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Width of grassland linkages for the conservation of butterflies in South African afforested areas
Biological Conservation 101 (2001) 85–96 www.elsevier.com/locate/biocon
Width of grassland linkages for the conservation of butterflies in South African afforested areas Sarah R. Pryke, Michael J. Samways * Invertebrate Conservation Research Centre, School of Botany and Zoology, University of Natal (Pietermaritzburg), Private Bag X01, Scottsville, 3209, South Africa Received 10 July 2000; received in revised form 14 November 2000; accepted 2 January 2001
Abstract Flight behaviours of 23 butterfly species were mapped to establish the effect of both pine afforestation and different-sized grassland linkages on localised butterfly movements. Blocks of pine trees caused most butterflies to change direction and move away from the pine edge. Only four species crossed the grassland/pine edge, and of these, only two flew farther than 20 m into the pine forest. The adjacent grassland/indigenous forest edge had a higher number of species, but very few of these entered the forest. Movement rates were significantly faster in the narrow and highly-disturbed linkages, than in the wide and open grasslands, with the linkages acting as conduits between the preferred grassland patches. However, only highly vagile and eurytopic species actually entered the narrower grassland linkages. In contrast, the wider linkages hosted a significantly higher species diversity and functioned as habitats per se and not just as movement corridors, with butterflies frequently stopping to nectar, oviposit, drink and sunbask. Knowledge of butterfly responses to different landscape structures has important conservation and management implications. From the results here, it is recommended that, for these butterflies, the natural grassland linkages should be wider than 250 m. # 2001 Elsevier Science Ltd. All rights reserved. Keywords: Lepidoptera; Habitat webs; Behaviour; Afforestation; Linkages
1. Introduction Natural landscape linkages (or movement corridors) have been proposed to facilitate and enhance the movement of species by increasing connectivity between suitable habitats. However, most of the work on linkages as conduits for species’ movements has been theoretical, and many of the field studies have alternative explanations. Therefore, the ability of movement corridors to sustain or restore biodiversity in fragmented landscapes has elicited considerable debate, with limited empirical support for the concept (Noss, 1987; Hobbs, 1992; Simberloff et al., 1992; Hess, 1994; Rosenberg et al., 1997). There has been increased recognition of the importance of behavioural studies in conservation (Lima and Zollner, 1993; Curio, 1996). As linkages aim to enable natural behaviour, and to direct movements, a behavioural approach to landscape linkages may provide one * Corresponding author. Tel.: +27-33-260-5328; fax: +27-33-2605105. E-mail address: [email protected] (M.J. Samways).
of the best opportunities for conservation in fragmented landscapes. Habitat boundaries may alter or deflect movement behaviours, and therefore, encourage effective linkage between otherwise separate habitats (Lima and Zollner, 1993; Kuussaari et al., 1996; Schultz, 1998; Haddad, 1999). Although many butterflies are highly vagile, others are sedentary and may require connectivity of natural habitats for movements, to avoid genetic defects through processes such as inbreeding and genetic drift. Also, dispersal by individuals [which may link local populations within metapopulations (Debinski, 1994)] may be reduced if the butterflies will not move through altered habitats. In the case of the endangered French butterfly Parnassius mnemosyne, Descimon and Napolitano (1993) detected reduced genetic diversity in small populations and in populations far from the centre of the species’ distribution. Therefore, the maintenance of connectivity in a fragmented landscape may be vital for many butterflies as well as other organisms. Other variables, such as linkage width, may also affect animal movements through the landscape (Inglis and
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Underwood, 1992; Simberloff et al., 1992). Width may determine the usefulness of linkages for dispersing animals, with narrow linkages having the disadvantage of increasing the relative amount of habitat edge where many species may experience higher mortality. Furthermore, these narrow linkages may restrict grasslandinterior species (Hill, 1995; Machtans et al., 1996). The need for empirical studies, addressing such linkage design and its effect on movement behaviour and ecology, has been stressed (Hobbs, 1992; Inglis and Underwood, 1992; Simberloff et al., 1992; Lindenmayer and Nix, 1993). Such information may be crucial for the management and implementation of linkages in landscapes (Noss, 1987; Harrison, 1992). A network of interconnected linkages between suitable habitat may be one solution for increasing landscape connectivity. Ideally, such linkages should be more than just for dispersal and should also be source habitats enabling long-term survival. Nevertheless, to avoid genetic deterioration, it is important that such habitat webs encourage movement. The importance of these habitat webs as movement linkages will depend on the ecology, dispersal ability and behaviour of a species, as well as its reaction to the bordering habitats. However, an important consideration is that localised species with limited dispersal abilities may not perceive the landscape to be as connected as may highly vagile and habitat-tolerant species (Shreeve, 1995). Therefore, it is vital to determine how each butterfly species responds to a given landscape type. In the afforested landscape of KwaZulu-Natal, South Africa, an extensive and continuous network of natural grassland linkages has been retained between the planted pine compartments. As the extent to which such linkages maintain or encourage movements is unknown, it would be useful to evaluate their effectiveness. The aim here is to establish how such linkages influence the movement pathways of butterflies. Movement behaviours are given for butterfly responses to linkages of varying widths. Linkage width was used as the main variable, because it is one of the most basic structural characteristics of habitats upon which practical landscape design requires a decision.
