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Habitat utilization by Lopinga achine (Nymphalidae: Satyrinae) larvae and ovipositing females: implications for conservation
BIOLOGICAL CONSERVATION
Biological Conservation 88 (1999) 69±74
Habitat utilization by Lopinga achine (Nymphalidae: Satyrinae) larvae and ovipositing females: implications for conservation Karl-Olof Bergman* LinkoÈping University, Department of Biology, S-581 83 LinkoÈping, Sweden Received 28 November 1997; received in revised form 27 June 1998; accepted 29 June 1998
Abstract Habitat utilization by larvae and ovipositing females of the red-Databook-listed butter¯y Lopinga achine was studied in partly open woodland in the province of OÈstergoÈtland, Sweden. Egg-laying females and larvae were found to have speci®c habitat requirements, being restricted to a narrow zone along the edges of glades under the tree and bush canopy. This dependence on edges can be ascribed to two factors: ®rst, egg survival was much higher at forest edges, being 48% compared with 12 and 14% in the sun of the open glades and in the shade, respectively. Second, host plant abundance in the shade under the tree and bush canopy is highest near the edge of the glades. The results have important conservation implications. Management to maintain glades and suitable edges is probably necessary for the long-term conservation of L. achine. Numbers of L. achine are probably a function of the area of edge-habitat suitable for oviposition, and the species seems to be sensitive to the amount of tree and bush cover. # 1999 Published by Elsevier Science Ltd. All rights reserved. Keywords: Lopinga achine; Habitat utilization; Larvae; Conservation; Carex montana
1. Introduction During the 20th century, butter¯y populations have declined in Japan, North America and throughout much of Europe, the decrease being especially pronounced over the last 50 years (Pyle, 1976; Heath, 1981; Balletto and Kudrna, 1985; Sibatani, 1990; Pollard and Eversham, 1995). This worldwide trend has led to increased interest in butter¯y conservation. Detailed autoecological studies of threatened butter¯y species are required to enhance conservation eorts (Warren, 1987a±c; Bourn and Thomas, 1993; Ravenscroft, 1994b; Thomas, 1995). Indeed, there are examples of where conservation work not based on ecological studies has failed (Thomas, 1984). In general, research has shown that the larval and egg stages of butter¯ies are more specialized than previously suspected. Females are selective during oviposition and use a small number of host plants in speci®c growthforms or microhabitats. In all other respects, however, the adults seemed to have less speci®c habitat requirements (Thomas, 1991). Thus, the habitat requirements * Fax: +46-13-282-611; e-mail: [email protected].
of egg-laying females and larvae should be considered to be an important aspect of butter¯y conservation studies. Lopinga achine Scopoli (Nymphalidae: Satyrinae) is one of the threatened butter¯ies with poorly known habitat requirements (van Helsdingen et al., 1996). It is classi®ed as vulnerable in the Swedish Red data book (EhnstroÈm et al., 1993). The species is threatened over large parts of Western Europe and has disappeared from many sites (Heath, 1981; Bink, 1992; van Helsdingen et al., 1996, Buszko, pers. comm.). It is included in the Bern Convention list (Council of Europe, 1993) of endangered ¯ora and fauna in Europe and in the Habitats Directive (Annex IV) (van Helsdingen et al., 1996). The species seems to occur locally, and with long distances between populations, throughout its distribution area from southern Fennoscandia through Central Europe to North and Central Asia and Japan (Kudrna, 1986; van Helsdingen et al., 1996). In Sweden it inhabits two regions: the province of OÈstergoÈtland (Fig. 1), where I have been studying it, and the island of Gotland in the Baltic (Henriksen and Kreutzer, 1982). In OÈstergoÈtland, the larvae of L. achine live mainly (>80% in ®eld counts) on a single host plant, Carex
0006-3207/99/$Ðsee front matter # 1999 Published by Elsevier Science Ltd. All rights reserved. PII: S0006 -3 207(98)00088 -3
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K.-O. Bergman / Biological Conservation 88 (1999) 69±74
Fig. 1. (a) The location of the 49 mainland populations of Lopinga achine in the province of OÈstergoÈtland, Sweden. (b) A map of the main study area, the largest mainland population, showing the typical vegetation structure of a L. achine site. Black is forested areas and white is open glades.
