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BIOLOGICAL CONSERVATION 141 (2008) 298 307

BIOLOGICAL CONSERVATION 141 (2008) 298 – 307 available at www.sc iencedirect.com journal homepage:

available at www.sc iencedirect.com

141 (2008) 298 – 307 available at www.sc iencedirect.com journal homepage: www.elsevier.com/locate/biocon

journal homepage: www.elsevier.com/locate/biocon

141 (2008) 298 – 307 available at www.sc iencedirect.com journal homepage: www.elsevier.com/locate/biocon
141 (2008) 298 – 307 available at www.sc iencedirect.com journal homepage: www.elsevier.com/locate/biocon

Evaluating hedgerow corridors for the conservation of native forest herb diversity

Vale´ rie Roy, Sylvie de Blois*

Department of Plant Science and the McGill School of Environment, McGill University, Macdonald Campus, 21, 111 Lakeshore Road, Sainte Anne de Bellevue, Que´bec, Canada H9X 3V9

ARTICLE INFO

ABSTRACT

Article history:

The maintenance of connecting habitats such as hedgerows in production landscapes

Received 30 January 2007

could become increasingly critical as species migration is expected to accelerate with

Received in revised form

climate change. Species of particular conservation interest that could benefit from con-

1 October 2007

necting habitats especially in agroecosystems are native forest herbs. It is still unclear,

Accepted 14 October 2007

however, which hedgerow habitats have the best potential of supporting diverse forest herb

Available online 26 November 2007

communities, making it hard to target particular structures for conservation. Our objective

was to identify the local and landscape characteristics of hedgerows that could help predict

 

Keywords:

their potential at maximizing the richness, abundance, and diversity of native forest herbs

Agricultural landscapes

of temperate deciduous forests of North-East America. We used multiple regression, Mor-

Biodiversity conservation

an’ I correlograms, and conditional autoregressive models to assess the effect of landscape

Biological connectivity

and historical variables (hedgerow age, amount of adjacent forest cover, connection to for-

Linear habitats

ests and other hedgerows) and of local variables (hedgerow width, canopy cover, cover of

Forest fragmentation

other species) on the response variables. The results show an increase in forest herb diver-

Plant dispersal

sity and abundance in hedgerows with time and with increasing nearby forest cover. Local

factors such as greater width and reduced cover of other species also relate to a greater

abundance and diversity of forest herbs in linear habitats. The fact that forest herb com-

munities can reassemble in hedgerow corridors with time implies that there could be

long-term benefits in maintaining and even creating linear habitats where there is a pool

of dispersing forest herbs.

2007 Elsevier Ltd. All rights reserved.

1.

Introduction

There is growing evidence that the achievement of biodiver- sity conservation objectives at the landscape or regional scale will have to take into account not only habitats within re- serves, but also the contribution of habitats in production landscapes (Saunders et al., 1991; Cabeza and Moilanen, 2003; Polasky et al., 2005). This implies a better assessment of the ecological functions of intensively managed habitats, including habitat corridors ( Townsend and Levey, 2005; Dams- chen et al., 2006), that would allow them to contribute signif-

icantly to the maintenance of biodiversity, even under suboptimal conditions. Whereas much research has been conducted to identify key factors in the selection of optimal habitats for reserves (e.g., Margules and Pressey, 2000; Lee et al., 2001), there is much to be done to extend and test similar emergent principles in habitats found in landscapes under intense management pressure ( Pereira et al., 2004; Fischer et al., 2006). In this paper, we investigate components of native plant biodiversity in agroecosystems focusing on a system of woo- dy hedgerows at the margin of agricultural fields. Because of

* Corresponding author: Fax: +1 514 398 7897. E-mail address: Sylvie.deblois@mcgill.ca (S. de Blois). 0006-3207/$ - see front matter 2007 Elsevier Ltd. All rights reserved.

doi:10.1016/j.biocon.2007.10.003

B IOLOGICAL CONSERVATION 141 (2008) 298 307

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their spatial and structural attributes, hedgerow habitats can extend forest conditions into production land ( de Blois et al., 2002b), potentially enhancing connectivity between frag- mented forest habitats ( Corbit et al., 1999). The maintenance of connecting habitats in production landscapes could be- come increasingly critical as species migration is expected to accelerate with climate change. Species of particular con- servation interest that could benefit from these habitats are the native forest herbs of temperate deciduous forests of North America and Europe, a subset of which has been com- monly reported in linear habitats ( Boutin and Jobin, 1998; de Blois et al., 2002a; Freemark et al., 2002; Deckers et al., 2005a; Roy and de Blois, 2006). It is still unclear, however, which hedgerow habitats have the best potential of support- ing diverse forest herb communities, making it hard to target particular structures for conservation. Our objective in this study was to identify the characteris- tics of hedgerows that could help predict their potential at maximizing native forest herb richness, abundance, and diversity. We addressed this issue at two levels and by mod- eling species richness, abundance, and diversity in relation to selected predictor variables for each level of observation. Landscape (or historical) variables such as adjacent forest cover or hedgerow age can usually be obtained from remote sensing data in most areas. They could help in the design of regional or landscape conservation plans for the selection of linear structures showing the best potential for conservation. In our landscape models, the sampling unit was a hedgerow. The local variables are those that depend largely on manage- ment practices at the field scale. They could help in providing on-site qualitative management guidelines that promote the persistence of native species in production landscapes. In our local models, the sampling unit was a hedgerow section that can differ in width, canopy cover, etc. In addition, since spatial autocorrelation can be a significant problem in a data- set such as ours, we compared the performance of standard regression models and models accounting for spatial covari- ance ( Lichstein et al., 2002). Finally, we discussed the insights that such models can indirectly lead into the underlying pro- cesses (i.e., patterns of dispersal, establishment, and sur- vival) that help maintain the diversity of semi-natural systems.