2. Methods 2.1. Butterfly behaviour Field observations were made at MONDI Goodhope Estate, KwaZulu-Natal, South Africa (29 400 4800 S 29 360 5000 S to 29 550 5800 E 30 000 0500 E; Fig. 1). The area consists of pine plantations (Pinus patula, mostly 30m tall), agricultural lands (crop and dairy farming), indigenous forests (diverse, multi-strata community of indigenous trees without alien pine trees (Cooper, 1985) in a
relatively undisturbed and extensive natural grassland. Pine trees are not indigenous to South Africa but were established as relatively small, even-aged stands ca. 1–50 ha rather than as a large homogenous, afforested area. The whole estate covered 1873 ha, with pines comprising about 66% of the area. The grassland linkages between the compartments varied in width from 20 m to ca. 750 m, while outside the estate they were 5 2 km wide. These and the outside sites were classified in to narrow (<50 m), intermediate (50–250 m), wide (250–750 m) and open (750–2000+ m) width categories. Thirty-eight study sites were selected that differed in structure depending on the width and levels of disturbance (cattle grazing, mown grass and exotic plants; Fig. 1). Butterfly flight patterns were monitored at twoweekly intervals from January to April 1999. These were recorded from 09:30 to 15:30 and on a rotational basis so that biases with respect to preferred flight times were minimised. Flight paths were only recorded on sunny days with <30% cloud cover, and were recorded in open spaces within narrow, intermediate, wide and open linkages, as well as at varying distances from the pine edges. This involved standing in a position with a clear view of the surrounding area and scanning with binoculars in all directions until a flying butterfly was sighted. Each butterfly was followed until it disappeared from view. The flight path was then drawn on a GISprepared map. ‘Movement time’ began when a butterfly flew into a linkage, and ended when it landed to feed, sunbask, oviposit or to drink from open water or mud, or when the butterfly flew out of sight. All behavioural activities were recorded during this time. When two or more butterflies appeared simultaneously, only one butterfly was tracked. Individuals that were prematurely lost from view, could not be identified, or were disturbed by predators, were excluded from the analyses. The data on complete flight paths were gathered and condensed into summary diagrams quantifying all the flight paths. The total distance covered by individual butterflies was estimated from these mapped flight-path summaries. The distance that a butterfly flew into the pine plantation or grassland was estimated using stakes at 10-, 20-, 50- and 100-m intervals. Distances greater than 100 m were calculated from the mapped movement paths. The natural forest was so dense that stakes were inserted only at 10- and 20-m intervals, as individual butterflies could not be followed for more than 20 m. This sampling continued throughout the peak flight period for the butterfly assemblage. Only individuals with 10 or more mapped flight patterns were considered significant for individual analysis. This resulted in only the 23 most abundant species (of the 31 species recorded) being analysed in detail. These different species varied in their size, movement ability and habitat preference (Table 1). Danaus chrysippus, Catopsilia florella, Vanessa cardui, Belenois aurota and
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Belenois creona are global or local migrants (Pringle et al., 1994), the large swallowtails (Papilio dardanus, Papilio demodocus, Papilio nireus and Graphium leonidas) are powerful fliers, and the lycaenids (Chrysoritis lycegenes and Lampides boeticus) and the skipper (Spialia spio) are less vagile. The remaining species (Amauris albimaculata, Cassionympha cassius, Paralethe dendrophilus, Hyalites encedon, Acraea horta, Hypolimnas misippus, Precis octavia, Precis hierta, Precis orithya, Colias electo and Eurema brigitta) are intermediate in size and flight mobility. 2.2. Data analyses Spearman’s Rank Correlation Coefficient was used to correlate the linkage width with the number of species
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and individuals. Movement times (in seconds) and distances (in metres) that a butterfly could fly, differed within and between linkage widths, and therefore, were standardised to movement speeds (m sec1). Movement rates were averaged for each species in each width category. A one-way analysis of variance (ANOVA) was used to compare differences in movement rates between the different linkage widths. Disturbance levels (cattle impact and the presence of exotic plants) identified by the first axis of the canonical correspondence analysis (CCA) were used to classify the disturbed sites into natural (0–1.7), low (1.7–2.6), medium (2.6–4.5) and high (4.5–6) disturbance. Only natural grassland linkages were used for estimating flight speeds, because of the low species richness and diversity in the disturbed sites. However, one linkage of each width in the low,
Fig. 1. The study area with 38 sites at Mondi Goodhope Estate, KwaZulu-Natal, South Africa.
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medium and highly disturbed grassland sites was used for assessing flight patterns. Chi-square tests of independence were used to test the null hypothesis that butterflies which flew into or over the pine trees, (i.e. left the grassland linkages) did so with equal probability for all sides of the forest or grassland habitat in question.
3. Results 3.1. Linkage width and movement speeds Linkage width was positively significantly correlated with the number of species (rs=0.39, P<0.01, n=37) and the number of individuals (rs=0.26, P<0.05, n=37) (Figs. 2 and 3). Average movement speeds were significantly dependent on the width of the linkage (Fig. 4). There was a significant difference between movement speeds in the narrow and in the intermediate width of linkages (F2,11=1.71, P<0.05), and between the wide (F2,11=2.85, P<0.01) and the open (F2,11=3.43, P<0.01) linkages. Similarly, there was a significant difference between the speeds in the intermediate and wide (F2,21=1.34, P<0.05) and open
(F2,21=3.22, P<0.01) linkages. However, there was no significant difference between the wide and open linkages, suggesting that movement speeds were relatively similar in linkages wider than 250 m. The highest average speed of 3.86 m sec1 for Papilio demodocus (Table 2), was recorded in the narrow linkage (<50 m). The slowest movements were recorded in the widest linkages, which was due to the butterflies using these linkages as a habitat (i.e. stopping to nectar, drink, sunbask and rest). Butterflies also flew faster through linkages that were highly disturbed, had few nectar flowers, a high density of exotic plants, short grasses and high impact from cattle. However, linkage width did not significantly affect the movement speeds of many migrant butterflies (e.g. Catopsilia florella, Danaus chrysippus and Belenois aurota). Likewise, some of the sedentary and local endemic butterflies (e.g. Chrysoritis lycegenes) were unaffected by linkage width (i.e. did not fly farther than 200 m in either the intermediate, wide or open linkages). Butterflies generally moved farthest and fastest in the narrowest corridors. Maximum speeds reached by butterflies in the narrow linkages were on average 2.2 times faster than in the intermediate, 8.9 times faster than in
Table 1 Total number of butterflies and their habitat preferences, status and geographical distribution recorded at Mondi Goodhope Estate Butterfly species
Total number of individuals
Habitat preference
Distribution
Current status
Nymphalidae Danaus chrysippus Amauris albimaculata Paralethe dendrophilus Cassionympha cassius Hyalites encedon Acraea horta Hypolimnas misippus Precis octavia Precis hierta Precis orithya Vanessa cardui
352 26 41 126 25 21 30 677 99 18 246
Open habitats Forest habitats Forest habitats Forest habitats Open habitats Open habitats Open habitats Open habitats Open habitats Open habitats Open habitats
Africa Southern Africa South Africa South Africa Southern Africa South Africa Africa Southern Africa Southern Africa Africa Africa, Europe
Common migrant Common in preferred habitat Locally common Common Common in preferred habitat Common Common Common Common Locally common Common migrant
Grassland habitats Open habitats
KwaZulu-Natal Africa
Endemic to the KwaZulu-Natal Midlands Common
Lycaenidae Chrysoritis lycegenes Lampides boeticus
47 56
Pieridae Colias electo Catopsilia florella Eurema brigitta Belenois aurota Belenois creona
21 52 102 361 97
Open habitats Open habitats Open habitats Open habitats Open habitats
Southern Africa Southern Africa Southern Africa Southern Africa Africa
Common Common Common Common Common
Papilionidae Papilio dardarnus Papilio demodocus Papilio nitreus Graphium leonidas
19 58 29 17
Forest habitats Open habitats Open habitats Open habitats
Southern Africa Africa Southern Africa Southern Africa
Locally common Common Common Locally common
Hesperiidae Spialia spio
22
Grassland habitats
Southern Africa
Common
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the wide and 13.3 times faster than in the open linkages. Although the widespread, common and highly mobile species flew along linkages of all sizes, very few of the local and relatively sedentary species entered linkages of widths <250 m. Those that did only spent a short time in them.
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3.2. Effect of pine plantation and natural forest boundaries Most butterflies flew straight along the narrow linkages, parallel with the edges with more species (Fig. 5) and higher densities (Fig. 6) towards the centre of the
Fig. 2. Regression of the proportion of species recorded against the width of the 38 grassland linkages.
