Effects of the type of montane forest edge on oak seedling establishment along forest–edge–exterior gradients

Effects of the type of montane forest edge on oak seedling establishment along forest–edge–exterior gradients

Forest Ecology and Management 225 (2006) 234–244 www.elsevier.com/locate/foreco Effects of the type of montane forest edge on oak seedling establishm...

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Forest Ecology and Management 225 (2006) 234–244 www.elsevier.com/locate/foreco

Effects of the type of montane forest edge on oak seedling establishment along forest–edge–exterior gradients Fabiola Lo´pez-Barrera a,b,*, Robert H. Manson b, Mario Gonza´lez-Espinosa c, Adrian C. Newton d a

School of GeoSciences, Institute of Environmental and Atmospheric Sciences, University of Edinburgh, Darwin Building, Mayfield Road, Edinburgh EH9 3JU, Scotland, United Kingdom b Departamento de Ecologı´a Funcional, Instituto de Ecologı´a, A.C. Km 2.5 Carretera Antigua a Coatepec No. 351, Congregacio´n El Haya, Xalapa, Veracruz 91070, Mexico c Divisio´n Conservacio´n de la Biodiversidad, El Colegio de la Frontera Sur, San Cristo´bal de las Casas 29290, Mexico d School of Conservation Sciences, Bournemouth University, Talbot Campus, Poole, Dorset BH12 5BB, United Kingdom Received 26 September 2005; received in revised form 28 December 2005; accepted 29 December 2005

Abstract Recent studies have highlighted the importance of different edge types in the modulation of edge-related responses associated with habitat fragmentation. Hard (high contrast with pastures) and soft (low contrast with old-fields) forest edges created by slash-and-burn agriculture have become common landscape features in regions dominated by Neotropical montane forest. The growth and survival of seedlings of five oak species (Quercus candicans, Quercus crassifolia, Quercus laurina, Quercus rugosa and Quercus segoviensis) was monitored experimentally by introducing seedlings across replicates of the forest–edge–exterior gradients (24, 12, 0, 12 and 24 m) typical for these two edge types (hard and soft) in the Chiapas Highlands, Mexico. Seedling survival and growth (measured in terms of basal area, new stem and leaf production, and defoliation) was generally greater in adjacent open habitats than in the forested portion of the gradient. However, seedling performance was optimal 12 m from the soft edges in the open habitat. Overall, Q. crassifolia had the lowest seedling survival, especially in the forested portion of hard forest edges, whereas Q. rugosa showed the highest growth rates and survival. This study shows that the edge effects detected along a forest–edge– exterior habitat gradient may depend in large part on the type of edge being studied. The implications of these results are discussed with respect to the influence of edge characteristics on forest patch dynamics in fragmented tropical montane landscapes. # 2006 Elsevier B.V. All rights reserved. Keywords: Quercus; Forest succession; Seedling survival and growth; Herbivory; Edge effects; Edge contrast; Tropical montane forest

1. Introduction One of the most obvious consequences of forest fragmentation is the creation of habitat edges. Forest edges may exert a significant control over forest regeneration processes, owing to spatial and temporal changes in microclimate (WilliamsLinera, 1990; Chen et al., 1995; Williams-Linera et al., 1998), abundance of seed dispersers and or predators (Manson et al., 1999; Molnar et al., 2001) and herbivores (Meiners et al., 2000; Manson et al., 2001). However, these edge-related responses and their consequences for plant community composition could

* Corresponding author. Tel.: +52 228 842 1800x4202; fax: +52 228 818 7809. E-mail address: [email protected] (F. Lo´pez-Barrera). 0378-1127/$ – see front matter # 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2005.12.055

be ameliorated or exacerbated as a result of the differences in edge type, which is determined by the type of vegetation adjoining forest fragments (Didham and Lawton, 1999; Mesquita et al., 1999) and the age of the forest edge itself (Gascon et al., 2000). Although there are numerous studies of edge effects in forest fragments (see review in Murcia, 1995; Sarlov-Herlin, 2001), recently it has been argued that ecologists should specify the type of edge studied. For example, hard edges (high contrast between fragments and adjacent matrix habitat) and soft edges (low contrast) may have different structural and therefore functional characteristics (Laurance et al., 2001; Strayer et al., 2003; Cadenasso et al., 2004; Ries et al., 2004). Understanding how the structure and configuration of edges alters the dynamics and persistence of spatial forest mosaics is important for understanding successional

