Biological Conservation 70 (1994) 129-134 © 1994 Elsevier Science Limited Printed in Great Britain. All rights reserved 0006-3207/94/$07.00 ELSEVIER INFLUENCE OF FOREST FRAGMENTATION ON SEED CONSUMPTION AND DISPERSAL OF SPANISH JUNIPER Juniperus thurifera Tomfis Santos & Jos6 L. Telleria Departamento de Biologia Animal I ( Zoologia). Facultad de Biologia, Universidad Complutense, 28040 Madrid, Spain (Received 26 June 1993; revised version received 10 January 1994; accepted 20 January 1994) Abstract consumers of seeds and fruits in these isolated habitats, We examined the effects of fragmentation on Spanish Telleria et al. (1991) showed that the density of winter- juniper Juniperus thurifera in central Spain by comparing ing mice in holm oak Quercus ilex woodlots increases as eight small forest fragments (SF: 0.2-16 ha) with two forest size decreases, and suggested that regeneration large forests (LF: 150 and 270 ha). Wood mice Apode- and long-term persistence of plant species whose mus sylvaticus, the only rodent seed eaters, were 8.9 propagules are consumed might be threatened within times more dense in SF, whereas thrushes Turdus spp., the fragments. the main avian seed dispersers, were 4.6 times more In this paper we analyse some effects of forest frag- abundant in LF. Finches (seed eaters) were scarce in mentation on the dispersal ecology of Spanish juniper both forest groups. Mean fruit abundance was signifi- Juniperus thurifera in an area of central Spain. In this cantly higher in LF. Seed consumption was mainly by area, Spanish juniper is a scarce tree species in forests mice in SF and by finches in LF. Thrush pellets with dominated by holm oaks and is the only fruit-produc- intact seeds, seedling abundance and the proportion of ing tree whose seeds are dispersed by wintering birds. trees with nearby seedlings, were all higher in LF. This Its persistence is therefore likely to be influenced by the evidence points to a decrease in the dispersal efficiency of increased numbers of mice and by the potential Spanish juniper in SF. We suggest that the processes changes in the abundance or behaviour of their disper- leading to reduced dispersal ability might be inherent to sal agents. Within this context, we hypothesized two fragmentation and represent a threat for the survival of negative effects of fragmentation on the dispersal of fruit-bearing plants in patchy environments. Spanish juniper: (1) an increase of fruit and seed con- sumption by rodents and a decrease of fruit consump- Keywords: fragmentation, Spain, Spanish juniper, Ju- tion by frugivorous birds; (2) a decrease in seedling niperus thurifera, thrushes, wood mice. recruitment, as a result of the reduced seed dispersal. INTRODUCTION STUDY AREA Habitat fragmentation occupies a central place in con- The study was carried out in Lerma (central Spain: servation biology (Soul6, 1986). The responses of species 42°5'N, 3°45'W) during winter 1989-90. Average to fragmentation are highly variable, depending on the altitude is 850 m and climatic conditions are inland species characteristics and on the particular pattern of mediterranean, with long, cold winters (Font, 1983). fragmentation involved. Plant persistence, for example, The region is covered by ploughed agricultural land- can be affected through a direct response to habitat re- scape, where small woodlots are isolated remnants of duction (Dzwonko & Loster, 1989), but it may also be the original forest. Sampling was carried out in two negatively affected by interspecific interactions, namely sets of forests. A first set of eight small forests (SF 1-8, by population changes of animal species that act as dis- 0.2, 0.3, 0.6, 1.2, 1.3, 2.0, 12 and 16 ha, respectively) persers, seed eaters or browsers, or by bringing seeds was sampled in an area (Santa Cecilia) with numerous from surrounding habitats (Janzen, 1983, 1986). small woodlots embedded in a matrix of crop fields. In the agricultural landscapes of central Spain, is- Distances between SF ranged from 100 m to 1-3 km lands of stable habitats (such as shelterbelts, forest and shapes were either square (two fragments) or rect- fragments and shrubland patches) surrounded by angular (six fragments). We also studied two large agricultural matrices usually support high densities of forests (LF1, 150 ha and LF2, 270 ha) in Quintanilla wintering wood mice Apodemus sylvaticus (Alcfintara, del Agua, about 15 km from Santa Cecilia; these 1986; Diaz, 1992). Mice are omnivorous and highly effi- allowed us to sample dispersal and predation patterns cient food searchers (Hansson, 1985; Santos & Telleria, indicative of the 'natural' situation previous to frag- 1991), hence they are expected to act destructively as mentation and could thus be considered as controls. 