Fig. 3. Regression of the proportion of individuals recorded against the width of the 38 grassland linkages.
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Table 2 The mean flight rates (1 S.E.) for the 23 butterfly species in varying grassland linkage widths Species
Danaus chrysippus Amauris albimaculata Paralethe dendrophilus Cassionympha cassius Hyalites encedon Acraea horta Hypolimnas misippus Precis octavia Precis hierta Precis orithya Vanessa cardui Chrysoritis lycegenes Lampides boeticus Colias electo Catopsilia florella Eurema brigitta Belenois aurota Belenois creona Papilio dardanus Papilio demodocus Papilio nireus Graphium leonidas Spialia spio Mean rate a b
Flying rate (m sec1) < 50m Narrow
50–250 m Intermediate
250–750 m Wide
>750 m Open
Pa
3.020.98 0.210.04 3.212.77 0.110.07
2.31 0.43 0.17 0.01 3.56 2.18 0.10 0.00 0.45 0.26 0.21 0.12 2.31 1.3 2.87 1.15 1.03 0.09 0.45 0.39 1.02 0.98 0.04 0.02 0.02 0.01 0.13 0.10 1.34 1.12 1.03 0.32 4.17 3.65 2.03 1.11
1.56 0.85 0.04 0.02 2.08 1.54 0.10 0.03 0.32 0.11 0.35 0.18 3.11 2.99 1.78 1.19 0.73 0.36 0.76 0.17 0.32 0.26 0.02 0.00 0.01 0.01 0.12 0.07 1.21 0.96 0.43 0.22 3.78 3.33 0.45 0.27 1.03 0.91 1.73 1.42 1.76 1.38 1.42 1.36 0.02 0.00
1.490.21 0.020.01 1.231.08 0.090.01 0.250.09 0.130.07 2.062.34 1.560.30 0.560.62 0.180.07 0.100.16 0.010.00 0.010.00 0.030.01 0.970.38 0.140.09 3.022.89 0.080.06 0.480.37 0.920.33 0.120.06 1.261.21 0.010.00
NS <0.01 NS NS NS NS NS <0.05 <0.05 NS <0.001 NS NS NS NS <0.01 NS <0.001 <0.01 <0.001 <0.05 NS NS
1.00 1.02
0.670.81
<0.05
b b b
3.453.28 1.120.20 b
2.982.84 b b b b b
3.194.11 2.142.01 b
b
3.863.72
3.81 2.28 2.13 1.86 1.98 1.74
b b b
b
2.551.58
1.48 1.33
Results of an ANOVA testing significant differences between the four width categories. Butterfly not recorded in the specified width category.
Fig. 4. Mean movement speeds (1 S.E.) for the 23 butterfly species. The Y-axis (time) includes time spent stopping (e.g. nectaring, drinking, ovipositing and sunbasking). The X-axis (distance) was the distance from the first point of observation to when the butterfly flew out of the linkage.
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linkage. Densities of many localised species [e.g. Chrysoritis lycegenes (Fig. 7e) and S. spio (Fig. 7f)] increased sharply with distance from the edge. However, a few of these species flew along the edge of the pine patches. For example, Cassionympha cassius followed the edge of the pine trees in a zigzag fashion, generally not moving
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more than 20 m away from the sheltered edge (Fig. 7c). The movements of natural forest species, for example Paralethe dendrophilus, were unaffected by the pine trees (Fig. 7b). Yet, the pine forest was a barrier to most species, with only a few species flying into it (e.g. V. cardui (Fig. 7a), Cassionympha cassius, Precis octavia
Fig. 5. The proportion of butterfly species recorded within linkages of different widths. Distance from the edge (value 0) is the linear distance to the nearest pine or natural forest boundary. Values >0 indicate presence in the grassland linkage, whereas values <0 indicate presence within the forest.
Fig. 6. The proportion of individual butterflies within linkages of different widths. Distance from the edge (value 0) is the linear distance to the nearest pine or natural forest boundary. Values >0 indicate presence in the grassland linkage, whereas values <0 indicate presence within the forest.
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Fig. 7. The proportional abundance of (a) Vanessa cardui, (b) Paralethe dendrophilus, (c) Cassionympha cassius, (d) Precis octavia, (e) Chrysoritis lycegenes and (f) Spialia spio within different linkage widths. Distance from the edge (value 0) is the linear distance to the nearest pine forest boundary. Values >0 indicate presence in the grassland linkage, whereas values <0 indicate presence within the forest.
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(Fig. 7d) and Precis dendrophilus) or over it (e.g. Papilio spp., Belenois spp. and Paralethe dendrophilus). Those that flew over had flight patterns that were significantly biased towards the pine-margins adjacent to the larger grassland patches (Table 3). Furthermore, all Papilio species and Paralethe dendrophilus were equally inclined to fly over the pine or natural forest as to fly along its boundary. Therefore, the large, continuous patches of forest appear to be a barrier, even to the highly mobile and frequently migrant butterflies. In contrast, the boundary of the indigenous forest had a greater number of species (Fig. 5) and individuals (Fig. 6) than did the pine forest. Also, the butterflies moved farther into the indigenous forest than into the pine plantation, even though the former was denser.
3.3. Landing sites and landscape barriers Butterflies stopped mostly for nectar, with resting and sunbasking the next most important landing activities (Fig. 8). Boulders and rocks were favoured landing sites for many species (e.g. Precis hierta, Precis octavia, P. orithya, V. cardui, Colias electo and D. chrysippus), especially early and late in the day. Short grasses were favoured landing sites for certain species (e.g. Acraea horta and V. cardui), tall grasses for others (e.g. E. brigitta, L. boeticus, Chrysoritis lycegenes, Hypolimnas misippus and S. spio) and bare ground for others still (e.g. Precis hierta, Precis octavia and Colias electo). After rain, mud puddles became important stopping points. Few butterflies stopped in the mowed or heavily
Table 3 The percentage of individual butterflies leaving the grassland linkages by flying over pine forest boundaries at different distances from the nearest open grassland patch (sample sizes in parentheses) Butterfly species
Distance from grassland patch <20 m
20–50 m
50–100 m
100–250 m
>250 m
X2 (d.f.=4)
Pa
Papilio demodocus Papilio nireus Belenois aurota Belenois creona Paralethe dendrophilus Danaus chrysippus Precis octavia
66 (6) 57 (4) 42 (14) 72 (5) 41 (8) 82 (27) 74 (63)
18 (9) 32 (4) 31 (59) 26 (7) 18 (12) 15 (20) 13 (95)
11 (12) 40 (9) 12 (56) 2 (13) 24 (7) 3 (64) 3 (121)
2 (13) 7 (5) 9 (78) 0 (27) 11 (8) 0 (85) 8 (219)
3 (11) 0 (7) 3 (94) 0 (21) 6 (6) 0 (104) 2 (101)
7.3 5.3 4.7 6.7 3.5 12.4 9.4
<0.01 <0.05 <0.05 <0.001 NS <0.001 <0.01
Mean
6216
228
14 18
8 3
41
7.1
<0.01
a Results of Chi-square tests of independence investigating whether butterflies left the linkage with equal probability through all parts of the perimeter.