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processes in fragmented forest landscapes, such as dispersal and colonisation (Strayer et al., 2003; Cadenasso et al., 2004). For example, Cadenasso and Pickett (2000, 2001) showed that seedling herbivory by voles and wind dispersal of seeds changed with manipulations of the vegetation structure of edges. Similarly, previous research in the Highlands of Chiapas documented that acorn removal and dispersal by small mammals varied between sites with hard and soft edges (Lo´pez-Barrera, 2003; Lo´pez-Barrera et al., 2005). Although most studies of forest fragments have found changes in the density and composition of tree seedlings along gradients from edges to the forest interior (Chen et al., 1992; Benitez-Malvido, 1998; Goldblum and Beatty, 1999), tree seedling performance (defined in terms of growth and survival) along these complex micro-environmental gradients is relatively unexplored (but see Meiners et al., 2000; Asbjornsen et al., 2004). Understanding of the effect of different edge types on tree seedling establishment is even more limited (Cadenasso and Pickett, 2000, 2001). Neotropical Montane forests in the Chiapas Highlands, as in many other mountainous regions of Latin America, have become increasingly fragmented due to land use change (Ochoa-Gaona and Gonzalez-Espinosa, 2000) and the anthropogenic degradation of remaining forest fragments (Ramirez-Marcial et al., 2001). Due to slash-and-burn agriculture, these forested areas are often bordered by a range of modified habitats producing different edge types within a forest mosaic. Forests bordered by open pastures result in abrupt boundary or hard edges and are characterised by extended gradients along which microclimate can change dramatically (Gascon et al., 2000). In contrast, the successional vegetation that characterises forests borders abutting abandoned pastures or fallows may intercept lateral light and wind near the edge, resulting in shaded or soft edge effects with little penetration into adjacent forests. These edges may thus act as a buffer that protects the forest interior from strong microclimatic fluctuations (Gascon et al., 2000). Insect and small mammal community composition and abundance may also respond to variations in microclimate along forest–edge– exterior gradients (Didham et al., 1996; Manson et al., 1999, 2001) and between edge types, resulting in different patterns of seed predation, seedling herbivory and tree seedling establishment (Ostfeld et al., 1997; Meiners et al., 2000; Meiners and Martinkovic, 2002). Understanding the role of different types of forest edges in determining patterns of tree establishment is critical to predicting forest regeneration and community composition in landscapes subject to intensive human use such as those of Chiapas, Mexico. Recent literature reviews of edge effects by Ries et al. (2004) and Harper et al. (2005) have concluded that, although edge contrast or abruptness is a main factor affecting the magnitude and direction of edge effects, there are few rigorous comparisons between edge types. Studies testing mechanistic hypothesis and defining variables to describe edge contrast are thus urgently needed. To our knowledge no study to date has experimentally evaluated the effect of different edge contrasts (hard versus soft) on tree

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seedling performance along a range of anthropogenically induced forest edges. This study addresses this concern as part of a broader research project examining how edge structure affects oak regeneration processes along forest edges and the resulting implications for oak expansion into open areas (Lo´pez-Barrera, 2003; Lo´pez-Barrera et al., 2005; Lo´pez-Barrera and Newton, 2005). Here we report species-specific patterns of seedling performance of five different oak species placed along the habitat gradient generated by hard or soft forest edges. The specific predictions we sought to test were: (a) that oak seedling performance is significantly greater at intermediate conditions of light and humidity (as forest edges and in open habitats with shrub cover) and (b) that seedling predation will vary across forest interior–edge–grassland gradients (Cadenasso and Pickett, 2000; Wada et al., 2000; Molnar et al., 2001; Wahungu et al., 2002). Specific hypotheses regarding the effects of hard and soft edges were that seedling survival and growth should covary with the abrupt changes expected in environmental variables such as light and humidity moving across hard edges, whereas such changes should be less pronounced moving along soft edges. 2. Methods 2.1. Study area The study area was located in the Highlands of Chiapas (1500–2700 m), in southern Mexico. The dominant vegetation consists of patches of diverse secondary plant communities associated with pine-oak forests, interspersed with pastures, agriculture and, on higher slopes, neotropical montane cloud forest (Gonzalez-Espinosa et al., 1991). Climate is temperate sub-humid (mean annual temperatures are 13–17 8C), with a summer rainfall regime (annual rainfall is 1100–1600 mm; >85% occurring from May to October) and occasional severe winter frosts in open areas at high elevations (>2200 m). The most common soils are darkbrown, shallow to moderately deep (30–100 cm) clays and clayey loams (Parra-Va´zquez, 1989). 2.2. Experimental plots The study was conducted in Rancho Merced Bazom (2020– 2560 m) located in the Huistan municipality some 20 km east of San Cristo´bal de Las Casas. Ranch land (approximately 22 ha) is individually owned by the families of three Tzotzil farmers. Dominant oak species in the canopy include Quercus laurina, Quercus crassifolia and Quercus rugosa, detailed information about forest structure and composition in this study site is presented in Gonzalez-Espinosa et al. (1991). Logging and agricultural activities have produced a mosaic of openings ranging from 0.5 to 2 ha and exhibiting varying stages of regeneration within the forest matrix. During an initial visit in May 2000, six representative study sites were chosen within this ranch based on the form (40 m of straight edge) and type of forest edge present (hard

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Table 1 Description of six edges studied in the Highlands of Chiapas, Mexico Edge

Altitude (m)

Latitude N

Longitude W

Aspect of forest edge

Slope (8)

Open area size (m2)

Edge age (years)

Edge tree height (m)

Forest tree height (m)

Forest disturbance

1 2 3 4 5 6

2410 2370 2380 2468 2440 2400

168440 23.200 168440 26.700 168440 25.700 168440 25.700 168440 37.000 168440 15.000

928290 12.300 928290 35.800 928290 24.200 928290 29.900 928290 26.300 928290 15.600

E W NE S E SW

38 19 11 16 45 16

800 1601 1128 3352 4448 1769

>60 34 >30 51 >60 >30

30.1  6.7 18.8  3.9 25.5  8.1 17.6  2.6 21.3  2.1 27.9  0.7

19.0  2.5 27.7  3.9 25.1  2.5 22.0  2.7 22.3  3.6 18.6  1.4

Low High Medium Medium High High

(soft) (soft) (soft) (hard) (hard) (hard)

Patch position and size were calculated using a GPS. Slope was calculated in the open area adjacent to the forest patch. Edge age was determined by interviews with site owners. Forest disturbance was estimated using a categorical index (Lo´pez-Barrera, 2003). Tree height (mean  1S.E.) was calculated in each site from five randomly chosen trees along the forest edge and five in the forest interior (40 m from the edge).