2.

Methods

2.1. Study area

The study was conducted in an area of ca. 20 km · 20 km at the boundary (45 40 0 N, 74 1 0 W) of Mirabel (48 594 ha) and Deux-Montagnes (30 499 ha), two regional county municipal- ities located west of Montreal, Quebec, Canada. This region is part of the St. Lawrence Lowlands Ecoregion marked by moist summers and cold, snowy winters ( Ecoregions Work- ing Group, 1989). Mature deciduous forests are dominated by Acer saccharum Marsh, in association with Carya cordifor- mis (Wang.) K. Koch., Fagus grandifolia Ehrh., and Fraxinus pennsylvanica Marsh ( Grandtner, 1966). The region has undergone extensive forest clearing for agriculture, indus- trial and urban development in the past two centuries, with continued pressure from agricultural intensification ( Jobin

et al., 2007) and, more recently, from suburban intensifica- tion (pers. obs.). Forest cover in the two counties was around 25% in 2001 and had remained stable since 1993 ( Jo- bin et al., 2007). Forest patches remaining within the agri- cultural matrix measure 19 ha on average ( Be´ langer et al., 1998). Agricultural land-uses in the two counties occupy be- tween 42% (Deux-Montagnes) and 63% (Mirabel) of the land- scape and include dairy farming (hay fields, pasture, fallow lands) as well as more intensive cultivation (corn and spe- cialized crops) (Jobin et al., 2007). The rest is urban or indus- trial area.

2.2. Landscape variables

Using recent aerial photographs and ground survey, we se- lected 117 hedgerows characterized by a woody cover (tall shrub or tree) and located at the margin of agricultural fields. We ignored hedgerows concealing a major drainage ditch be- cause of the different type of understory vegetation in these structures. There was no minimal distance set between hedgerows although parallel hedgerows in this landscape will usually be separated by a field at least 200 m wide. With the exception of the adjacent land-use that was determined in the field, we gathered information on historical and land- scape-scale habitat characteristics (Table 1) through aerial photographs. We used a series of aerial photographs from 1930 (the oldest available), 1949, 1954, 1964, 1970, 1977, 1983, 1988, 1994, and 1999 (scale from 1:20 000 to 1:5000) to evaluate the minimum age of a hedgerow. Hedgerows in this land- scape tend to separate properties or different types of fields. The surveyed hedgerows originated either during the time period covered by the aerial photographs through spontane- ous regeneration at the edge of open fields (except for two hedgerows that were recent forest remnants) or originated prior to the time covered by the aerial photographs. In the latter case, it is possible that some hedgerows present in the 1930s were linear remnants of the forest that had origi- nally been cleared for agriculture, but they could also have originated at the edge of open fields. In southern Quebec, lots tended to be large at first but were often subdivided into smaller ones ( Brisson and Bouchard, 2003), possibly resulting in new hedgerows. As well, tree size may not correlate well with tree age in open field conditions ( de Blois and Bouchard, 1995) and therefore the exact origin of some of the hedgerows cannot be known only from aerial photographs. We calcu- lated minimum age of a hedgerow using the first time a woo- dy (i.e., shrubs, scattered trees) cover was present on aerial photographs with previous photographs showing no hedge- row structure. We corroborated the historical data by coring trees in hedgerow sections. The majority of trees cored were on average younger than the age assigned to the hedgerow structure itself. Hedgerows that had never been clear-cut since 1930 were assigned a minimum age of 85 years old, the age of the oldest trees. Aerial photographs from 1999 were integrated into a GIS (ArcView 3.3, ESRI, 2002). We calculated the total area of forest contained in buffer zones of 50, 100, and 200 m around each surveyed hedgerow as an estimate of the potential available habitat for the forest species pool for recolonization in hedge- rows ( Butaye et al., 2002). These distances were chosen be-

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BIOLOGICAL CONSERVATION 141 (2008) 298 307

Table 1 – Predictor variables for landscape and local regression models (including abbreviations used in models)

Level

Variable

Range

Landscape

Age of hedgerow (AGE) Intensity of adjacent land-use (LANDUSE) Forest area in a 50 m/100 m/200 m buffer (F50/F100/F200)