Fig. 8. Mean number of butterfly behaviours observed within each linkage width category. The behaviours of observed butterflies were categorised as either flying, reproductive (which included mating swirls, mating and oviposition), nectaring, basking or resting, or other (which included water drinking, mud puddling and territoriality).
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Fig. 9. Proportion of species recorded in each linkage width-category for different disturbance levels. Disturbance included cattle trampling and grazing, mowing, agriculture and human disturbance.
grazed grasslands, although even fewer landed in natural forest. Heavily grazed and mown grasses were a barrier for many species (Fig. 9), except for Acraea horta, which commonly landed and rested among the short grass. Most species moved quickly, without stopping, over or along mown tracks to reach the natural grasslands. Most landings were in the natural grasslands where there were the largest number of nectar sources and oviposition sites. Large dams (>150 m wide) were a barrier to some species (e.g. Acraea horta, S. spio and P. lycegenes), which flew around the edge to get to the other side. However, some other species, especially the large mobile ones (e.g. Papilio spp. and Belenois spp.) flew directly over the water.
4. Discussion This study only assessed how linkages influence dispersal, and did not aim to establish whether these linkages were also habitats that provided all the resources for completing life cycles. Nevertheless, the fact that slow-moving, endemic butterflies occurred within linkages 250 m wide suggests that such linkages permit some residence as well as diffusion of these butterflies of conservation significance. Having conditions suitable for such gradual permeation of the landscape is important, as individuals of relatively sedentary species, such as lycaenids, are unlikely to disperse more than 2 km (Hanski and Kuussaari, 1995).
The four commonest species in this study occurred in most linkages, and are well-known as habitat generalists and migrants. Also, all the large and strong fliers, irrespective of phylogeny, moved relatively independently of habitat type, whether in natural grassland or in alien pines. None of these above species are currently of conservation value. This mirrors the situation with Pieris rapae in Europe, which disperses long distances in random directions (Fahrig and Paloheimo, 1988). Precis hierta and Precis octavia penetrated the first few rows of pine trees. However, as only four species entered the pine compartments, connectivity for these animals clearly would have been much lower in the absence of grassland linkages. Other species flew along (e.g. Cassionympha cassius) or over (e.g. Papilio spp., Belenois spp., Paralethe deudrophilus) the pine trees, indicating that these alien stands are not a complete barrier to some species. Similarly, pine forests are only a partial barrier for the American butterfly Junonia coenia (Haddad, 1999). Movement over unsuitable habitat can have enormous benefits for gene flow, as in the case of the European Proclossiana eunomia (Baguette and Ne`ve, 1994). Most species however, tended to avoid the pines and did not even follow the edges of the compartments as they did along the edges of the natural forest. Although these forest edges are naturally very sharp (Kotze and Samways, 2001) they did not present such a tall and dark wall as did the pines. This was illustrated by the different permeability of the edges, with several more species entering the natural forest than the pine compartments.
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Nevertheless, they often turned back once they had entered the forest. Some species appeared to actually stay clear of the pine (and forest) boundaries, with their densities being higher away from the edges (20 m or so). Similar behaviour has been observed for the threatened American habitat specialist Icaricia icarioides fenderi (Schultz, 1998). In the case of the European Mellicta athalia, even small patches of unsuitable vegetation may have such an influence that they separate subpopulations (Warren, 1987). Many of the butterfly species here, especially those that were relatively tolerant of pines, showed a change in behaviour with habitat. They moved farther and faster along increasingly disturbed grassland linkages, which were acting as movement conduits. This is probably because the increased disturbance levels offered little for most of their life activities, and their behaviour was to rapidly seek more appropriate habitat. A parallel example is that of the sweet potato weevil (Cylas formicarius elagantulus) which moves up to 1000 m in fields without sweet potatoes compared to 500 m in fields with them (Miyatake et al., 1995). In contrast, the wide linkages supported higher densities of butterflies with, slower speeds and more random movements compared with the narrower linkages. Such wide linkages with their high interior to edge ratio, were virtually acting as habitats per se. It is not surprising therefore, that densities were higher in these areas, especially as it is well known that higher insect densities occur in larger patches (Kareiva, 1985; Bach, 1988; Hill et al., 1996). In general, it was clear that the wider natural linkages provided better habitat for the grassland-specialist species, which tended not even to enter the narrow (<50 m) linkages. What are the conservation recommendations that arise from this study? First, we must clearly distinguish between a long, narrow strip of land being only a movement corridor or, on the other hand, having habitat value for permanent living. Secondly, a narrow corridor is inherently less suitable as a habitat because of the influence of neighbouring pines either directly on the insect behaviour or indirectly through influencing the grassland plants, and hence the habitat quality (Samways and Moore, 1991). An additional consideration is that narrow linkages inevitably receive more disturbance than wider linkages given the same amount of human and cattle traffic. The next question that arises is then how wide should a linkage be? Which, of course, rests on having determined the conservation goal. This study shows that any linkage is better than none, but that also the wider the linkage the more value it has for those species of more conservation concern. There reaches a point when the increasing width elevates the linkage from simply a movement corridor to an interconnected habitat. For these butterflies, this figure is 250 m wide. But it is clear that such a habitat linkage
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must be part of greater linkages throughout the landscape. A web of such habitat linkages appears, at least from the information here, to go a long way to reconciling economic production of pines with the conservation of biodiversity.
Acknowledgements We thank Ricky Pott and the field managers of MONDI Goodhope Estate, as well as the farmers in the study area, for practical support. Financial support was provided by MONDI forests, the World Wide Fund for Nature (South Africa). Two anonymous referees and the editor made constructive and stimulating comments. Catherine Murray kindly assisted with final preparation of the manuscript.
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Kotze, D.J., Samways, M.J., 2001. No general edge effects for Afromontane forest/grassland ecotones. Biodiversity and Conservation (in press). Kuussaari, M., Nieminen, M., Hanski, I., 1996. An experimental study of migration in the Glanville fritillary butterfly Melitaea cinxia. Journal of Animal Ecology 65, 791–801. Lima, S.L., Zollner, P.A., 1993. Towards a behavioural ecology of ecological landscapes. Trends in Ecology and Evolution 11, 131– 135. Lindenmayer, D.B., Nix, H.A., 1993. Ecological principles for the design of corridors. Conservation Biology 7, 627–630. Machtans, C.S., Villard, M., Hannon, S.J., 1996. Use of riparian strips as movement corridors. Conservation Biology 10, 1366–1379. Miyatake, T., Kawasaki, K., Kohoma, T., Moriya, S., Shimoji, Y., 1995. Dispersal of male sweet potato weevils (Coleoptera: Curculionidae) in fields with and without sweet potato plants. Environmental Entomology 24, 1167–1174. Noss, R.F., 1987. Corridors in real landscapes: a reply to Simberloff and Cox. Conservation Biology 1, 159–164.