montana (Cyperaceae) (Bergman, unpublished). However, knowledge about the host-plant range of a species does not provide sucient basis for developing appropriate conservation measures. For instance, most of the host plants of Britain's butter¯ies have wider geographical ranges and extend further north than do the butter¯ies (Dennis and Shreeve, 1991). This indicates that factors other than host plant occurrence are important for butter¯y distribution. The aim of this work was to study how L. achine larvae and ovipositing females utilize their habitat, and to determine the habitat requirements. This knowledge should facilitate eorts to preserve the species, including the development of guidelines for managing sites where it occurs.
2.2. Oviposition
2. Materials and methods
In and around glades where adults were numerous, I systematically searched plants in the families Poaceae, Juncaceae and Cyperaceae for larvae. These surveys were made in randomly selected transects running perpendicular to the edges of the glades (Fig. 1). Along these transects 12 contiguous 1-m2 quadrats were checked for larvae, six in the open and six under tree/ bush canopy. These transect surveys were made in four populations between 20 September and 3 October 1990. In total, 63 transects were surveyed, comprising 756 m2. Furthermore, host plants within a 1-m2 area under each of 23 bushes growing in the open were examined. The following spring (22 May±6 June 1991), searches were made for larvae around areas where they had been found in the autumn, covering 46 transects (552 m2) and 20 bushes. The percentage cover of Carex montana was also estimated at ®ve sites along 48 randomly selected transects (576 m2) and in one quadrat under each of 20 bushes growing singly in the open.
2.1. Study animal and study site Lopinga achine ¯ies in one generation in June±July and hibernates in the larval stage. In OÈstergoÈtland the butter¯y frequents glades in partly open oak woodland Quercus robur L. with hazel Corylus avellana L. (Fig. 1). If left undisturbed, the successional stage constituting the habitat lasts 30±50 years until closure of the canopy. The habitat on Gotland is dierent, being partly open coniferous forest with a well-developed scrub layer of Frangula alnus Mill., Sorbus aucuparia L., S. intermedia (Ehrh.) Pers. and Juniperus communis L. Forty-nine populations are known in OÈstergoÈtland, most of which exchange small numbers of migrants according to mark± recapture studies (Bergman, unpublished). The surroundings are usually open ®elds or spruce plantations. Most populations are small, consisting of some hundreds of adults (Bergman, unpublished). Three populations comprise >1000 adults.
Ovipositing females were followed in the ®eld in areas of high adult density. I used binoculars to observe the females without disturbing them. Immediately after oviposition the exact spot was marked, and the distance to the edge of the nearest glade was measured. Oviposition sites were grouped in zones 1 m wide in relation to the distance to the edge. Most of the observations (48 out of 84 egg-layings) were made in the largest population and the rest in nine other populations. 2.3. Larval habitat utilization and occurrence of Carex montana
K.-O. Bergman / Biological Conservation 88 (1999) 69±74
2.4. Egg survival in the ®eld Eggs were obtained in the laboratory from freshly collected females. To estimate egg survival in the ®eld 176 newly laid eggs from 13 females and two populations were placed in three dierent environments in a glade where ovipositing females had been observed. Fifty-eight eggs were placed in a sun-exposed position 3±6 m from the edge of the glade, 61 along the edge, 0.2±0.5 m under the tree and bush canopy, and 57 in the shade under the tree/bush canopy, 2±5 m from the edge. Females drop their eggs on the ground, so the eggs were placed singly on hazel leaves attached as close to the ground as possible with a needle and touching the surrounding vegetation to mimic natural conditions and to allow predation. The eggs were checked daily. Hatching was considered to have de®nitely occurred in cases where the larva was found or small pieces of eggshell, typical of hatched eggs, were observed. Hatching was considered probable where the egg remained, with the larva visible through the shell until the due hatching date, but no egg-shell remains were found. Predation was assumed where pieces of egg were found before it should have hatched. Predation was considered probable in cases where an egg disappeared before the estimated time of hatching, but no pieces of egg were found. Egg losses through factors other than predation were considered to be small. Eggs were considered to have died from dehydration if their shells crumpled.