6–85 years Low, medium, high 0–11 801/0–49 216/0–207 771 m 2 0–275/0–1052/0–3090 m

Length of the hedgerow network in a 50 m/100 m/200 m buffer (N50/N100/N200)

#

of connections to a forest patch (F_CONN)

0–2

of connections to other hedgerows (H_CONN) Length of hedgerow *

#

0–4

40–590 m

Local

Hedgerow width (WIDTH) Canopy cover (CANOPY) Tree basal area (TREE) Shrub cover (SHRUB) Ruderal herb cover (RUDERAL) Available ground space (GROUND)

1.5–32.7 m

0–100%

0–0.038 m 2 /m 2 0–10%, 11–25%, 26–50%, 51–75%, 76–100% 0–10%, 11–25%, 26–50%, 51–75%, 76–100% 0–10%, 11–25%, 26–50%, 51–75%, 76–100%

* Length was used as a covariable to control for sampling effort.

 

cause many species in our species pool are expected to dis- perse mostly at small distances ( Roy and de Blois, 2006). With- in the same buffer areas, the summed length of neighboring hedgerows was also calculated with the assumption that a well connected network could facilitate dispersal (Sarlo¨ v Her- lin and Fry, 2000; Bartuszevige et al., 2006). Since longer hedgerows generate greater buffer areas, we brought values to a common scale by dividing forest cover by buffer area and by dividing the total length of neighboring hedgerows by the length of the associated hedgerow. We also noted the number of direct connections to forest patches and to perpen- dicular hedgerows. The adjacent land-use was classified into three classes of land-use intensity (adapted from Boutin and Jobin, 1998), from the lowest intensity with forage or pasture on both sides of the hedgerow to highest intensity with cash crops on both sides of the hedgerow.

2.3. Floristic survey

We inventoried the forest herb composition of the 117 hedge- rows, which added up to a total of 26.6 km of linear structure sampled. The floristic survey took place in May and June 2005 to include early spring and summer species. For this study, ‘forest herbs’ were defined as herbaceous, vascular plants characteristic of the understory of temperate deciduous for- est interior and described as such by Marie-Victorin (1995), a local authority. For the total length of each hedgerow, we positioned contiguous quadrats (5 m long by 2 m wide) cen- tered on the midline (or close by in the presence of a stone wall). In each quadrat, forest herb populations were charac- terized by occurrence and abundance. We used a semi-quan- titative measure of abundance based on the number of rooted stems, including seedlings (class 1 = 1; class 2 = 2–10; class 3 = 11–25; class 4 = 26–50; class 5 = more than 50). For analysis at the hedgerow level, we calculated: (1) forest herb species richness as the total number of native forest herb species present within a hedgerow; (2) forest herb abundance as the sum of the abundance (using mid-class value) of all species in all quadrats of a hedgerow, and (3) the Shannon–Weiner diversity index calculated as P p i log(p i ) where p i is the rela- tive frequency of species i in the hedgerow.

2.4. Local variables

Once the canopy was fully developed in June–July, we re- turned to the same hedgerows to describe habitat structure. Starting at the same position, we sampled every four quadrats (5 m long by 2 m wide) for the whole length of the hedgerow for structural characteristics. Each structural quadrat is there- fore associated with 4 contiguous floristic quadrats, which we defined as a hedgerow section measuring 2 m · 20 m. Given the relative homogeneity of hedgerow structure across a given section, we assumed that the structural variables mea- sured in the first 5 m of a section were consistent throughout the 20 m. Consequently, for a given 20 m section, species rich- ness, abundance and Shannon’s diversity index were calcu- lated by pooling the vegetation data collected in the four corresponding floristic quadrats. For each hedgerow section, we collected information on six local habitat variables ( Table 1). We measured width be- tween the lateral limits of woody vegetation growth. We quantified the degree of canopy closure in the center of the quadrat using a convex spherical densiometer (Robert E. Lem- mon, Forest Densiometers). Total basal area characterized tree density and was established by measuring the diameter at breast height of each living tree greater than 3.5 cm of diameter found in the quadrat. We visually estimated shrub cover within the 5 · 2 m quadrat to the closest percentage class (class 1 = 0–10%; class 2 = 11–25%; class 3 = 26–50%; class

4 = 51–75%; class 5 = 76–100%). The total cover of all herba-

ceous species other than native forest species (i.e., ruderal herb cover) as well as the available ground space (character- ized as ground space free from rocks, trunks or other debris) were also visually estimated to the closest percentage class but inside a 1 · 1 m plot positioned in the center of the larger

5 · 2 m quadrat.