versus soft; n = 3 per treatment), as well as our ability to obtain the permission of the owners for field research (Table 1; Lo´pez-Barrera et al., 2005; Lo´pez-Barrera and Newton, 2005). Data on vegetation structure, composition and the degree of human disturbance in each of the study sites are reported in Lo´pez-Barrera (2003). A rectangular experimental plot (20 m  60 m) was established in each site (35 m from the forest edge into the forest interior and 25 m from the edge into adjacent disturbed habitat) and surrounded by a 2 m fence composed of steel wire mesh (mesh openings of 4.5 cm) to exclude livestock and large- to intermediate-sized mammals. Experimental plots were located on the sides of clearings with the straightest edges and the largest expanse of continuous forest. Pastures within the plots of sites with hard edges were trimmed by machete at regular intervals (6 weeks on average but more frequently during the rainy season) to mimic the height of herbaceous vegetation (5–10 cm) typical for grazed areas. The mean distance between study sites was 588  276 m (S.D.). 2.3. Experimental seedling production From September 2000 to November 2000 acorns of five Quercus species (all evergreen trees, except Quercus segoviensis which is semi-deciduous) were collected in four different sites around the study area: Merced Bazom (Q. laurina Humb. and Bonpl. and Q. crassifolia Humb. and Bonpl.), Moxviquil (Q. segoviensis Liebm.), Mitziton (Q. rugosa Ne´e) and Huitepec (Quercus candicans Ne´e). After collection, an equal number of acorns from each parent source were mixed together for each species. Acorn viability and damage was tested by water floation (Gribko and Jones, 1995). Following this protocol, only sinking acorns were deemed viable and used for experimental seedling production. Before sowing, acorns were soaked in water for 24 h to enhance acorn hydration. Acorns of different species were separated in rectangular polystyrene containers (47 cm  30 cm) filled with mineral soil (10 cm deep layer) and covered with approximate 3 cm of pine and oak litter to increase germination rates (Lo´pez-Barrera and GonzalezEspinosa, 2001). Germination usually occurs immediately in the case of Q. crassifolia, Q. segoviensis and Q. rugosa, while acorns of Q. candicans and Q. laurina remain dormant until

the start of winter rains in January–February (Lo´pez-Barrera and Newton, 2005). Shoot emergence began in November for Q. crassifolia and Q. segoviensis and late December for Q. rugosa, Q. laurina and Q. candicans shoots appeared in late January. After seedling emergence, oak seedlings were individually transplanted into black plastic bags containing mineral soil (1966 cm3). All mineral soil and leaf litter used in the nursery was collected from the same location within the forest in Merced Bazom. Seedlings were grown in a greenhouse for 6 months prior to transplanting into experimental plots. The nursery was located at El Colegio de La Frontera Sur, in San Cristobal de Las Casas, Chiapas (2100 m altitude, 13–14 8C mean annual temperature and 1160 mm mean annual rainfall). Seedlings were watered every third day and used in experiments only if they showed no signs of disease or desiccation. Seedlings within each species were selected to be as similar as possible in height, number of leaves and vigour. Plants with losses of some leaf area owing to attack by insects could not be avoided for certain species (e.g. Q. rugosa and Q. segoviensis) and this damage was quantified at the beginning of field experiments. 2.4. Experimental design Seedlings of five oak species (Q. candicans, Q. crassifolia, Q. laurina, Q. rugosa and Q. segoviensis) were transplanted at two types of forest edge (hard and soft). We defined the forest edge as starting at the base of the first trunks of mature trees encountered moving into the forest (Jose et al., 1996; Oosterhoorn and Kappelle, 2000). In each of the six sites (three sites of each edge type), transects were established running parallel to the edge at 12 m intervals from the forest into adjacent open areas (specific distances along the forest– edge–exterior gradient: 24, 12, 0, 12 and 24 m). This design enabled us to study the forest–edge–exterior gradient while controlling for the spatial dependence of potential seedling predators as small mammals. Ten seedlings per species (nine seedlings in the case of Q. candicans) were planted in a random order along each transect at 0.8 m intervals using holes dug by trowels to a depth of approximately 20 cm. Transplantation of seedlings was completed in 1 day (9 July 2001) with each of the 1470 seedlings identified using numbered plastic tags attached to the stem by a loose wire thread at ground level.

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After being transplanted, the seedlings were monitored at 2month intervals for 11 months. However, in February 2004 (34 months after the start of the experiment) seedling survival was checked again. Seedling height, basal diameter, number of leaves, number of damaged leaves and a categorical value for insect damage were recorded for each seedling during each revision. Each seedling was scored as undamaged, damaged by herbivores, mechanically damaged or dead from other causes. As each herbivore damages seedlings in a unique way, we could score the damage generated by specific herbivores. Small mammals clip seedling stems approximately 2–4 cm above the soil surface while invertebrate damage consists mostly of defoliation or root damage. Percentage of defoliation was assessed categorically (0: no defoliation, 1: low, 2: medium and 3: high). Leaf area loss was estimated visually as a fraction of extrapolated extent of original leaf area. Soil moisture and PAR were also measured every 2 months. Soil moisture (percent of fresh weight) was estimated for two cylindrical samples (18 cm3) collected randomly along each transect at a depth of 4 cm within mineral soil. Photosynthetically active radiation (PAR, mmol m2 s1) was measured using a ceptometer (Sunfleck Decagon Pullman, Washington, USA). Four measurements (average of 30 readings) taken at 5 m intervals along each transect at the top of the plants were averaged to provide one value per transect. 2.5. Microsite characterization To characterise the microsite where the seedling were planted at each distance from the forest edge, ground vegetation cover and the shrub stratum were measured prior to planting using the line-intercept method (Mueller-Dombois and Ellenberg, 1974). We noted the species and degree of crown overlap with a line delineated by a meter tape (strung 15–20 cm above the ground). The accumulated length occupied by any one species out of the total length of the meter tape was used to calculate the percentage cover for that species. The same meter tape was also used to measure two separate layers of understory vegetation including: (1) prostrate herbs (<15 cm) and (2) tall herbs, shrubs or tree saplings (>15 and <50 cm); the height of this last layer was also measured for each species.