Pringle, E.L.L., Henning, G.A., Ball, J.B., 1994. Pennington’s Butterflies of Southern Africa, 2nd Edition. Struik Winchester, Cape Town. Rosenberg, D.K., Noon, B.R., Meslow, E.C., 1997. Biological corridors: form, function and efficiency. BioScience 47, 677–687. Samways, M.J., Moore, S.D., 1991. Influence of exotic conifer patches on grasshopper (Orthoptera) assemblages in a grassland matrix at a recreational resort, Natal, South Africa. Biological Conservation 57, 205–219. Schultz, C.B., 1998. Dispersal behaviour and its implication for reserve design in a rare Oregon butterfly. Conservation Biology 12, 284–292. Schreeve, T.G., 1995. Butterfly mobility. In: Pullin, A.S. (Ed.), Ecology and Conservation of Butterflies. Chapman and Hall, London, pp. 37–64. Simberloff, D., Farr, J.R., Cox, J., Mehlman, D.W., 1992. Movement corridors: conservation bargains or poor investments? Conservation Biology 6, 493–504. Warren, M.S., 1987. The ecology and conservation of the heath fritillary butterfly, Mellicta athalia. (III) population dynamics and effects of habitat management. Journal of Applied Ecology 24, 499–513.
Width of grassland linkages for the conservation of butterflies in South African afforested areas Sarah R. Pryke, Michael J. Samways * Invertebrate Conservation Research Centre, School of Botany and Zoology, University of Natal (Pietermaritzburg), Private Bag X01, Scottsville, 3209, South Africa Received 10 July 2000; received in revised form 14 November 2000; accepted 2 January 2001
Abstract Flight behaviours of 23 butterfly species were mapped to establish the effect of both pine afforestation and different-sized grassland linkages on localised butterfly movements. Blocks of pine trees caused most butterflies to change direction and move away from the pine edge. Only four species crossed the grassland/pine edge, and of these, only two flew farther than 20 m into the pine forest. The adjacent grassland/indigenous forest edge had a higher number of species, but very few of these entered the forest. Movement rates were significantly faster in the narrow and highly-disturbed linkages, than in the wide and open grasslands, with the linkages acting as conduits between the preferred grassland patches. However, only highly vagile and eurytopic species actually entered the narrower grassland linkages. In contrast, the wider linkages hosted a significantly higher species diversity and functioned as habitats per se and not just as movement corridors, with butterflies frequently stopping to nectar, oviposit, drink and sunbask. Knowledge of butterfly responses to different landscape structures has important conservation and management implications. From the results here, it is recommended that, for these butterflies, the natural grassland linkages should be wider than 250 m. # 2001 Elsevier Science Ltd. All rights reserved. Keywords: Lepidoptera; Habitat webs; Behaviour; Afforestation; Linkages
1. Introduction Natural landscape linkages (or movement corridors) have been proposed to facilitate and enhance the movement of species by increasing connectivity between suitable habitats. However, most of the work on linkages as conduits for species’ movements has been theoretical, and many of the field studies have alternative explanations. Therefore, the ability of movement corridors to sustain or restore biodiversity in fragmented landscapes has elicited considerable debate, with limited empirical support for the concept (Noss, 1987; Hobbs, 1992; Simberloff et al., 1992; Hess, 1994; Rosenberg et al., 1997). There has been increased recognition of the importance of behavioural studies in conservation (Lima and Zollner, 1993; Curio, 1996). As linkages aim to enable natural behaviour, and to direct movements, a behavioural approach to landscape linkages may provide one * Corresponding author. Tel.: +27-33-260-5328; fax: +27-33-2605105. E-mail address: [email protected] (M.J. Samways).
of the best opportunities for conservation in fragmented landscapes. Habitat boundaries may alter or deflect movement behaviours, and therefore, encourage effective linkage between otherwise separate habitats (Lima and Zollner, 1993; Kuussaari et al., 1996; Schultz, 1998; Haddad, 1999). Although many butterflies are highly vagile, others are sedentary and may require connectivity of natural habitats for movements, to avoid genetic defects through processes such as inbreeding and genetic drift. Also, dispersal by individuals [which may link local populations within metapopulations (Debinski, 1994)] may be reduced if the butterflies will not move through altered habitats. In the case of the endangered French butterfly Parnassius mnemosyne, Descimon and Napolitano (1993) detected reduced genetic diversity in small populations and in populations far from the centre of the species’ distribution. Therefore, the maintenance of connectivity in a fragmented landscape may be vital for many butterflies as well as other organisms. Other variables, such as linkage width, may also affect animal movements through the landscape (Inglis and
0006-3207/01/$ - see front matter # 2001 Elsevier Science Ltd. All rights reserved. PII: S0006-3207(01)00042-8
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Underwood, 1992; Simberloff et al., 1992). Width may determine the usefulness of linkages for dispersing animals, with narrow linkages having the disadvantage of increasing the relative amount of habitat edge where many species may experience higher mortality. Furthermore, these narrow linkages may restrict grasslandinterior species (Hill, 1995; Machtans et al., 1996). The need for empirical studies, addressing such linkage design and its effect on movement behaviour and ecology, has been stressed (Hobbs, 1992; Inglis and Underwood, 1992; Simberloff et al., 1992; Lindenmayer and Nix, 1993). Such information may be crucial for the management and implementation of linkages in landscapes (Noss, 1987; Harrison, 1992). A network of interconnected linkages between suitable habitat may be one solution for increasing landscape connectivity. Ideally, such linkages should be more than just for dispersal and should also be source habitats enabling long-term survival. Nevertheless, to avoid genetic deterioration, it is important that such habitat webs encourage movement. The importance of these habitat webs as movement linkages will depend on the ecology, dispersal ability and behaviour of a species, as well as its reaction to the bordering habitats. However, an important consideration is that localised species with limited dispersal abilities may not perceive the landscape to be as connected as may highly vagile and habitat-tolerant species (Shreeve, 1995). Therefore, it is vital to determine how each butterfly species responds to a given landscape type. In the afforested landscape of KwaZulu-Natal, South Africa, an extensive and continuous network of natural grassland linkages has been retained between the planted pine compartments. As the extent to which such linkages maintain or encourage movements is unknown, it would be useful to evaluate their effectiveness. The aim here is to establish how such linkages influence the movement pathways of butterflies. Movement behaviours are given for butterfly responses to linkages of varying widths. Linkage width was used as the main variable, because it is one of the most basic structural characteristics of habitats upon which practical landscape design requires a decision.