2.5. Data analysis

We investigated: (1) the effect of landscape variables alone (landscape model) and (2) the effect of local variables alone (local model), on three separate response variables, i.e., forest herb species richness, abundance and diversity. To insure

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consistency in the way we measured hedgerow ages, we ex- cluded from the landscape model 27 hedgerows that had a mature structure in 1954 but for which older aerial photos (1930, 1949) were unavailable. We also excluded the only 2 hedgerows for which we had evidence that they were still part of a forest patch 41 years ago since they were the only remnant hedgerows of known origin and were clearly outliers in our system. In the landscape model, hedgerows ( n = 88) were considered the sampling unit. For the local model, sec- tions ( n = 1174) were considered the sampling unit. We standardized all explanatory variables. We normalized the response variables of the landscape models using a Box– Cox transformation. Richness and abundance data of the lo- cal models were square-root transformed in order to reduce skewness and kurtosis. No transformation could improve normality of local Shannon data. Because there were a signif- icant relationship between hedgerow length and the response variables and since we were interested in effects beyond those related to sampling effort in hedgerows of different length, we chose to use in our landscape models the residuals of a linear regression with standardized hedgerow length as the response variable (linear regression, N = 88 hedgerows, standardized length vs richness: R 2 = 0.18, p < 0.0001; length vs abundance: R 2 = 0.30, p < 0.0001; length vs diversity:

R 2 = 0.12, p = 0.0015). For the landscape and local models, we conducted three series of analysis: (1) an ordinary least square multiple regres- sion (OSL); (2) calculation of spatial autocorrelation in the residuals of the preliminary regression models; (3) conditional autoregressive model (CAR) that includes spatial effect. For the ordinary least square (OLS) multiple regression, a step- up procedure, as detailed below, was preferred over a step- wise approach because some of the explanatory variables were strongly intercorrelated ( Ambrosini et al., 2002; Betts et al., 2006). We first evaluated the relative importance of each explanatory variable with a likelihood ratio test for nested models (Haining, 1990; Lichstein et al., 2002; Tognelli and Kelt, 2004). Larger likelihood ratio values indicate a greater contri- bution to the model. We manually entered independent vari- ables in order of decreasing likelihood ratio statistic until additional predictors became non-significant when added to the model. The correlation structure of variables entering final models were investigated to ensure they were not corre- lated. For each pair of explanatory variables with a correlation greater than 0.6, the variable with the greater residual devi- ance was excluded. By violating the independence assumption of classical sta- tistical tests, spatial autocorrelation can result in an overesti- mation of habitat effects on species distribution ( Legendre, 1993; Lichstein et al., 2002; Betts et al., 2006). This effect can be important in linear habitats ( Maheu-Giroux and de Blois, 2007) and especially with a sampling scheme such as ours be- cause nearby hedgerows or hedgerow sections are likely to share common characteristics. We chose to retain as much information as possible in our large dataset, including infor- mation about spatial structure, and potentially increase statistical power. We accounted for spatial effect statistically by first looking for spatial autocorrelation in the residuals of all the preliminary regression models using Moran’I correlo- grams (Moran, 1950). For the landscape models, we set incre-

ments at 200 m (average field width) up to a maximum distance of 10 000 m. For the local models, we set increments at 20 m (length of a section) up to a maximum distance of 600 m (length of the longest hedgerow). We calculated the sta- tistical significance of I with permutation tests (999 permuta- tions) conducted for each distance class separately. We first verified the global significance of each correlogram using a regular Bonferroni correction for multiple tests ( Legendre and Legendre, 1998). We then determined the significance of I for each distance class using the progressive Bonferroni correction in which a is divided by the current class number ( Legendre and Legendre, 1998). These analyses were carried out using Matlab 7.0 ( Mathworks, 2004). When spatial autocorrelation was detected, we accounted for it using a conditional autoregressive model (CAR) ( Hain- ing, 1990; Cressie, 1993; Lichstein et al., 2002; Tognelli and Kelt, 2004; Maheu-Giroux and de Blois, 2007). CAR models as- sume that the response is a function of both the explanatory variables and the values of the response at neighboring loca- tions. Autoregressive models are similar to ordinary least squares models, with the addition of an autocovariate, a term related to the residual variation in neighboring locations ( Keitt et al., 2002). The neighborhood relationship is expressed in a symmetric matrix of spatial weights. We defined weights to decrease with increasing distance between locations ( w ij = 1/distance ij for landscape models; w ij ¼ 1=distance ij for local models) up to a maximum neighborhood distance. The latter was selected as the maximum distance at which the residuals from the preliminary model were autocorrelated. As for the preliminary models, we tested the contribution of each explanatory variable with the presence of the autocovar- iate using a likelihood ratio test. We used Nagelkerke R 2 to as- sess OLS and CAR models goodness of fit ( Lichstein et al., 2002). All multiple regression analyses were conducted using R software ( CRAN, 2005).

2

3.

Results

Fifty-one forest herb species were identified in our hedgerows ( Table 2 ). We found between 0 and 30 forest herb species, with an average of 10 species per hedgerow. Eight species were rather common (frequency >50%): Maianthemum racemosum, Actaea rubra , Viola pubescens , Circaea lutetiana, Trillium erectum, Polygonatum pubescens, Caulophyllum thalictroides, and Viola sororia. For all models except the landscape model predicting diversity, OLS residuals were positively autocorrelated, indi- cating that the assumption of independent errors was vio- lated and required to be corrected by the addition of an autocovariate term. As expected, the effect of the autocovar- iate on species occurrence or abundance was highly signifi- cant both at the local and landscape level ( Tables 3 and 4). Although regression coefficients changed as a result of including an autocovariate, all variables significant in the OLS models remained significant in the CAR models. Likeli- hood ratio statistics indicate that age and neighboring forest cover had a similar input in the CAR landscape model and that width was the most important variable in the CAR local model ( Fig. 1). In general, the significant variables tended to explain abundance better than richness or Shannon diversity.