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the initial number of leaves as a covariate), difference in the proportion of seedlings with defoliation, RGR of basal area, RGR of stem height and difference in stem height/diameter ratio. For this analysis, the measurement unit used was the average of 10 seedlings (nine seedlings in the case of Q. candicans) at each distance from the edge. Seedlings considered dead at the end of the experiment were excluded from the growth analyses. Variation in the degree of defoliation had two components: the proportion of leaves damaged and a categorical value (1–3) of lost leaf area. A relative index of leaf damage was calculated, by first transforming the proportion of leaves damaged into a categorical variable with four levels (1–4), then adding both categorical values together to provide an overall index. The difference between the initial and final status of the seedlings was analysed using ANOVA (SPSS v.10.0.1) for all the experimental factors and their interactions. The number of seedlings that produced more than one stem during the study period was analysed with a Chi-square test for the association between edge type and distance from the edge and a separate analysis was used to test for the effects of species (Crosstabs procedure, SPSS v.10.0.1). Soil moisture (arcsine transformed), PAR reaching the soil surface (log10 transformed), total vegetation cover (arcsine transformed) and mean height of the prostrate vegetation layer (log10 transformed) in each transect were analysed using ANOVAs testing the effect of date of sampling (only for soil moisture and PAR), edge type and distance from the edge. Tukey’s HSD multiple comparisons were used to detect significant differences among treatment means (using SPSS v.10.0.1). Herbaceous and shrub species diversity were calculated in each transect P and study site using Shannon–Wiener’s diversity index (H =  ( pi)(ln pi)) and Evenness index (J = H/ln(S)), where S is the total number of species in the habitat. These indices were calculated using Species Diversity and Richness (PISCES v. 2.3). Significant differences in species diversity and evenness between distances from the edge and edge types were examined using single-factor ANOVAs. Negative distances indicate meters from the edge (distance 0) into adjacent open areas. In the text mean  1S.E. are reported unless otherwise stated.

2.6. Statistical analysis 3. Results Relative growth rates (RGR) were calculated using basal area (sum of the basal area of all the stems of each seedling) and stem height (considering only the tallest stem present for each seedling). RGR was calculated using the formula: R = (ln V2  ln V1)/(T2  T1), where R is the rate of increment and V1 and V2 are any growth variable at time 1 and time 2. T2 and T1 are the period of time (Harper, 1977). A full factorial ANOVA was used to test for the influence of edge type (hard and soft), distance from the edge (24, 12, 0, 12 and 24 m) and species (Q. candicans, Q. crassifolia, Q. laurina, Q. rugosa and Q. segoviensis). Response variables were the proportion of seedling survival (arcsine square root transformed), number of leaves (log10 transformed and using

3.1. Environmental variables along the forest–edge– exterior gradients There were no significant differences in soil moisture among edge types and distances from the edge (P > 0.05; Table 2). However, soil moisture varied with the sampling dates (F = 265.96; d.f. = 5, 120; P < 0.001), reaching the highest levels during July (45.23  0.28%) and gradually decreasing towards the lowest value recorded in March and May (8.84  0.49 and 10.37  1.04%, respectively). PAR was affected by the interaction between edge type and distance from the edge (F = 2.46; d.f. = 4, 120; P = 0.049). Changes in

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Table 2 Mean (1S.E.) of vegetation and environmental variables measured along transects running parallel to different edge types and moving from the adjacent open areas (negative distances) into the forest (positive distances) Hard

Soft

24 m

12 m

Dead wood (%) 0 0 Leaf litter (%) 0.4  0.3 0.2  0.1 Gramineous 39.1  17.0 36.6  15.3 species (%) Herbs (%) 60.4  17.0 62.2  14.9 Ferns and 0 0.5  0.5 epiphytes (%) Vines (%) 0 0 Shrubs and tree 0 0.5  0.5 saplings (%) Herbaceous 12.4  0.4 12.0  0.3 height (cm) Soil moisture 18.1  2.3 20.1  2.8 (%) PAR 614.8  125.2 533.0  135.3 (mmol m2 s1)

24 m

0m

12 m

24 m

0 73.2  9.8 1.5  1.5

0 3.3  3.3 77.5  5.2 71.1  8.4 0.9  0.9 0

12 m

2.9  2.9 0 29.5  14.0

4.0  3.2 3.7  0.7 3.6  2.2

0m

12 m

24 m

3.0  1.6 0.7  0.7 0.8  0.8 45.5  16.2 62.5  9.0 62.2  16.0 13.2  10.1 0 0.3  0.3

13.3  6.8 3.1  1.2

5.1  1.5 6.1  1.5

4.8  2.6 8.2  1.9

65.5  12.2 0

57.4  20.9 18.0  10.2 5.1  2.7 9.5  5.3 6.3  6.3 10.9  4.1 17.4  2.9 10.0  8.1

0.2  0.2 8.8  3.7

2.4  1.5 8.0  4.2

3.0  0.9 9.5  4.0

0 2.1  1.2

1.0  0.6 24.0  18.1

0.6  0.4 8.7  2.6

2.6  1.9 2.2  2.2 11.8  5.1 14.8  6.1

16.5  1.1

21.1  1.4 21.3  1.7

23.4  0.9

37.9  6.7

19.0  1.1

26.5  1.3 22.8  1.6

19.2  2.5

19.1  2.5 19.3  2.2

18.5  2.4

19.5  2.3

19.3  2.2

19.1  2.2 18.7  2.2

73.8  28.5 21.8  7.7 31.0  2.5 383.2  47.5 233.6  78.4 19.4  2.5

17.8  1.8 31.0  11.0

Edge type was either soft (sites 1–3) or hard (sites 4–6). Means of environmental variables were generated using five separate measures taken during experiments. See the text for a more detailed description of these variables.