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Anity for edges was found for the larvae with 60 out of 97 found in this 2-m zone in the autumn and 38 out of 86 (44%) in the spring. These distributions dier signi®cantly from even distributions along the transects perpendicular to the edges ( w2=188.4 and 112.4, respectively, df=11, p=0.0001). To test the distribution of ovipositions against the larval distribution across the edges of the glades, the data were grouped into ®ve zones: 0±6 m from the edges in the open area of the glade and 0±1, 1±2, 2±3 and 3±6 m from the edge in the woodland area. The distribution of ovipositions did not dier signi®cantly from that of larvae in either spring or autumn ( w2=8.26, df=4, NS and w2=2.01, df=4, NS). However, the distributions of autumn and spring larvae diered signi®cantly from each other ( w2=14.74, df=4, p=0.005) (Fig. 2). The density of the host plant C. montana was highest around the edges of the glades (Fig. 3). There were signi®cant dierences in the cover of C. montana between
2.5. Egg survival and relative humidity Egg hatching in the laboratory was followed at four dierent relative humidities (RH 50, 80, 90, 100%) controlled by adjusting the concentration of aqueous KOH-solutions in sealed containers (Solomon, 1951). Thirty 2-day-old eggs were placed in each container.
Fig. 2. Number of ovipositions and numbers of larvae of Lopinga achine during September±October 1990 and May±June 1991, at different distances from the nearest edge of glades. The area >6 m into the closed wood was checked for eggs but not for larvae. ``Single bush'' refers to single bushes in the open glade.
3. Results 3.1. Oviposition, larval habitat utilization and occurrence of C. montana Eighty-four ovipositions were observed in the ®eld. All females observed ovipositing did so sitting on plants, even though they drop the eggs to the ground without attaching their eggs to any plant. The females showed a strong anity for the edges of the glades. Forty-four (52%) of the ovipositions occurred in a 2-mwide zone from the edge of the tree/bush (Fig. 2). Only 10 (12%) ovipositions occurred in the open part of the glades, and three occurred under single bushes. This frequency distribution diers signi®cantly from an even distribution in relation to the distance from the edge of the glade (w2=122.9, df=11, p=0.0001).
Fig. 3. Ground cover of Carex montana at dierent distances from edges of glades. ``Single bush'' refers to single bushes in the open glade.
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K.-O. Bergman / Biological Conservation 88 (1999) 69±74
quadrats along the transects (one-way ANOVA: F=3.929, df=11,564, p<0.0001). Correlations between C. montana cover and numbers of ovipositions and larvae, respectively, were tested separately for the open areas and closed areas. Numbers of ovipositions and the occurrence of autumn and spring larvae were each closely correlated with the cover of C. montana within the 6-m section of transect under the tree/bush canopy (r=0.95, p=0.0029; r=0.96, p=0.0027; r=0.82, p=0.046). There was no correlation between C. montana cover and ovipositions or autumn larvae in the open area stretching 6 m outwards from the edge, whereas the number of spring larva was correlated with the cover of C. montana (r=0.97, p=0.0008). However, only 13 (15%) of the spring larva and 3 (3%) of the autumn larva occurred in the open area (Fig. 2). Numbers of ovipositions and larvae under isolated bushes in the open glades were not analyzed statistically. 3.2. Egg survival in the ®eld and laboratory The survival of eggs placed along the edges (48%) diered signi®cantly from that of the sun-exposed eggs (14%) and eggs in the shade (12%) (Fig. 4) (w2=25.33, df=2, p=0.0001). Mortality factors also diered between areas. The proportion of eggs that had died from desiccation was higher in the sun-exposed areas (48%) than at the edge (9%) and in the shade (0%). The high mortality in the shade was due, instead, to predation (98% of the dead eggs), whereas predation accounted for 84% of the egg mortality along the edge and 48% in the sun (Fig. 4). The mean time to hatching diered signi®cantly between the three environments and was longest in the shade (17.1 days), intermediate at the edge (15.6 days) and shortest in the sun (14.6 days) (one-way ANOVA: F=11.86, df=2,41, p<0.0001).