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BIOLOGICAL CONSERVATION 141 (2008) 298 307

Table 2 – Relative frequency (number of hedgerows in which species i occurs/total number of hedgerows) pre- sented in decreasing order and relative abundance (sum of total abundance for species i in all hedgerows/sum of total abundance for all species) for 51 species of forest herbs sampled

Species

Frequency Abundance

(%)

(%)

1. Maianthemum racemosum (L.) Link

90.60

18.55

2. Actaea rubra (Ait.) Willd.

85.47

6.63

3. Viola pubescens Ait.

71.79

7.11

4. Circaea lutetiana L.

70.94

9.97

5. Trillium erectum L.

61.54

4.08

6. Polygonatum pubescens (Willd.) Pursh

58.97

3.50

7. Caulophyllum thalictroides (L.) Michx.

53.85

1.37

8. Viola sororia Willd.

52.14

4.99

9. Maianthemum canadense Desf.

41.88

3.13

10. Athyrium felix-femina (L.) Roth

41.03

2.40

11. Hydrophyllum virginianum L.

34.19

9.85

12. Erythronium americanum Ker-Gawl.

33.33

8.12

13. Sanguinaria canadensis L.

33.33

1.33

14. Trillium grandiflorum (Michx.) Salisb.

33.33

2.75

15. Onoclea sensibilis L.

27.35

1.57

16. Carex radiata (Wahlenb.) Small

22.22

2.11

17. Actaea pachypoda Ell.

20.51

0.16

18. Asarum canadense L.

19.66

1.71

19. Arisaema triphyllum (L.) Schott

17.09

0.85

20. Carex gracillima Schwein.

17.09

1.62

Dryopteris carthusiana (Vill.) H.P. Fuchs

21.

17.09

0.48

22. Aralia nudicaulis L.

15.38

0.59

23. Dryopteris marginalis (L.) Gray

11.11

0.39

24. Ranunculus abortivus L.

11.11

0.38

Dryopteris intermedia (Muhl. Ex Willd.) Gray

25.

10.26

0.32

26. Matteuccia struthiopteris (L.) Todaro

10.26

1.51

27. Uvularia grandiflorum Sm.

10.26

0.42

28. Allium tricoccum Ait.

8.55

0.93

29. Impatiens capensis Meerb.

8.55

0.91

30. Thalictrum dioicum L.

6.84

0.15

31. Carex deweyana Schwein.

5.13

0.26

32. Streptopus lanceolatus (Ait.) Reveal

5.13

0.11

33. Tiarella cordifolia L.

5.13

0.11

34. Prenanthes alba L.

3.42

0.03

35. Viola canadensis L.

3.42

0.08

36. Carex peckii Howe

2.56

0.43

37. Viola labradorica Schrank

2.56

0.05

38. Carex hirtifolia Mackenzie

1.71

0.07

39. Carex intumescens Rudge

1.71

0.04

40. Dicentra canadensis (Goldie) Walp.

1.71

0.68

41. Orthilia secunda (L.) House

1.71

0.02

42. Adiantum pedatum L.

0.85

0.00

Athyrium thelypterioides (Michx.) Desv.

43.

0.85

0.03

44. Carex blanda Dewey

0.85

0.02

45. Carex leptonervia (Fern.) Fern.

0.85

0.02

46. Carex pedunculata Muhl. ex Willd.

0.85

0.02

Dennstaedtia punctilobula (Michx.) T. Moore

47.

0.85

0.03

48. Dicentra cucullaria (L.) Bernh.

0.85

0.02

49. Hepatica nobilis Schreb.

0.85

0.04

50. Osmunda claytoniana L.

0.85

0.01

51. Pteridium aquilinum (L.) Ku¨ hn

0.85

0.05

Note : Nomenclature follows the Integrated Taxonomic Information System (ITIS) on-line database ( http://www.itis.usda.gov ).

For the landscape model, adjacent forest area and hedgerow age were both positively related to species richness, abun- dance and diversity (Table 3). Species richness also increased with the number of connections to other hedgerows and spe- cies abundance decreased with increasing land-use intensity, although these relationships were less important than the one for forest cover and age. A simple linear regression of spe- cies richness or species abundance on forest cover or on hedgerow age confirms that the relationships, although weak, were highly significant (Fig. 2). The local model indicated that abundance, richness and diversity increased with hedgerow width, canopy cover, and available ground space ( Table 4 ). Shrub cover and ruderal herb cover were negatively related to the response variables, especially abundance. Tree basal area was not retained in the model. Residuals from CAR mod- els showed no autocorrelation suggesting that the CAR mod- els were appropriate.