light were more abrupt crossing the hard versus soft edges (Table 2). Total ground cover, in contrast, was only affected by distance from the edge (F = 25.17; d.f. = 4, 20; P < 0.001). Total species diversity did not change with distances from the edge and edge types (ANOVA, P > 0.05). Species evenness was affected by distance from the edge (F = 2.99; d.f. = 4, 20; P = 0.043), however none of the pairwise comparisons were significant (Tukey’s HSD, P > 0.05). 3.2. Seedling survival After 321 days (from July 2001 to May 2002), 14.3% of 1470 seedlings were recorded as dead. Seedling survivorship was affected by the edge type–distance interaction (Table 3;

Fig. 1, circles). In sites with soft edges, mortality was significantly greater at the edge and within the forest (0, 12 and 24 m) versus adjacent open areas (12 and 24 m). In sites with hard edges, seedling survival did not change with distance from the edge (ANOVA, P > 0.05). Mortality within the forest was mostly due to rot (25.3  5.3% of the total dead seedlings), apparently caused by pathogens or fungi (18.4  4.9%), root damage by herbivores (6.7  3.1%) or rodents (2.2  1.4%); for 47.3  3.2% of the seedlings, the cause of mortality was not determined. In hard edges the opposite trend was observed with greater mortality at 24 m into the open areas compared to the edge and forest interior. Mortality in the open areas adjacent to hard edges was mostly due to shoot desiccation (38.6  8.6%) or root damage by herbivores (13.4  5.6%), although for

Table 3 ANOVA of the influence of experimental factors Source of variation

d.f.

TSS SS

T D S TD TS DS TDS

1 4 4 4 4 16 16

0.558 0.831 2.350 1.602 0.165 2.328 0.701

Covariate Error

1 100

6.231

LN F

SS **

8.96 3.33* 9.43*** 6.43*** 0.66 ns 2.33** 0.70 ns

H/D F

0.058 4.4495 3.311 0.276 0.125 0.861 0.103

2.56 ns 49.02*** 36.11*** 3.00* 1.36 ns 2.35** 0.28 ns

0.379 2.271

16.55***

SS 2131.1 3334.5 2940.5 308.59 61.39 2400.3 1283.3 12615.4

RGRBA F

SS ***

16.89 6.61*** 5.83*** 0.61 ns 0.12 ns 1.19 ns 0.64 ns

0.010 0.120 0.027 0.012 0.004 0.019 0.011 0.131

RGRSH F

SS **

7.72 22.78*** 5.26*** 2.33 ns 0.75 ns 0.91 ns 0.51 ns

0.0029 0.0015 0.0070 0.0015 0.0000 0.0016 0.0018 0.0089

DS F ***

32.09 4.26** 19.80*** 4.33** 0.02 ns 1.17 ns 1.26 ns

SS

F

0.564 1.099 2.335 1.122 0.178 1.853 1.041

7.51** 3.65** 7.76*** 3.73** 0.59 ns 1.54 ns 0.86 ns 7.514

T: edge type (hard and soft), D: distance from the edge (24, 12, 0, 12 and 24 m), S: species (Q. candicans, Q. crassifolia, Q. laurina, Q. rugosa and Q. segoviensis) and their interactions on total seedling survival (TSS), leaf number (LN), difference in stem height/diameter ratio (H/D), relative growth rate of basal area (RGRBA) and maximum stem height (RGRSH), and the difference in the proportion of defoliated seedlings (DS). The covariate for LN was the initial number of leaves of the seedlings. ns: P > 0.05. * P  0.05. ** P  0.01. *** P  0.001.

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Fig. 1. Seedling survival (mean  1S.E., %) after 321 days (11 months) as a function of distance from the edge (negative distances indicate meters from the edge into the grassland) and edge type: hard (filled circles) and soft (open circles). Filled (hard edges) and open (soft edges) bars represent the survival 34 months after the set up of the experiment.

45.0  8.8% of the seedlings the cause of mortality was not determined. Stems clipped by rodents were more common in the secondary vegetation of soft edges than in hard edges (16.0% versus 7.1%). No evidence was found for frost heaving as a cause of seedling mortality in open areas. Comparing species-specific survival probabilities, there was a significant decrease in seedling survival recorded only for Q. crassifolia in forests compared to open areas after 11 months of observation. This change was mostly due to rot (44% of seedlings) with remaining seedling death in the forest plots due to wilting with no apparent mechanical or pathogenic damage. After 34 months this interaction was no longer significant (P > 0.05) and all the species showed the same pattern initially presented by Q. crassifolia. There were however significant differences between species (F = 7.31; d.f. = 4, 100; P < 0.001) with Q. crassifolia survival being the lowest (44.34  6.71%), followed by Q. segoviensis (63.71  5.34%), Q. candicans (64.35  4.82%), Q. laurina (70.48  3.91%) and Q. rugosa (72.84  4.25%). By 34 months (July 2001–February 2004) seedling mortality increased to 36.8% and was still affected by edge  distance interactions (F = 3.60; d.f. = 4, 100; P = 0.009), however patterns were somewhat different than those recorded after 11 months. In sites with hard edges there was greater seedling survival at the edge (0 m) and 12 m from the edge into the exterior compared to the forest (12 and 24 m into the forest), whereas in sites with soft edges there was a gradual decrease in seedling survival moving from the exterior into the forest (Fig. 1, bars). 3.3. Effects of edge and distance on growth By the end of the study period the relative height growth rate of surviving seedlings had changed significantly with distance from the edge but only in sites with soft edges (Table 3). Seedlings planted at 12 m from the edge into the open areas