Fig. 4. Survival and mortality of Lopinga achine eggs in ®eld experiments in three dierent environments in partly open woodland (sun exposed, 58 eggs; glade edges, 61 eggs; inside wood, 57 eggs).
These hatching times diered signi®cantly from each other in all three pairwise combinations (sun exposed vs edge, p=0.047; sun exposed vs shade, p<0.0001; edge vs shade, p=0.004; ScheeÂ's F post-hoc test). In the laboratory, egg survival diered between dry and humid conditions ( w2=63.44, df=3, p=0.0001). Almost all of the eggs survived (>93%) at 80, 90 and 100% relative humidity, whereas survival was only 27% at 50% relative humidity. 4. Discussion In north-western Europe L. achine inhabits partly open woodland where it ¯ies in the glades (Lepidopterologen-Arbeitsgruppe, 1988; Ebert and Rennwald, 1991; Bink, 1992; van Helsdingen et al., 1996). My study suggests that it has speci®c habitat requirements that in most cases can only be met along the edges of the glades where the females prefer to lay their eggs (Fig. 2). Even though its primary host plant, Carex montana, also occurs in the open areas of the glades (Fig. 3) only 3±15% of the ovipositions and larva occur there. The fact that there was a good correlation between C. montana cover and number of ovipositions and autumn larval occurrence for the transect section under the tree/ bush canopy, and no correlation in the open area, indicates that factors other than host plant abundance also govern habitat utilization. This is in line with the results of other studies where threatened or rare butter¯ies depend on host plants growing under speci®c conditions. For instance, some species depend on close-cropped swards and warm microclimates (Thomas, 1983a; Thomas et al., 1986), whereas others depend on longer swards (Thomas, 1983b) or dierent levels of tree and bush cover (Pollard, 1979; Warren, 1987a; Sparks et al., 1994). Butter¯y numbers in a given area are often related to the abundance of host plants growing under the right conditions rather than to the total abundance of host plants (Bourn and Thomas, 1993). This may explain extinctions on sites where host plants are still abundant. In Suolk, 42% of the butter¯y species have become extinct as compared with ``only'' 5% of the vascular plants (Thomas, 1991). Five populations of L. achine in OÈstergoÈtland disappeared during the 1960s and 1970s, probably because the sites became too overgrown, resulting in the disappearance of glades and edges. The host plant, C. montana, is still present at these sites. Similarly, in OÈstergoÈtland L. achine has not been found colonizing areas with C. montana where trees and bushes are absent. Therefore, it is probable that the abundance of L. achine is related to the area of edge habitat suitable for egg-laying and that the butter¯y is sensitive to speci®c successional stages in the vegetation. Declines of L. achine in Baden-WuÈrttemberg and
K.-O. Bergman / Biological Conservation 88 (1999) 69±74
Switzerland have also been attributed to vegetational succession, the closure of open woodlands and the establishment of spruce plantations (LepidopterologenArbeitsgruppe, 1988; Ebert and Rennwald, 1991). The extinction of Carterocephalus palaemon in England, another butter¯y preferring edges, was attributed to canopy closure in the woodland (Warren, 1991; Ravenscroft, 1994a). One reason for the dependence of L. achine on edges may be that egg survival is higher at edges than in the sun or under the shade of a closed bush/tree canopy, according to my ®eld experiments (Fig. 4). The main mortality factor for the sun-exposed eggs seemed to be desiccation. However, some of the naturally dropped eggs may fall into crevices with greater humidity than the experiment eggs experienced, so the desiccation mortality may be somewhat overestimated. Laboratory experiments con®rmed that the eggs of L. achine are sensitive to dry conditions and they have been shown to be more vulnerable to desiccation than the eggs of four other satyrines at 30% relative humidity (Karlsson and Wiklund, 1985): 100% in L. achine, up to 15% in three Lasiommata species and 29% in Pararge aegeria. The eggs of L. achine have a high number of aeropyles (tiny openings in the egg shell) (GarcõÂa-Barros and MartõÂn, 1995), which may be the reason for the low resistance