4.

Discussion

While selecting hedgerow habitats for biodiversity conserva- tion in production landscapes, two variables among the set we considered stand out as being good predictors of forest herbs species abundance and richness: the presence and abundance of a forest cover in the immediate surrounding and the time since the hedgerow was first colonized by trees or tall shrubs. The latter relationship suggests that the poten- tial of newly created linear habitats to support species-rich native plant communities increases with time, with clear implications for conservation and the corridor function. Temperate forest herbs are often characterized by long generation times; they produce relatively few seeds that lack adaptations for long-distance dispersal and several can repro- duce vegetatively ( Bierzychudek, 1982; Whigham, 2004). The maintenance of a forest cover nearby hedgerows likely pro- vides a pool of dispersing propagules for hedgerow coloniza- tion. This could be especially important for forest herbs that have limited colonization capacities, such as ant-dispersed species and species with no specific dispersal mode. Roy and de Blois (2006) showed that species with these traits gen- erally occurred less in hedgerows than in forest interior. The dispersal limitation of forest herbs in isolated habitats or in recent or post-agricultural forests has also been well docu- mented (Peterken and Game, 1984; Grashof-Bokdam, 1997; Butaye et al., 2001; Singleton et al., 2001; Kolb and Diekmann, 2004). As well, the extent of remnant (or ancient) forest cover left in a landscape has been linked to the species richness of forest herb communities in post-agricultural sites (Vellend, 2003). Whereas hedgerows adjacent to forest patches can be colonized more readily by forest species, especially if dis- persal vectors use both the forest and adjacent hedgerows, only good dispersers will colonize isolated hedgerows. At the landscape scale, plant populations are not only linked by seed or propagule dispersal, but also by pollen ex- change. These exchanges with larger nearby populations in forest can contribute to the fitness of small connected popu- lations in hedgerows, especially for populations of self- incompatible species such as Trillium grandiflorum (Schmucki and de Blois, in review). Populations of this species have been

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Table 3 – Parameter estimates with significance level for two types of regression models (OLS and CAR) relating each of forest herb richness, abundance, or diversity in hedgerows with landscape variables

Variable

OLS model a

CAR model b

Richness

 
 

AGE

0.38 *

0.32 *

F200

0.46 **

0.54 ****

H_CONN Autocov 200 m

0.24

25.72 ***

Abundance

 
 

AGE

1.23 *

2.20 **** 1.44 ** 1.03 * 51.91 ****

F200

1.64 **

LANDUSE Autocovariate 400 m

Diversity

 
 

AGE

0.16*

N/A c

F200

0.21 **

N/A

Only the significant variables are included. Refer to Table 1 for definitions of abbreviations.

a

OLS = ordinary least squares model based on landscape

variables. The model does not account for spatial covariance.

b

CAR = conditional autoregressive model including an autoco-

variate term that accounts for spatial effect up to the maximum

distance at which the residuals from the preliminary model were autocorrelated.

N/A = absence of autocorrelation in OLS model based on diver- sity makes correction with a CAR model unnecessary.

c

*

p 6 0.01.

**

p 6 0.001.

*** p 6 0.0001. **** p 6 0.00001.

 

p 6 0.05.

found to be more genetically diverse in large forest popula- tions than in small populations ( Vellend, 2004), and could be more diverse in hedgerows connected through pollen exchanges to large forest populations than in isolated hedge- rows. In our system and at the temporal and spatial scale of our observations, the beneficial effects of connectivity seem to depend less on the maintenance of one or more direct con- nections with forests, although connections to other hedge- rows seem to play a role, than on landscape context and the extent of nearby forests. Increasing the number of intersec- tions in a hedgerow network could result in higher localized plant diversity or abundance at the nodes because of in- creased width or increased activities of animals dispersing seeds ( Deckers et al., 2005b). Because of the traits of forest herbs, we expect a time-lag in their response to changes in the landscape, either after the fragmentation of continuous forest into remnant linear habitats or when new habitat becomes available through the formation of spontaneous hedgerows. Some species with long-life cycle may persist well after fragmentation and their presence may reflect more past than current landscape condi- tions ( Lindborg and Eriksson, 2004; Vellend et al., 2006). On the other hand, secondary or post-agricultural forests often remain species-poor for extended periods of time in spite of site suitability (Honnay et al., 1999; Bellemare et al., 2002; Flinn and Vellend, 2005; Helm et al., 2006), likely because of

Table 4 – Parameter estimates with significance level for two types of regression models (OLS and CAR) relating each of forest herb richness, abundance, or diversity in hedgerow sections with local variables

Variable

OLS model a

CAR model b

Richness WIDTH CANOPY SHRUB RUDERAL GROUND Autocov 280 m

0.11 **** 0.07 * 0.16 **** 0.14 **** 0.17 ****

0.14 **** 0.05 * 0.09 **** 0.07 *** 0.07 **** 131.53 ****

Abundance WIDTH CANOPY SHRUB RUDERAL GROUND Autocov 500 m

0.68 ** 0.37 1.08 **** 1.30 **** 1.54 ****

0.93 **** 0.26 0.66 **** 0.69 **** 0.72 **** 138.40 ****

Diversity WIDTH CANOPY SHRUB RUDERAL GROUND Autocov 500 m

0.04 **** 0.02 * 0.05 **** 0.04 **** 0.05 ****

0.05 **** 0.02 * 0.03 **** 0.02 ** 0.02 ** 128.54 ****

Only the significant variables are included. Refer to Table 1 for definitions of abbreviations.