Fig. 2. Effect of edge type (hard: shaded bars vs. soft: open bars) and distance from the edge (negative distances indicate meters from the edge into the grassland) on: (A) RGR of stem height, (B) the difference in leaf number during the study period and (C) the proportion of seedlings showing any level of defoliation at the end of the experiment. Values are mean  1S.E.

adjacent to soft edges had higher increments in maximum stem height than seedlings planted at the edge (Fig. 2A). This seedling response coincides with areas of higher cover by shrubs and tree saplings (F = 4.93; d.f. = 4, 20; P = 0.006; Table 2), and taller herbaceous vegetation (Table 2). Basal area relative growth rates were significantly affected by the main experimental factors: edge type and distance from the edge (Table 3). Seedlings basal area increased faster in sites with hard (0.063  0.006 mm2 mm2 month1) versus sites with soft edges (0.047  0.005 mm2 mm2 month1). Seedlings planted in open areas (24 and 12 m) accumulated more basal area (0.082  0.008 and 0.093  0.008, respectively) than seedlings growing along the edge (0.047  0.008) or the forest interior (12 and 24 m; 0.027  0.006 and 0.024  0.006, respectively). The interactions between these factors was marginally non-significant (P = 0.061). At the end of the 11-month study period the number of seedlings that produced new stems varied in relation to the edge  distance interaction (x2 = 7.99; d.f. = 3; P = 0.046). Seedlings planted in the grasslands (24 and 12 m) of hard edges produced more stems (17 and 16 multi-stemmed seedlings, respectively) than those along the edge (two multi-stemmed seedlings). In sites with soft edges, 14 seedlings planted 24 m into adjacent open areas produced more than one stem, however only 4 seedlings did so at 12 m from the forest

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edge. Seedlings generally did not produce more stems within forest interiors (only 2 cases recorded) but rather 69 seedlings (from this 53 were Q. crassifolia seedlings) suffered a reduction of the number of stems possessed at the start of experiments (x2 = 20.79; d.f. = 4; P < 0.001). Differences in leaf number were related to the interaction between edge type and distance (Table 3) being more pronounced in sites with hard edges. Leaf number for seedlings planted in open areas increased, whereas leaf number of seedling planted within the forest decreased (Fig. 2B). Herbivore damage to seedlings was significantly affected by the edge type  distance interaction (Table 3). Fig. 2C shows the final pattern of seedlings defoliation where more seedlings were defoliated at the edge and 12 m into adjacent grasslands compared with the other distances. This pattern was only significant for sites with hard edges (ANOVA, P > 0.05). Seedling defoliation intensity, as determined by the leaf damage index, was affected only by distance from the forest edge (F = 8.76; d.f. = 4, 100; P < 0.001). Seedlings planted in the edge and forest suffered significantly more defoliation than those seedlings planted in open areas whose level of damage actually decreased during the experiment (due to lower damage to new leaves and/or the abscission of damaged leaves; Fig. 3). Significant changes were detected in the height/diameter ratio of seedlings as a function of edge type and distance from the edge (Table 3). Seedlings growing along edges showed smaller changes in height/diameter ratios irrespective of edge

Fig. 3. Difference in the (A) leaf damage index and (B) seedling height/ diameter ratio at the end of the experiment as a function of distance from the edge (negative distances indicate meters from the edge into the grassland). Values are mean  1S.E. Different letters indicate significant differences as determined by Tukey’s HSD comparisons (P < 0.05).

Fig. 4. Relationship between the mean seedling height/diameter ratio at the end of the experiment and the mean photosynthetically active radiation (PAR, mmol m2 s1). Circles and the dashed regression line represent data from sites with soft edges (y = 0.0206x + 57.37, R2 = 0.49). Triangles and the solid regression line (y = 0.0179x + 53.377, R2 = 0.67) represent data from sites with hard edges.