to desiccation (GarcõÂa-Barros, pers. comm.). Judging from my results it seems that even commonly occurring relative humidities of 50±60% can cause considerable egg mortality. Although predation was high in all three environments, it was highest within the wood, where it was the main egg mortality factor (Fig. 4). The longer development time there may be one reason for the higher predation rate, but other factors, such as predator abundance, are probably also involved. However, no observations were done on the predators involved. These results suggest that the anity of L. achine for glade edges may be ascribed to two factors: (1) host plant abundance in the shade under the tree and bush canopy is highest near the edge of the glades; and (2) selection against oviposition in the sun as well as in the shade due to high egg mortality. In a similar way, Stephanitis pyrioides (Hemiptera) avoids low survival in open sunny habitats and in shaded habitats by preferentially colonizing plants growing in partial shade (Trumbule and Denno, 1995). 4.1. Conservation implications Detailed ecological studies that identify key environmental variables are a prerequisite for success of butter¯y conservation eorts (Murphy et al., 1990). To preserve L. achine it is clearly important to maintain suitable glades containing C. montana by grazing or clearing at regular intervals to prevent closure. To
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improve overgrown sites of L. achine, I suggest that small clearings (10±30 m in diameter) should be created, wide enough to allow the sun to reach ground and with C. montana at the edges. On the other hand, areas with few trees and bushes are not suitable for L. achine either, so too many clearings may be harmful. Thus it may be necessary to maintain a delicate balance in this respect. To provide more eective management guidelines than described here for preserving L. achine populations, it may be necessary to study the structure of trees and bushes to understand the optimal openness of a site for L. achine. Long-term population dynamics are probably determined by the degree of openness of the site and the amount of suitable edge habitat.
Acknowledgements This work was supported by the World Wide Fund for Nature, ``Eklandskapsfonden'', the Swedish Environmental Protection Agency and LinkoÈping University. I wish to thank Jan Landin for useful comments and Eva Enquist for statistical advice. References Balletto, E., Kudrna, O., 1985. Some aspects of the conservation of butter¯ies in Italy, with recommendations for a future strategy. Bolletino delta Societa entomologica italiana 117, 39±59. Bink, F.A., 1992. Ecologische atlas van de dagvlinders van Noordwest-Europa. Schuyt & Co, Haarlem, The Netherlands. Bourn, N.A.D., Thomas, J.A., 1993. The ecology and conservation of the brown argus butter¯y Aricia agestis in Britain. Biological Conservation 63, 67±74. Council of Europe, 1993. Convention on the Conservation of European Wildlife and Natural Habitats. Appendices to the Convention. Secretariat Memorandum prepared by the directorate of environment and local authorities. Council of Europe Publishing, Strasbourg. Dennis, R.L.H., Shreeve, T.G., 1991. Climatic change and the British butter¯y fauna: opportunities and constraints. Biological Conservation 55, 1±16. Ebert, G., Rennwald, E., 1991. Die schmetterlinge Baden-WuÈrttembergs 2. Ulmer Verlag, Stuttgart. EhnstroÈm, B., GaÈrdenfors, U., LindeloÈw, AÊ., 1993. RoÈdlistade evertebrater i Sverige 1993. Databanken foÈr hotade arter, Uppsala. GarcõÂa-Barros, E., MartõÂn, J., 1995. The eggs of European satyrine butter¯ies (Nymphalidae): external morphology and its use in systematics. Zoological Journal of the Linnean Society 115, 73±115. Heath, J., 1981. Threatened Rhopalocera (Butter¯ies) in Europe. Nature and Envirorunent Series no. 23. Council of Europe Publishing, Strasbourg. Henriksen, H.J., Kreutzer, I., 1982. The butter¯ies of Scandinavia in nature. Skandinavisk bogfoÈrlag, Odense. Karlsson, B., Wiklund, C., 1985. Egg weight variation in relation to egg mortality and starvation endurance of newly hatched larvae in some satyrid butter¯ies. Ecological Entomology 10, 205±211. Kudrna, O., 1986. Aspects of the conservation of butter¯ies in Europe. Aula Verlag, Wiesbaden, Germany.