2. Methods 2.1. Butterfly behaviour Field observations were made at MONDI Goodhope Estate, KwaZulu-Natal, South Africa (29 400 4800 S 29 360 5000 S to 29 550 5800 E 30 000 0500 E; Fig. 1). The area consists of pine plantations (Pinus patula, mostly 30m tall), agricultural lands (crop and dairy farming), indigenous forests (diverse, multi-strata community of indigenous trees without alien pine trees (Cooper, 1985) in a
relatively undisturbed and extensive natural grassland. Pine trees are not indigenous to South Africa but were established as relatively small, even-aged stands ca. 1–50 ha rather than as a large homogenous, afforested area. The whole estate covered 1873 ha, with pines comprising about 66% of the area. The grassland linkages between the compartments varied in width from 20 m to ca. 750 m, while outside the estate they were 5 2 km wide. These and the outside sites were classified in to narrow (<50 m), intermediate (50–250 m), wide (250–750 m) and open (750–2000+ m) width categories. Thirty-eight study sites were selected that differed in structure depending on the width and levels of disturbance (cattle grazing, mown grass and exotic plants; Fig. 1). Butterfly flight patterns were monitored at twoweekly intervals from January to April 1999. These were recorded from 09:30 to 15:30 and on a rotational basis so that biases with respect to preferred flight times were minimised. Flight paths were only recorded on sunny days with <30% cloud cover, and were recorded in open spaces within narrow, intermediate, wide and open linkages, as well as at varying distances from the pine edges. This involved standing in a position with a clear view of the surrounding area and scanning with binoculars in all directions until a flying butterfly was sighted. Each butterfly was followed until it disappeared from view. The flight path was then drawn on a GISprepared map. ‘Movement time’ began when a butterfly flew into a linkage, and ended when it landed to feed, sunbask, oviposit or to drink from open water or mud, or when the butterfly flew out of sight. All behavioural activities were recorded during this time. When two or more butterflies appeared simultaneously, only one butterfly was tracked. Individuals that were prematurely lost from view, could not be identified, or were disturbed by predators, were excluded from the analyses. The data on complete flight paths were gathered and condensed into summary diagrams quantifying all the flight paths. The total distance covered by individual butterflies was estimated from these mapped flight-path summaries. The distance that a butterfly flew into the pine plantation or grassland was estimated using stakes at 10-, 20-, 50- and 100-m intervals. Distances greater than 100 m were calculated from the mapped movement paths. The natural forest was so dense that stakes were inserted only at 10- and 20-m intervals, as individual butterflies could not be followed for more than 20 m. This sampling continued throughout the peak flight period for the butterfly assemblage. Only individuals with 10 or more mapped flight patterns were considered significant for individual analysis. This resulted in only the 23 most abundant species (of the 31 species recorded) being analysed in detail. These different species varied in their size, movement ability and habitat preference (Table 1). Danaus chrysippus, Catopsilia florella, Vanessa cardui, Belenois aurota and
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Belenois creona are global or local migrants (Pringle et al., 1994), the large swallowtails (Papilio dardanus, Papilio demodocus, Papilio nireus and Graphium leonidas) are powerful fliers, and the lycaenids (Chrysoritis lycegenes and Lampides boeticus) and the skipper (Spialia spio) are less vagile. The remaining species (Amauris albimaculata, Cassionympha cassius, Paralethe dendrophilus, Hyalites encedon, Acraea horta, Hypolimnas misippus, Precis octavia, Precis hierta, Precis orithya, Colias electo and Eurema brigitta) are intermediate in size and flight mobility. 2.2. Data analyses Spearman’s Rank Correlation Coefficient was used to correlate the linkage width with the number of species
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and individuals. Movement times (in seconds) and distances (in metres) that a butterfly could fly, differed within and between linkage widths, and therefore, were standardised to movement speeds (m sec1). Movement rates were averaged for each species in each width category. A one-way analysis of variance (ANOVA) was used to compare differences in movement rates between the different linkage widths. Disturbance levels (cattle impact and the presence of exotic plants) identified by the first axis of the canonical correspondence analysis (CCA) were used to classify the disturbed sites into natural (0–1.7), low (1.7–2.6), medium (2.6–4.5) and high (4.5–6) disturbance. Only natural grassland linkages were used for estimating flight speeds, because of the low species richness and diversity in the disturbed sites. However, one linkage of each width in the low,
Fig. 1. The study area with 38 sites at Mondi Goodhope Estate, KwaZulu-Natal, South Africa.
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medium and highly disturbed grassland sites was used for assessing flight patterns. Chi-square tests of independence were used to test the null hypothesis that butterflies which flew into or over the pine trees, (i.e. left the grassland linkages) did so with equal probability for all sides of the forest or grassland habitat in question.
3. Results 3.1. Linkage width and movement speeds Linkage width was positively significantly correlated with the number of species (rs=0.39, P<0.01, n=37) and the number of individuals (rs=0.26, P<0.05, n=37) (Figs. 2 and 3). Average movement speeds were significantly dependent on the width of the linkage (Fig. 4). There was a significant difference between movement speeds in the narrow and in the intermediate width of linkages (F2,11=1.71, P<0.05), and between the wide (F2,11=2.85, P<0.01) and the open (F2,11=3.43, P<0.01) linkages. Similarly, there was a significant difference between the speeds in the intermediate and wide (F2,21=1.34, P<0.05) and open
(F2,21=3.22, P<0.01) linkages. However, there was no significant difference between the wide and open linkages, suggesting that movement speeds were relatively similar in linkages wider than 250 m. The highest average speed of 3.86 m sec1 for Papilio demodocus (Table 2), was recorded in the narrow linkage (<50 m). The slowest movements were recorded in the widest linkages, which was due to the butterflies using these linkages as a habitat (i.e. stopping to nectar, drink, sunbask and rest). Butterflies also flew faster through linkages that were highly disturbed, had few nectar flowers, a high density of exotic plants, short grasses and high impact from cattle. However, linkage width did not significantly affect the movement speeds of many migrant butterflies (e.g. Catopsilia florella, Danaus chrysippus and Belenois aurota). Likewise, some of the sedentary and local endemic butterflies (e.g. Chrysoritis lycegenes) were unaffected by linkage width (i.e. did not fly farther than 200 m in either the intermediate, wide or open linkages). Butterflies generally moved farthest and fastest in the narrowest corridors. Maximum speeds reached by butterflies in the narrow linkages were on average 2.2 times faster than in the intermediate, 8.9 times faster than in
Table 1 Total number of butterflies and their habitat preferences, status and geographical distribution recorded at Mondi Goodhope Estate Butterfly species
Total number of individuals
Habitat preference
Distribution
Current status
Nymphalidae Danaus chrysippus Amauris albimaculata Paralethe dendrophilus Cassionympha cassius Hyalites encedon Acraea horta Hypolimnas misippus Precis octavia Precis hierta Precis orithya Vanessa cardui
352 26 41 126 25 21 30 677 99 18 246
Open habitats Forest habitats Forest habitats Forest habitats Open habitats Open habitats Open habitats Open habitats Open habitats Open habitats Open habitats
Africa Southern Africa South Africa South Africa Southern Africa South Africa Africa Southern Africa Southern Africa Africa Africa, Europe
Common migrant Common in preferred habitat Locally common Common Common in preferred habitat Common Common Common Common Locally common Common migrant
Grassland habitats Open habitats
KwaZulu-Natal Africa
Endemic to the KwaZulu-Natal Midlands Common
Lycaenidae Chrysoritis lycegenes Lampides boeticus
47 56
Pieridae Colias electo Catopsilia florella Eurema brigitta Belenois aurota Belenois creona
21 52 102 361 97
Open habitats Open habitats Open habitats Open habitats Open habitats
Southern Africa Southern Africa Southern Africa Southern Africa Africa
Common Common Common Common Common
Papilionidae Papilio dardarnus Papilio demodocus Papilio nitreus Graphium leonidas
19 58 29 17
Forest habitats Open habitats Open habitats Open habitats
Southern Africa Africa Southern Africa Southern Africa
Locally common Common Common Locally common
Hesperiidae Spialia spio
22
Grassland habitats
Southern Africa
Common
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the wide and 13.3 times faster than in the open linkages. Although the widespread, common and highly mobile species flew along linkages of all sizes, very few of the local and relatively sedentary species entered linkages of widths <250 m. Those that did only spent a short time in them.