type (Fig. 3B). A regression analysis showed that the stem height/diameter ratio was negatively correlated with light (PAR; Fig. 4). Seedlings along soft edges (2.3  1.4) and within the forest interior (Fig. 4) favored increases in stem height versus diameter, whereas along hard edges (5.3  1.5) and in open areas (Fig. 4) seedlings appeared to have the opposite energy investment strategy. 3.4. Differences between species in seedling growth Quercus species showed significantly different relative growth rates for stem height (Table 3); Q. rugosa growth rates (cm cm1 month1) (0.039  0.002) were significantly higher than Q. candicans (0.023  0.002), Q. laurina (0.022  0.002), Q. segoviensis (0.023  0.002) or Q. crassifolia (0.019  0.002). Relative growth rates calculated using basal area also varied significantly among species (Table 3). Increased in basal area (mm2 mm2 month1) were significantly higher for Q. rugosa (0.071  0.009) and Q. laurina (0.069  0.007) as compared to Q. segoviensis (0.036  0.008). Q. candicans (0.054  0.007) and Q. crassifolia (0.044  0.010) exhibited intermediate values. Finally, while significant differences were observed between species in terms of changes in stem height/diameter ratio during the experiment (Table 3), this pattern was due to Q. laurina showing higher stem/diameter ratios relative to the other species at the beginning (59.3  1.4) but not end (50.8  1.6) of experimentation. Species-specific patterns of defoliation intensity (leaf damage index) were significantly different (F = 6.65; d.f. = 4, 100; P < 0.001). Both Q. segoviensis and Q. crassifolia seedlings exhibited significant increases in the degree of leaf damage during the experiment. While damage to the leaves of Q. candicans and Q. rugosa seedlings actually decreased during the same time period. A different pattern was noted when contrasting the proportion of defoliated seedlings between species (Table 3). Q. laurina and Q. rugosa (0.81  0.03 and 0.80  0.02, respectively) had a significantly higher proportion of defoliated seedlings as compared to Q. candicans (0.65  0.04), Q. crassifolia (0.47  0.04) and Q. segoviensis (0.52  0.03).

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Significant differences were also observed between species (x2 = 12.71; d.f. = 3; P = 0.005) in new stem production; Q. crassifolia seedlings produced multiple stems (24 seedlings) significantly more often than the other species. Q. candicans seedlings never produced more than one stem. Differences in leaf number among species varied as a function of distance from the edge (Table 2). While leaf number fell for all species in the forested portion of the gradient, Q. laurina seedlings growing in open areas (24 and 12 m) showed increases in leaf number that were significantly greater (24.1  9.0 and 29.6  8.9 leaves, respectively) than other species. 4. Discussion 4.1. Effects of edge type and distance on seedling performance Our findings support the hypothesis that oak seedlings have higher seedling survival along forest edges versus interiors; however this was true only for hard edges. This type of edge exhibited light levels intermediate between the adjacent open areas and forest interiors, whereas the light conditions recorded in soft edges were more similar to those prevailing in forest interiors. Seedling performance in the non-forested portion of the gradient (12 and 24 m) was actually the highest observed (higher survival and stem growth rates), but only in sites with soft edges. The open habitat created by more robust herbaceous and woody secondary vegetation appeared to generate intermediate light conditions that favored seedling development. These findings are supported by other studies showing that partial shade can benefit oak regeneration in tropical montane oak forests (Quintana-Ascencio et al., 1992; Camacho-Cruz et al., 2000; Asbjornsen et al., 2004) and temperate forests (Meiners et al., 2000). Similarly, experiments conducted in greenhouses have shown that oak seedling growth is optimal under intermediate light levels: 56% for Q. petraea (Jarvis, 1964), 50% for Q. douglassi (Callaway, 1992), 68% for Q. ilex (Rey-Benayas, 1998) and 30% for Q. rubra (Phares, 1971). The cause of seedling mortality in forest interiors, while difficult to elucidate in most cases, was apparently due to the combination of several factors operating simultaneously. Interaction between factors such excessive moisture and fungal and insect attacks has been documented previously (QuintanaAscencio et al., 1992; Robin et al., 2001). Taken together, our results suggest that future studies exploring the effects of edges on forest regeneration and tree community composition should consider forest edge type as an important experimental variable for analysis. 4.2. Stem height/diameter ratio In this experiment, intermediate stem/diameter ratios were recorded along both edge types, suggesting that some seedling growth responses may have faced trade-offs along

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the edges we studied. Energy allocation for growth in height or diameter may represent one such trade-off since gaining height is important for competition with neighbours, but greater stem diameter is necessary to support stems both mechanically and physiologically (Sumida et al., 1997). Thadani and Ashton (1995) found that seedlings of Q. leucotrichophora growing in a Himalayan forest showed higher height/diameter ratios where canopy cover, and presumably competition, increased. Similar patterns (using PAR) were observed in this study, and suggest that oak seedling growth responses along the gradients created by forest edges are determined mainly by changes in light availability along such gradients. Contrary to our expectations that the abrupt change in microclimate associated with hard edges would be correlated with similar changes in seedling performance, increases in seedling height did not covary with light along this gradient. Instead, increases in the height of seedlings were low and fairly uniform moving from forests into adjacent open areas. A likely explanation for the reduced stem growth in the full sunlight conditions is that the favoured biomass allocation strategy was in root growth to compete successfully with herbs and grasses and to thus increase water absorbing capacity (Gardiner and Hodges, 1998; Asbjornsen et al., 2004). Significant differences may have been observed along this gradient if experiments had been conducted long enough to observe a shift from below ground to above ground investment in biomass. While no change in height was observed, seedlings planted in grasslands in sites with hard edges produced more new leaves than their counterparts in open areas adjacent to soft edges, perhaps to support increases in below ground biomass. Other studies have reported an increase in the number of leaves as canopy openness increases for Q. crispipilis (Quintana-Ascencio et al., 1992), Q. castanea and Q. acutifolia (Asbjornsen et al., 2004), Q. michauxii (Collins and Battaglia, 2002) and Q. leucotrichofora (Thadani and Ashton, 1995). 4.3. Seedling defoliation Seedlings growing in the forested portion of the gradient had higher defoliation intensity (amount of damage done to defoliated seedlings) versus those growing in adjacent open areas, irrespective of edge type. This pattern was apparently caused by increased herbivory by lepidopteran larvae and is similar to that observed by Humphrey and Swaine (1997) who found that Q. robur and Q. petraea seedlings were significantly more defoliated under closed versus open oak canopies or those dominated by Betula spp. Riley and Jones (2003) also showed that seedlings of Q. alba suffered more leaf herbivory in understorey plots than in adjacent clearcuts. The most likely explanation for the pattern of defoliation detected in this study is the small spatial scale in which oak-specific herbivores complete their life cycles. After emerging and feeding in the canopy, lepidopteran larvae feeding on oak canopies frequently fall and continue feeding on oak seedlings in the understory before pupation in