129 130 Tom6s Santos, Josk L. Telleria LF1 and LF2 were 2 km apart and moderately rectan- fruit abundance per tree gular in shape. 21 Firewood extraction is fairly intense throughout the study area, but our observations show that this does 18 not selectively affect the density or size structure of the tree stratum in the forests studied. Seedlings are very 15 vulnerable to grazing (Ceballos & Ruiz, 1979) but sts sheep and rabbits Oryctolagus cuniculus were rarely 12 recorded in these woods. Fire damage from stubble burning, however, is a potential disturbance. 9 Tree composition in the forests is dominated by small forests I ~ holm oaks (27.3-31.3% cover in LF and 20-87% in SF; 6 mean 33.4%), Spanish juniper being a minor species (3-5.8% cover in LF and 0.3-7.5% in SF; mean 2.7%). 3 The shrub layer is mainly formed by species of the gen- era Cistus, Genista, Thymus and Lavandula. Sparse 0 grasses grow in these woodlots, mostly in cleared areas. danusry February early-March mid-March late-March Fig. 1. Temporal changes in the mean abundance (and stan- BIOLOGY OF SPANISH JUNIPER dard deviation) of juniper fruits in Lerma. Fruit abundance is the average of the mean number of fruits per tree obtained The Spanish juniper, a monoecius, long-lived tree in eight small and two large forests. around 4-5 m tall, is a Tertiary relict which is dis- tributed throughout the western Mediterranean Basin, with its main quarters in the central Spanish highlands small size of these woodlots allowed us to census their total area by walking straight through them. The total (Ceballos & Ruiz, 1979). The genus Juniperus has ani- mal-dispersed fleshy cones (hereafter called fruits) (Her- area surveyed was 92 ha in LF and 32.2 ha in SF. rera, 1987; Snow & Snow, 1988). The main dispersers in Europe are small and medium-sized passerines (e.g. Fruit abundance and seed consumption We sampled fruits and seeds under the canopy of indi- robin Erithacus rubecula and thrushes Turdus spp.) vidual junipers in each forest. For each of four 15 x 15 (Herrera, 1981a,b; Debussche & Isenmann, 1985a, b,c; cm random plots beneath each tree (total area 0.09 m2), Snow & Snow, 1988). Rodents are well-known con- we recorded (a) the number of fresh fruits; (b) the num- sumers of both fruits and seeds (Gilbert, 1980; Holthui- ber of intact, undamaged seeds; (c) the number of seeds jzen & Sharik, 1985). damaged by rodents and (d) the number of seeds con- Germination rate of Spanish juniper is low, and regen- sumed by birds; (c) and (d) were added for each tree, eration and growth very slow (Ceballos & Ruiz, 1979). It thus providing a total seed consumption estimate. The flowers in spring and ripe fruits are available during the four plots were pooled into a single sample per tree. autumn-winter period of the following year (Ceballos & Undamaged seeds are left by both mice and birds. Ruiz, 1979). In late January 1990 we recorded the propor- Mice tend to eat mainly the outer pulp early in the tion of trees bearing ripe fruits in a sample from the two winter, leaving the seeds intact and then, in late winter, LF (181 trees) and all SF (214 trees) taken from both the they eat the seeds. Intact seeds are also left in thrush interior and edges of the forests. The means were almost pellets. Seeds consumed by birds and rodents were the same (45-9% and 45.8% in LF and SF respectively), readily distinguished, since mice obtain the seeds (en- although there was much greater variability among SF dosperm) by chewing the husk, while birds usually (15.4-73.7%) than in LF (44.2-48.5%). crack seed husks longitudinally in two halves. The number of half-husks found (attributed to birds) was METHODS Table 1. Densities (no. birds/10 ha) and numbers (in brackets) Rodent and bird abundance of avian frugivores and seed eaters in LF (92 ha censused) and Rodents were recorded in the previous winter (early SF (32.2 ha censused) March 1989) from snap-traps placed in all the woods Species Large forests Smallforests (for details see Telleria et al., 1991), and from tawny owl Strix aluco pellets that were collected and examined. Erithacus rubecula 4-0 (37) 1.2 (4) We studied wintering birds through December Turdus merula 2.8 (26) 2.2 (7) 1989-March 1990. All forests were censused twice, the Turdus iliacus 5-9 (54) -- two LF and the 12- and 16-ha SF stands by means of Turdus philomelos 16-8 (155) 3.1 (10) Turdus viscivorus 0.4 (4) -- the line-transect method (J~irvinen & V~iisanen, 1975), All frugivores 30.0 (276) 6.5 (21) using a 50-m main belt width. Untransformed main belt densities (number of birds/10 ha) were compared Fringilla coelebs 6.5 (60) 0-6 (2) Carduelis chloris O. 1 (1) -- with the densities obtained by searching for birds All seed eaters 6.6 (61) 0.6 (2) throughout the rest of SF.