, especially if the hedgerow had to be recolonized from adjacent forest patches. Accordingly, the dispersal rate reported for myrmecochore and barochore seeds in the literature does not appear sufficient for frequent establishment of these species in hedgerows within the time-scale assumed by our historical data, a pattern which is consistent with other studies on forest herb migration (Takahashi and Kamitani, 2004). It can be reasonably assumed, on the other hand, that anemochory should facilitate dispersal at the landscape scale and into hedgerows especially if the latter act as trap for seeds. Surprisingly, however, we found that wind dispersal was less common in hedgerows than in forest patches. Wind dispersed seeds were also comparatively slow at dispersing into artificial forests in a study conducted by Takahashi and Kamitani (2004). Contrary to wind-dispersed seeds of trees for instance, propagules of low-lying species may disperse relatively close to the source. Another hypothesis that would require further testing is that, given the narrow size of hedgerows, most wind dispersed seeds or wind dispersed pollen produced within hedgerows are lost in unfavourable adjacent agricultural habitats. Therefore, the probability for abiotically, or rather randomly, dispersed propagules of finding a safe site within hedgerows could be lower than the one for biotically dispersed species whose vectors discriminately use corridors to move across

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the landscape (Tewksbury et al., 2002). Endozoochory, however, was not associated with a particular habitat type in our system. The most significant measured attribute associated with increased densities of forest herb populations in hedgerows was the capacity for vegetative propagation. Dupre´ and Ehrle´n (2002) found clonal perennials to be negatively affected by patch isolation in Swedish forests. Using an emergent group approach, Kolb and Diekmann (2005) found similar patterns for clonal forest specialists with few diaspores in German forests, suggesting that reproductive strategy could be a good predictor of the response to fragmentation. Vegetative propagation should contribute little to hedgerow colonization from adjacent forest patches unless there is spatial continuity between habitats. However, it could be an advantageous strategy, at least temporarily, allowing for population persistence in hedgerows particularly if conditions are not adequate for sexual reproduction because of harsher climatic conditions or lack of pollinators. For remnant populations, this could provide an insurance against rapid extinction in suboptimal habitats. Species such as Maianthemum racemosum, which was associated with hedgerows in our analysis, produce not only ramets but also apomictic seeds. Similarly, Maienthemum canadense can produce several ramets well before flowering. On the other hand, species such as Trillium grandiflorum that lacks vegetative propagation could be maintained at lower abundance in hedgerows compared to clonal species or gradually decline, especially if environmental conditions were to affect T. grandiflorum reproductive performance within hedgerow populations, as suggested for post-agricultural forests (Vellend, 2005). It is possible that other traits or strategies that we did not evaluate for lack of data are similarly affected and that the significant traits in our study are correlated with other unmeasured traits causing the patterns observed. Other demographic attributes such as longevity, the presence of a persistent seed bank (Dupre´ and Ehrle´n, 2002), the time required for seed germination, dormancy, the age of first reproduction and the mean dispersal distance could have given additional insights into the processes that allow the recruitment or persistence of forest herbs in hedgerows. Competitive ability against ruderal species and response to disturbances such as high levels of soil phosphate (Honnay et al., 1999), or herbicide drift (Jobin et al., 1997) may also be important factors explaining the reduced frequency of many forest herbs in hedgerows. Competitive ability may be partly related to plant height though, but we did not detect any significant pattern for this trait.

4.3.

Relevance of the emergent group approach

While the use of emergent groups was meant to facilitate the management of a large number of species and traits, this trait-based classification of woodland herbs only partly reinforced conclusions from analysing individual traits in our system. The significant groups that were formed supported results for the low representation of early dispersers (group 2), abiotic pollination and wind-dispersal (group 3) in hedgerows. As happened with ferns in this study, most trait-based classifications of plants found in the literature

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converge to a growth-form-based classification (e.g. Leishman and Westoby, 1992; Lavorel et al., 1997; Mabry et al., 2000). For example, while studying the environmental response of plants in Belgian hedgerows, Deckers et al. (2004b) classified ‘‘long-lived early flowering species with woodland preference’’ as one functional type. Finding emergent groups within species assemblages that present little variation in traits, like temperate forest herbs, represents a challenge (McIntyre and Lavorel, 2001). Deciding which attributes should make the basis for group partition and specifying the categories for each one is inherently subjective, resting on data availability and our judgment (Simberloff and Dayan, 1991). In our case, an individual-trait-based approach was informative, although there is certainly benefit in evaluating whether certain combinations of traits are commonly found in a given environment (Kolb and Diekmann, 2005).

5.

Conclusion

In spite of some limitations, a functional trait approach such as the one used in this study can provide relevant information for conservation. Several forest herbs in our system appear able to survive the disturbances in hedgerows for extended periods of time, or have been able to colonize hedgerows relatively rapidly. Because they have evolved as long-lived perennials, it seems possible for some forest herbs to persist, at least temporarily, under suboptimal conditions in hedgerows. The extent to which their presence at a site reflects past or present environmental or spatial landscape conditions, however, is not entirely clear, and for many species we lack the most basic information about their ability to withstand or escape disturbances. However, it appears from our study that certain traits could be associated with the survival or vulnerability of forest herbs in hedgerows and that both dispersal and environmental heterogeneity at a site regulate species persistence in this system. The long-term viability of species showing several traits that make them more vulnerable to hedgerow conditions (e.g. early flowering, lack of vegetative propagation) and therefore their ability to benefit from the corridor function provided by hedgerows remain however questionable. Special attention should therefore be given to species presenting such traits in designing or conserving forested corridors. Our survey was biased towards wooded hedgerows that tended to be species-rich. However, several wooded hedgerows that were initially surveyed in our study area and that appeared adequate as habitat for forest herbs were speciespoor, suggesting that other factors that remain to be identified could seriously limit the presence of forest herbs in linear habitats. A better understanding of the processes associated with the selection of specific traits and by which biodiversity is maintained in intensively managed landscapes should help us develop efficient conservation strategies that maximize the conservation potential of remaining habitats. This study highlights some of the traits of native forest species that could make them vulnerable to further intensification, but also provides insights on those characters that are most likely to benefit from the maintenance or restoration of wooded corridors in an inhospitable matrix.

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Acknowledgements This research was supported by an FQRNT scholarship to V. Roy and FQRNT and NSERC grants to S. de Blois. We are grateful to J. Snider for his assistance in the field. We wish to thank P. Legendre, S. Dray and R. Schmucki for valuable statistical support and J. Brisson for reviewing an earlier draft of this manuscript.

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