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the forest floor leaf litter (Humphrey and Swaine, 1997; Wada et al., 2000). Seedlings growing near conspecific adults are therefore more likely to exhibit greater defoliation than seedlings growing some distance from adult trees (e.g. Q. crispula; Wada et al., 2000). While the amount of damage done to defoliated seedlings increased moving into forests from exterior, the proportion of seedling suffering defoliation did not change significantly along this same gradient. Such differences in defoliation responses may have been an artefact of our sampling protocol. We examined only the difference between the initial and the final condition of seedlings but did not explore more subtle temporal trends. Seedling defoliation by lepidopteran larvae is known to be episodic, with larvae falling from canopies mainly during the spring (Wada et al., 2000), which might have resulted in higher initial defoliation intensities for seedlings planted in July which disappeared over time. Similarly, low leaf turnover for seedlings growing within the forest as compared with the seedlings growing in open areas resulted in higher leaf damage index for forest interior seedlings by the end of the experiment. By shedding damaged leaves at a faster rate, seedlings in open areas actually showed less intense defoliation damage at the end versus the start of experiments. Higher leaf damage in oak seedlings may also induce a higher leaf turnover in and of itself (Wadell et al., 2001) or less subsequent damage due to changes in the physical or chemical composition of leaves (Wold and Marquis, 1997). Further analysis of data from this experiment is thus warranted to detect temporal changes in the defoliation patterns. 4.4. Species-specific seedlings performance While a high number of oak species coexist in the region of study (about 18 species; Gonzalez-Espinosa et al., 1997), information is lacking on their regeneration requirements based on physiology and evolutionary adaptive strategies. Q. crassifolia demonstrated marked shade-intolerance and may also have problems acclimatizing to the change in light levels moving from the greenhouse (moderate) to forest (very low light), as has been reported for Q. robur (Welander and Ottosson, 1998). Both Q. laurina and Q. rugosa displayed relatively high overall seedling performance resulting from greater morphological plasticity that allowed them to thrive in both high and low light conditions. 4.5. Implications for oak regeneration and edge dynamics Taken together, our findings suggest that oak seedling performance is lower in the forest portion of the gradient than in adjacent open areas, with intermediate levels of performance observed only along the hard forest edges. Meiners et al. (2000) found that the probability of seedling establishment and the growth of Q. palustris in a temperate forest increased positively with distance from the forest edge into the old-fields. This response suggests that acorns moving greater distances from the oak canopy may result in seedlings with a higher

probability of establishment, thus highlighting the importance of dispersal for plant population dynamics and forest regeneration. The abandoned grasslands dominated by shrub patches and tall herbs along the soft edges in this study may provide particularly appropriate sites for oak regeneration. While oak seedlings appear capable of eventually colonizing open grasslands where large herbivores are suppressed, results of this and other studies in the region (Gonzalez-Espinosa et al., 1991, 1997; Quintana-Ascencio et al., 1992) suggest that the regeneration of oak forests could be accelerated in landscapes where mid-successional plant communities replace pastures or crops, thus facilitating small mammals movements and acorns dispersal into microsites favourable for acorn germination and growth (Lo´pez-Barrera, 2003; Lo´pez-Barrera and Newton, 2005). Further research on the later phases of seedling establishment and sapling performance in these sites is needed as there is evidence that competition for resources may become more important as seedlings age. The wide range of edge effects observed in this study suggest that the environmental gradient present along edges with different contrasts is not uniform and that oak recruitment appears to depend mainly on species-specific responses to variation in light availability. This study thus highlights the importance of experimental tests of the effects of different edge types (Ries et al., 2004) or patch contrast (Harper et al., 2005) and variability observed within sites and replicates suggest that these factors should be addressed more explicity in future studies. In order to develop a comprehensive theory of forest edge effects, future studies should identify the forest regeneration processes and mechanisms that are affected by edges, as well as the spatial and temporal scale at which they operate. Rigorous experimental testing of such complex models will facilitate predictions of the long-term impacts of fragmentation and other landscape-level changes on forest degradation and regeneration. Acknowledgements We would like to thank to C. Legg and N. Ramı´rez-Marcial, who offered relevant information and valuable comments during the research. We are extremely grateful to the many people who helped with the fieldwork, including: M. Martı´nezIco´, A. Luna-Go´mez, J. Bautista-Bolo´m, J.C. Bautista-Bolo´m, P. Giro´n-Herna´ndez and H. Castan˜eda-Ocan˜a. Many thanks to the owners of the study plots in Rancho Merced Bazom who provided access to the sites. El Colegio de la Frontera Sur (ECOSUR) provided the fieldwork and laboratory facilities. The Consejo Nacional de Ciencia y Tecnologı´a (CONACYT) and the British Council provided a graduate scholarship to F. Lo´pez-Barrera (ref. no. 131197 and MEX2900177, respectively). CONACYT also covered part of the research expenses. Additional financial support was provided by the European Commission under the INCO-DC programme (framework 4) as part of the SUCRE (ERBIC-18 CT 97-0146) and BIOCORES (PL ICA4-2000-10029) projects.

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