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Lepidopterologen-Arbeitsgruppe, 1988. Tagfalter und ihre LebensraÈume. Basel & Fotorotar AG, Basel. Murphy, D.D., Freas, K.E., Weiss, S.B., 1990. An environment± metapopulation approach to population viability analysis for a threatened invertebrate. Conservation Biology 4, 41±51. Pollard, E., 1979. Population ecology and change in range of the white admiral butter¯y Ladoga camilla L. in England. Ecological Entomology 4, 61±74. Pollard, E., Eversham, B.C., 1995. Butter¯y monitoring 2Ðinterpreting the changes. In: Pullin, A.S. (Ed.), Ecology and Conservation of Butter¯ies. Chapman and Hall, London, pp. 23±36. Pyle, R.M., 1976. Conservation of Lepidoptera in the United States. Biological Conservation 9, 55±75. Ravenscroft, N.O.M., 1994a. The ecology of the chequered skipper Carterocephalus palaemon in Scotland. I. Microhabitat. Journal of Applied Ecology 31, 613±622. Ravenscroft, N.O.M., 1994b. The ecology of the chequered skipper Carterocephalus palaemon in Scotland. II. Food plant quality and population range. Journal of Applied Ecology 31, 623±630. Sibatani, A., 1990. Decline and conservation of butter¯ies in Japan. Journal of Research on the Lepidoptera 29, 305±315. Solomon, M.E., 1951. Control of humidity with potassium hydroxide, sulphuric acid and other solutions. Bulletin of Entomological Research 42, 543±554. Sparks, T.H., Porter, K., Greatorex-Davies, J.N., Hall, M.L., Marrs, R.H., 1994. The choice of oviposition sites in woodland by the Duke of Burgundy butter¯y Hamaeris lucina in England. Biological Conservation 70, 257±264. Thomas, J.A., 1983a. The ecology and conservation of Lysandra bellargus (Lepidoptera: Lycaenidae) in Britain. Journal of Applied Ecology 20, 59±83. Thomas, J.A., 1983b. The ecology and status of Thymelicus acteon (Lepidoptera: Hesperiidae) in Britain. Ecological Entomology 8, 427±435. Thomas, J.A., 1984. The conservation of butter¯ies in temperate countries: past eorts and lessons for the future. In: Vane-Wright, R.I., Ackery, P.R. (Eds.), Biology of Butter¯ies: Symposium of the
Royal Entomological Society of London No. 11. Academic Press, London, pp. 333±353. Thomas, J.A., 1991. Rare species conservation: case studies of European butter¯ies. In: Spellerberg, I.F., Goldsmith, F.B., Morris, M.G. (Eds.), The Scienti®c Management of Temperate Communities for Conservation. Blackwell Scienti®c Publications, Oxford, pp. 149±197. Thomas, J.A., 1995. The ecology and conservation of Maculinea arion and other European species of large blue butter¯y. In: Pullin, A.S. (Ed.), Ecology and Conservation of Butter¯ies. Chapman and Hall, London, pp. 180±197. Thomas, J.A., Thomas, C.D., Simcox, D.J., Clarke, R.T., 1986. Ecology and declining status of the silver-spotted skipper butter¯y (Hesperia comma) in Britain. Journal of Applied Ecology 23, 472± 481. Trumbule, R.B., Denno, R.F., 1995. Light intensity, host-plant irrigation, and habitat-related mortality as determinants of the abundance of azalea lace bug (Heteroptera: Tingidae). Environmental Entomology 24, 898±908. van Helsdingen, P.J., Willemse, L., Speight, M.C.D., 1996. Background Information on Invertebrates of the Habitats Directive and the Bern Convention. Part 1: Crustacea, Coleoptera and Lepidoptera. Council of Europe. Nature and Environment Series no. 79. Council of Europe