OLS = ordinary least squares model based only on local variables. The model does not account for spatial covariance.

a

b

CAR = conditional autoregressive model including an autoco-

variate term that accounts for spatial effect up to the maximum distance at which the residuals from the preliminary model were autocorrelated.

*

p 6 0.01.

**

p 6 0.001.

*** p 6 0.0001. **** p 6 0.00001.

 

p 6 0.05.

dispersal limitation (Ehrle´ n and Eriksson, 2000; Verheyen and Hermy, 2004). Our oldest hedgerows are of uncertain ori- gin and may have included remnants that would contribute to high diversity because they retained species from the origi- nal forest pool. The only two known remnant outliers that we sampled were clearly species-rich, but were also young hedgerow structure that may have yet to lose the species most sensitive to edge effects (‘extinction debt’ sensu Tilman et al., 1994). Nevertheless, the relationship we measured be- tween hedgerow age and species richness held even when we considered only a subset of the youngest hedgerows that have clearly originated during the time period we considered ( n = 49; p < 0.001). Since the absence of a seed bank in most forest herb species (Hyatt and Casper, 2000) implies a reliance on propagule dispersal to colonize new sites, this result and the observed influence of adjacent forest cover suggest that hedgerows are indeed colonized by a portion of the forest spe- cies pool over time. Colonization appears to occur at relatively short (i.e., <30 years) time scale for a subset of ‘fast’ species that could benefit from the restoration or creation of connect- ing habitats, especially when the need to migrate increases as

304

BIOLOGICAL CONSERVATION 141 (2008) 298 307

Richness

Ordinary least squares (OLS)BIOLOGICAL CONSERVATION 141 (2008) 298 – 307 Richness 80 Conditional 70 autoregressive (CAR) 60 50 40

80 Conditional 70 autoregressive (CAR) 60 50 40 30 20 10 0 Age F200 H_conn
80
Conditional
70
autoregressive (CAR)
60
50
40
30
20
10
0
Age
F200
H_conn
Width
Canopy
Shrub
Ruderal
Ground
Abundance
80
70
60
50
40
30
20
10
0
Age
F200
Landuse
Width
Canopy
Shrub
Ruderal
Ground
Diversity
80
70
60
50
40
30
20
10
0
Age
F200
Width
Canopy
Shrub
Ruderal
Ground
Likelihood ratio statistic
Likelihood ratio statistic
Likelihood ratio statistic

Significant explanatory variables

Fig. 1 – Likelihood ratio (LR) statistics for predictor variables in ordinary least squares (OLS) and conditional autoregressive (CAR) models to explain the richness, abundance, and diversity of forest herbs in hedgerows. Larger LR values indicate greater contribution to model fit. Only significant variables were included. The dotted lines separate the variables from the landscape model (left) from those of the local model (right). Refer to Table 1 for definitions of abbreviations.

expected with global warming. It will take much more time, however, for a particular hedgerow to acquire a significant proportion of the forest species pool, including the slow mi- grants, and potentially contribute to metapopulation dynam- ics if exchanges (either of seeds or pollen) are maintained with adjacent forest patches. This also assumes that manage- ment practices within the hedgerows are adequate to allow populations to survive and migrate at significant temporal scale. In this study, we did not consider species composition or traits. A previous study investigating functional traits in hedgerows of the same landscape, however, showed that spe- cies with poor dispersal capacity and species that flower very

early in the season were less likely to be present or abundant in hedgerows compared to forest interiors ( Roy and de Blois, 2006), suggesting that both dispersal effect and niche effect, perhaps at different temporal scale ( Verheyen et al., 2003), act on species distribution in this system. Among the local habitat variables, hedgerow width had the largest independent contribution and demonstrated a positive relationship with all three response variables, but mostly with species abundance. Hedgerows have a high edge-to-area ratio and are consequently more exposed to fluctuations in temperature and moisture than forests ( Murcia, 1995; Roy and de Blois, 2006). For organisms adapted

B IOLOGICAL CONSERVATION 141 (2008) 298 307

305

8 7 R 2 = 0.16 6 p < 0.0001 5 4 3 2 1
8
7
R 2 = 0.16
6
p < 0.0001
5
4
3
2
1
0
-2.5
-2
-1.5
-1
-0.5
0
0.5
1
1.5 2
Species richness
30 25 R 2 = 0.14 p = 0.0004 20 15 10 5 0 -2.5
30
25
R 2 = 0.14
p = 0.0004
20
15
10
5
0
-2.5
-2
-1.5
-1
-0.5
0
0.5
1
1.5
2
Species abundance