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3.2. Effect of pine plantation and natural forest boundaries Most butterflies flew straight along the narrow linkages, parallel with the edges with more species (Fig. 5) and higher densities (Fig. 6) towards the centre of the
Fig. 2. Regression of the proportion of species recorded against the width of the 38 grassland linkages.
Fig. 3. Regression of the proportion of individuals recorded against the width of the 38 grassland linkages.
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Table 2 The mean flight rates (1 S.E.) for the 23 butterfly species in varying grassland linkage widths Species
Danaus chrysippus Amauris albimaculata Paralethe dendrophilus Cassionympha cassius Hyalites encedon Acraea horta Hypolimnas misippus Precis octavia Precis hierta Precis orithya Vanessa cardui Chrysoritis lycegenes Lampides boeticus Colias electo Catopsilia florella Eurema brigitta Belenois aurota Belenois creona Papilio dardanus Papilio demodocus Papilio nireus Graphium leonidas Spialia spio Mean rate a b
Flying rate (m sec1) < 50m Narrow
50–250 m Intermediate
250–750 m Wide
>750 m Open
Pa
3.020.98 0.210.04 3.212.77 0.110.07
2.31 0.43 0.17 0.01 3.56 2.18 0.10 0.00 0.45 0.26 0.21 0.12 2.31 1.3 2.87 1.15 1.03 0.09 0.45 0.39 1.02 0.98 0.04 0.02 0.02 0.01 0.13 0.10 1.34 1.12 1.03 0.32 4.17 3.65 2.03 1.11
1.56 0.85 0.04 0.02 2.08 1.54 0.10 0.03 0.32 0.11 0.35 0.18 3.11 2.99 1.78 1.19 0.73 0.36 0.76 0.17 0.32 0.26 0.02 0.00 0.01 0.01 0.12 0.07 1.21 0.96 0.43 0.22 3.78 3.33 0.45 0.27 1.03 0.91 1.73 1.42 1.76 1.38 1.42 1.36 0.02 0.00
1.490.21 0.020.01 1.231.08 0.090.01 0.250.09 0.130.07 2.062.34 1.560.30 0.560.62 0.180.07 0.100.16 0.010.00 0.010.00 0.030.01 0.970.38 0.140.09 3.022.89 0.080.06 0.480.37 0.920.33 0.120.06 1.261.21 0.010.00
NS <0.01 NS NS NS NS NS <0.05 <0.05 NS <0.001 NS NS NS NS <0.01 NS <0.001 <0.01 <0.001 <0.05 NS NS
1.00 1.02
0.670.81
<0.05
b b b
3.453.28 1.120.20 b
2.982.84 b b b b b
3.194.11 2.142.01 b
b
3.863.72
3.81 2.28 2.13 1.86 1.98 1.74
b b b
b
2.551.58
1.48 1.33
Results of an ANOVA testing significant differences between the four width categories. Butterfly not recorded in the specified width category.
Fig. 4. Mean movement speeds (1 S.E.) for the 23 butterfly species. The Y-axis (time) includes time spent stopping (e.g. nectaring, drinking, ovipositing and sunbasking). The X-axis (distance) was the distance from the first point of observation to when the butterfly flew out of the linkage.
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linkage. Densities of many localised species [e.g. Chrysoritis lycegenes (Fig. 7e) and S. spio (Fig. 7f)] increased sharply with distance from the edge. However, a few of these species flew along the edge of the pine patches. For example, Cassionympha cassius followed the edge of the pine trees in a zigzag fashion, generally not moving
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more than 20 m away from the sheltered edge (Fig. 7c). The movements of natural forest species, for example Paralethe dendrophilus, were unaffected by the pine trees (Fig. 7b). Yet, the pine forest was a barrier to most species, with only a few species flying into it (e.g. V. cardui (Fig. 7a), Cassionympha cassius, Precis octavia
Fig. 5. The proportion of butterfly species recorded within linkages of different widths. Distance from the edge (value 0) is the linear distance to the nearest pine or natural forest boundary. Values >0 indicate presence in the grassland linkage, whereas values <0 indicate presence within the forest.
Fig. 6. The proportion of individual butterflies within linkages of different widths. Distance from the edge (value 0) is the linear distance to the nearest pine or natural forest boundary. Values >0 indicate presence in the grassland linkage, whereas values <0 indicate presence within the forest.
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Fig. 7. The proportional abundance of (a) Vanessa cardui, (b) Paralethe dendrophilus, (c) Cassionympha cassius, (d) Precis octavia, (e) Chrysoritis lycegenes and (f) Spialia spio within different linkage widths. Distance from the edge (value 0) is the linear distance to the nearest pine forest boundary. Values >0 indicate presence in the grassland linkage, whereas values <0 indicate presence within the forest.
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(Fig. 7d) and Precis dendrophilus) or over it (e.g. Papilio spp., Belenois spp. and Paralethe dendrophilus). Those that flew over had flight patterns that were significantly biased towards the pine-margins adjacent to the larger grassland patches (Table 3). Furthermore, all Papilio species and Paralethe dendrophilus were equally inclined to fly over the pine or natural forest as to fly along its boundary. Therefore, the large, continuous patches of forest appear to be a barrier, even to the highly mobile and frequently migrant butterflies. In contrast, the boundary of the indigenous forest had a greater number of species (Fig. 5) and individuals (Fig. 6) than did the pine forest. Also, the butterflies moved farther into the indigenous forest than into the pine plantation, even though the former was denser.