Publishing, Strasbourg. Warren, M.S., 1987a. The ecology and conservation of the heath fritillary butter¯y, Mellicta athalia. I. Host selection and phenology. Journal of Applied Ecology 24, 467±482. Warren, M.S., 1987b. The ecology and conservation of the heath fritillary butter¯y Mellicta athalia. II. Adult population structure and mobility. Journal of Applied Ecology 24, 483±498. Warren, M.S., 1987c. The ecology and conservation of the heath fritillary butter¯y, Mellicta athalia. III. Population dynamics and the eect of habitat management. Journal of Applied Ecology 24, 499± 513. Warren, M.S., 1991. The chequered skipper, Carterocephalus palaemon, in northern Europe. British Butter¯y Conservation Society Occasional Paper no. 2, Colchester.
Biological Conservation 88 (1999) 69±74
Habitat utilization by Lopinga achine (Nymphalidae: Satyrinae) larvae and ovipositing females: implications for conservation Karl-Olof Bergman* LinkoÈping University, Department of Biology, S-581 83 LinkoÈping, Sweden Received 28 November 1997; received in revised form 27 June 1998; accepted 29 June 1998
Abstract Habitat utilization by larvae and ovipositing females of the red-Databook-listed butter¯y Lopinga achine was studied in partly open woodland in the province of OÈstergoÈtland, Sweden. Egg-laying females and larvae were found to have speci®c habitat requirements, being restricted to a narrow zone along the edges of glades under the tree and bush canopy. This dependence on edges can be ascribed to two factors: ®rst, egg survival was much higher at forest edges, being 48% compared with 12 and 14% in the sun of the open glades and in the shade, respectively. Second, host plant abundance in the shade under the tree and bush canopy is highest near the edge of the glades. The results have important conservation implications. Management to maintain glades and suitable edges is probably necessary for the long-term conservation of L. achine. Numbers of L. achine are probably a function of the area of edge-habitat suitable for oviposition, and the species seems to be sensitive to the amount of tree and bush cover. # 1999 Published by Elsevier Science Ltd. All rights reserved. Keywords: Lopinga achine; Habitat utilization; Larvae; Conservation; Carex montana
1. Introduction During the 20th century, butter¯y populations have declined in Japan, North America and throughout much of Europe, the decrease being especially pronounced over the last 50 years (Pyle, 1976; Heath, 1981; Balletto and Kudrna, 1985; Sibatani, 1990; Pollard and Eversham, 1995). This worldwide trend has led to increased interest in butter¯y conservation. Detailed autoecological studies of threatened butter¯y species are required to enhance conservation eorts (Warren, 1987a±c; Bourn and Thomas, 1993; Ravenscroft, 1994b; Thomas, 1995). Indeed, there are examples of where conservation work not based on ecological studies has failed (Thomas, 1984). In general, research has shown that the larval and egg stages of butter¯ies are more specialized than previously suspected. Females are selective during oviposition and use a small number of host plants in speci®c growthforms or microhabitats. In all other respects, however, the adults seemed to have less speci®c habitat requirements (Thomas, 1991). Thus, the habitat requirements * Fax: +46-13-282-611; e-mail: [email protected].