Hedgerow age

8 R 2 = 0.13 7 p = 0.0004 6 5 4 3 2 1
8
R
2 = 0.13
7
p
= 0.0004
6
5
4
3
2
1
0
-2
-1
0
1
2
3
4
Species richness
35 R 2 = 0.10 30 p = 0.0024 25 20 15 10 5 0
35
R
2 = 0.10
30
p = 0.0024
25
20
15
10
5
0
-2
-1
0
1
23
4
Species abundance

Forest cover 200m buffer

Fig. 2 – Scatterplots of total species richness and total species abundance (a) with hedgerow age, and (b) with forest cover in a 200 m buffer. Species richness and abundance were normalized using a Box–Cox transformation. Hedgerow age and forest cover were standardized. N = 88 hedgerows used in the landscape models.

to a more uniform environment such as forest herbs, habitat suitability is likely improved in wider hedgerows by the pres- ence of a core area characterized by more buffered, temperate habitat conditions, at least at the scale at which forest herbs perceive their environment. In fact, more forest herbs oc- curred in the center of hedgerows than at the edge (unpub- lished). In addition, given that some forest herbs in our species pool are animal-dispersed, hedgerow width could indirectly affect plant populations by influencing animal use of the linear network. In Sweden, Sarlo¨ v Herlin and Fry (2000) demonstrated that the number of animal-dispersed woody species increased more significantly with hedgerow width than the number of wind-dispersed species. By provid- ing more resources and less exposure to predators, wide hedgerows generally favour the presence of birds ( Hinsley and Bellamy, 2000) and possibly of small mammals. Within hedgerows, the abundance of forest herbs may be limited by competition from shrubs and ruderal species that benefit from increased disturbances related to more intense field management. In another hedgerow system of a similar landscape, it was found that, independent of hedgerow age, competitive ruderal species were more likely to colonize nar- row hedgerows adjacent to the more intensively managed fields, whereas the probability of finding forest herbs in hedgerows increased as the intensity of adjacent agricultural practices (from intensive crop to fallow land) decreased (de Blois et al., 2002a). The microclimatic conditions of hedge- rows generally characterized by increased light penetration, increased air and soil temperature fluctuations, decreased air humidity and an increased level of agronutrients in the soil give a competitive advantage to ruderal herbaceous spe-

cies and invasive shrub species over shade-tolerant forest interior species ( Honnay et al., 2005; Roy and de Blois, 2006). Forest herbs in some hedgerows are subjected to levels of shrub competition not experienced in forest patches. A dense shrub cover can change the seasonal patterns of light avail- ability and affect understory herbs that depend on the period before canopy expansion for much of their annual carbon gain ( Miller and Gorchov, 2004). The resulting reduction in growth and fecundity can suppress the long-term reproduc- tive success of herbaceous species and consequently reduce population growth rate.

5.

Conclusion

The potential for hedgerows to support relatively diverse na- tive forest herb communities increases with time and the maintenance of a forest cover in the adjacent landscape, and to a lesser extent, with connections to other hedgerows. Management practices that lead to wider hedgerows with re- duced competition from other species, by minimizing, for in- stance, disturbances from field maintenance, are expected to result in an increase in the richness and abundance of forest herbs within linear habitats. A direct link to a forest patch does not appear to influence forest herbs in this system, but it may possibly affect which species will be able to colonize. The fact that forest herb communities, or at least a subset of the regional pool, can reassemble in hedgerows with time implies that there could be long-term benefits in maintaining and creating linear habitats where there is a pool of dispers- ing forest herb propagules. A structurally diverse hedgerow flora can also have a positive effect on the diversity of other

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taxa ( Jobin et al., 2001). Most hedgerows, however, are subject to disturbances from agricultural management practices and even species that have managed to colonize and establish small populations can be extirpated. With inappropriate management, hedgerows may act more as sinks than as valu- able biodiversity conservation units, but the conflict between the legitimate need to maintain weed and pest-free agricul- tural fields and the urgency to conserve native species where they are most threatened is not easily resolved. We believe that hedgerows can contribute, at least for a subset of species, to extend forest conditions into the agricultural matrix, possi- bly mitigating in part the impacts of habitat loss and frag- mentation on dispersing species with minimal effect on crop yield. Based on our results, we should at the very least aim to conserve the remaining species-rich hedgerows and facilitate, whenever conditions allow, the emergence of new linear structures that will have the potential to sustain the dispersal of native plants in the long-term.

Acknowledgments

This research was supported by an FQRNT scholarship to V.R. and NSERC and FQRNT grants to S.d.B. We are grateful to J. Snider, M. Bourgon-Desroches and V. Paul for their assistance in the field and to R. Schmucki for help with statistical anal- ysis. We wish to thank E. Bennett, M. Vellend, M. Waterway and three anonymous reviewers for commenting on an ear- lier draft of this manuscript.

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