3.3. Landing sites and landscape barriers Butterflies stopped mostly for nectar, with resting and sunbasking the next most important landing activities (Fig. 8). Boulders and rocks were favoured landing sites for many species (e.g. Precis hierta, Precis octavia, P. orithya, V. cardui, Colias electo and D. chrysippus), especially early and late in the day. Short grasses were favoured landing sites for certain species (e.g. Acraea horta and V. cardui), tall grasses for others (e.g. E. brigitta, L. boeticus, Chrysoritis lycegenes, Hypolimnas misippus and S. spio) and bare ground for others still (e.g. Precis hierta, Precis octavia and Colias electo). After rain, mud puddles became important stopping points. Few butterflies stopped in the mowed or heavily
Table 3 The percentage of individual butterflies leaving the grassland linkages by flying over pine forest boundaries at different distances from the nearest open grassland patch (sample sizes in parentheses) Butterfly species
Distance from grassland patch <20 m
20–50 m
50–100 m
100–250 m
>250 m
X2 (d.f.=4)
Pa
Papilio demodocus Papilio nireus Belenois aurota Belenois creona Paralethe dendrophilus Danaus chrysippus Precis octavia
66 (6) 57 (4) 42 (14) 72 (5) 41 (8) 82 (27) 74 (63)
18 (9) 32 (4) 31 (59) 26 (7) 18 (12) 15 (20) 13 (95)
11 (12) 40 (9) 12 (56) 2 (13) 24 (7) 3 (64) 3 (121)
2 (13) 7 (5) 9 (78) 0 (27) 11 (8) 0 (85) 8 (219)
3 (11) 0 (7) 3 (94) 0 (21) 6 (6) 0 (104) 2 (101)
7.3 5.3 4.7 6.7 3.5 12.4 9.4
<0.01 <0.05 <0.05 <0.001 NS <0.001 <0.01
Mean
6216
228
14 18
8 3
41
7.1
<0.01
a Results of Chi-square tests of independence investigating whether butterflies left the linkage with equal probability through all parts of the perimeter.
Fig. 8. Mean number of butterfly behaviours observed within each linkage width category. The behaviours of observed butterflies were categorised as either flying, reproductive (which included mating swirls, mating and oviposition), nectaring, basking or resting, or other (which included water drinking, mud puddling and territoriality).
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Fig. 9. Proportion of species recorded in each linkage width-category for different disturbance levels. Disturbance included cattle trampling and grazing, mowing, agriculture and human disturbance.
grazed grasslands, although even fewer landed in natural forest. Heavily grazed and mown grasses were a barrier for many species (Fig. 9), except for Acraea horta, which commonly landed and rested among the short grass. Most species moved quickly, without stopping, over or along mown tracks to reach the natural grasslands. Most landings were in the natural grasslands where there were the largest number of nectar sources and oviposition sites. Large dams (>150 m wide) were a barrier to some species (e.g. Acraea horta, S. spio and P. lycegenes), which flew around the edge to get to the other side. However, some other species, especially the large mobile ones (e.g. Papilio spp. and Belenois spp.) flew directly over the water.
4. Discussion This study only assessed how linkages influence dispersal, and did not aim to establish whether these linkages were also habitats that provided all the resources for completing life cycles. Nevertheless, the fact that slow-moving, endemic butterflies occurred within linkages 250 m wide suggests that such linkages permit some residence as well as diffusion of these butterflies of conservation significance. Having conditions suitable for such gradual permeation of the landscape is important, as individuals of relatively sedentary species, such as lycaenids, are unlikely to disperse more than 2 km (Hanski and Kuussaari, 1995).
The four commonest species in this study occurred in most linkages, and are well-known as habitat generalists and migrants. Also, all the large and strong fliers, irrespective of phylogeny, moved relatively independently of habitat type, whether in natural grassland or in alien pines. None of these above species are currently of conservation value. This mirrors the situation with Pieris rapae in Europe, which disperses long distances in random directions (Fahrig and Paloheimo, 1988). Precis hierta and Precis octavia penetrated the first few rows of pine trees. However, as only four species entered the pine compartments, connectivity for these animals clearly would have been much lower in the absence of grassland linkages. Other species flew along (e.g. Cassionympha cassius) or over (e.g. Papilio spp., Belenois spp., Paralethe deudrophilus) the pine trees, indicating that these alien stands are not a complete barrier to some species. Similarly, pine forests are only a partial barrier for the American butterfly Junonia coenia (Haddad, 1999). Movement over unsuitable habitat can have enormous benefits for gene flow, as in the case of the European Proclossiana eunomia (Baguette and Ne`ve, 1994). Most species however, tended to avoid the pines and did not even follow the edges of the compartments as they did along the edges of the natural forest. Although these forest edges are naturally very sharp (Kotze and Samways, 2001) they did not present such a tall and dark wall as did the pines. This was illustrated by the different permeability of the edges, with several more species entering the natural forest than the pine compartments.
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Nevertheless, they often turned back once they had entered the forest. Some species appeared to actually stay clear of the pine (and forest) boundaries, with their densities being higher away from the edges (20 m or so). Similar behaviour has been observed for the threatened American habitat specialist Icaricia icarioides fenderi (Schultz, 1998). In the case of the European Mellicta athalia, even small patches of unsuitable vegetation may have such an influence that they separate subpopulations (Warren, 1987). Many of the butterfly species here, especially those that were relatively tolerant of pines, showed a change in behaviour with habitat. They moved farther and faster along increasingly disturbed grassland linkages, which were acting as movement conduits. This is probably because the increased disturbance levels offered little for most of their life activities, and their behaviour was to rapidly seek more appropriate habitat. A parallel example is that of the sweet potato weevil (Cylas formicarius elagantulus) which moves up to 1000 m in fields without sweet potatoes compared to 500 m in fields with them (Miyatake et al., 1995). In contrast, the wide linkages supported higher densities of butterflies with, slower speeds and more random movements compared with the narrower linkages. Such wide linkages with their high interior to edge ratio, were virtually acting as habitats per se. It is not surprising therefore, that densities were higher in these areas, especially as it is well known that higher insect densities occur in larger patches (Kareiva, 1985; Bach, 1988; Hill et al., 1996). In general, it was clear that the wider natural linkages provided better habitat for the grassland-specialist species, which tended not even to enter the narrow (<50 m) linkages. What are the conservation recommendations that arise from this study? First, we must clearly distinguish between a long, narrow strip of land being only a movement corridor or, on the other hand, having habitat value for permanent living. Secondly, a narrow corridor is inherently less suitable as a habitat because of the influence of neighbouring pines either directly on the insect behaviour or indirectly through influencing the grassland plants, and hence the habitat quality (Samways and Moore, 1991). An additional consideration is that narrow linkages inevitably receive more disturbance than wider linkages given the same amount of human and cattle traffic. The next question that arises is then how wide should a linkage be? Which, of course, rests on having determined the conservation goal. This study shows that any linkage is better than none, but that also the wider the linkage the more value it has for those species of more conservation concern. There reaches a point when the increasing width elevates the linkage from simply a movement corridor to an interconnected habitat. For these butterflies, this figure is 250 m wide. But it is clear that such a habitat linkage
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must be part of greater linkages throughout the landscape. A web of such habitat linkages appears, at least from the information here, to go a long way to reconciling economic production of pines with the conservation of biodiversity.
Acknowledgements We thank Ricky Pott and the field managers of MONDI Goodhope Estate, as well as the farmers in the study area, for practical support. Financial support was provided by MONDI forests, the World Wide Fund for Nature (South Africa). Two anonymous referees and the editor made constructive and stimulating comments. Catherine Murray kindly assisted with final preparation of the manuscript.
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