of egg-laying females and larvae should be considered to be an important aspect of butter¯y conservation studies. Lopinga achine Scopoli (Nymphalidae: Satyrinae) is one of the threatened butter¯ies with poorly known habitat requirements (van Helsdingen et al., 1996). It is classi®ed as vulnerable in the Swedish Red data book (EhnstroÈm et al., 1993). The species is threatened over large parts of Western Europe and has disappeared from many sites (Heath, 1981; Bink, 1992; van Helsdingen et al., 1996, Buszko, pers. comm.). It is included in the Bern Convention list (Council of Europe, 1993) of endangered ¯ora and fauna in Europe and in the Habitats Directive (Annex IV) (van Helsdingen et al., 1996). The species seems to occur locally, and with long distances between populations, throughout its distribution area from southern Fennoscandia through Central Europe to North and Central Asia and Japan (Kudrna, 1986; van Helsdingen et al., 1996). In Sweden it inhabits two regions: the province of OÈstergoÈtland (Fig. 1), where I have been studying it, and the island of Gotland in the Baltic (Henriksen and Kreutzer, 1982). In OÈstergoÈtland, the larvae of L. achine live mainly (>80% in ®eld counts) on a single host plant, Carex
0006-3207/99/$Ðsee front matter # 1999 Published by Elsevier Science Ltd. All rights reserved. PII: S0006 -3 207(98)00088 -3
70
K.-O. Bergman / Biological Conservation 88 (1999) 69±74
Fig. 1. (a) The location of the 49 mainland populations of Lopinga achine in the province of OÈstergoÈtland, Sweden. (b) A map of the main study area, the largest mainland population, showing the typical vegetation structure of a L. achine site. Black is forested areas and white is open glades.
montana (Cyperaceae) (Bergman, unpublished). However, knowledge about the host-plant range of a species does not provide sucient basis for developing appropriate conservation measures. For instance, most of the host plants of Britain's butter¯ies have wider geographical ranges and extend further north than do the butter¯ies (Dennis and Shreeve, 1991). This indicates that factors other than host plant occurrence are important for butter¯y distribution. The aim of this work was to study how L. achine larvae and ovipositing females utilize their habitat, and to determine the habitat requirements. This knowledge should facilitate eorts to preserve the species, including the development of guidelines for managing sites where it occurs.
2.2. Oviposition
2. Materials and methods
In and around glades where adults were numerous, I systematically searched plants in the families Poaceae, Juncaceae and Cyperaceae for larvae. These surveys were made in randomly selected transects running perpendicular to the edges of the glades (Fig. 1). Along these transects 12 contiguous 1-m2 quadrats were checked for larvae, six in the open and six under tree/ bush canopy. These transect surveys were made in four populations between 20 September and 3 October 1990. In total, 63 transects were surveyed, comprising 756 m2. Furthermore, host plants within a 1-m2 area under each of 23 bushes growing in the open were examined. The following spring (22 May±6 June 1991), searches were made for larvae around areas where they had been found in the autumn, covering 46 transects (552 m2) and 20 bushes. The percentage cover of Carex montana was also estimated at ®ve sites along 48 randomly selected transects (576 m2) and in one quadrat under each of 20 bushes growing singly in the open.
2.1. Study animal and study site Lopinga achine ¯ies in one generation in June±July and hibernates in the larval stage. In OÈstergoÈtland the butter¯y frequents glades in partly open oak woodland Quercus robur L. with hazel Corylus avellana L. (Fig. 1). If left undisturbed, the successional stage constituting the habitat lasts 30±50 years until closure of the canopy. The habitat on Gotland is dierent, being partly open coniferous forest with a well-developed scrub layer of Frangula alnus Mill., Sorbus aucuparia L., S. intermedia (Ehrh.) Pers. and Juniperus communis L. Forty-nine populations are known in OÈstergoÈtland, most of which exchange small numbers of migrants according to mark± recapture studies (Bergman, unpublished). The surroundings are usually open ®elds or spruce plantations. Most populations are small, consisting of some hundreds of adults (Bergman, unpublished). Three populations comprise >1000 adults.
Ovipositing females were followed in the ®eld in areas of high adult density. I used binoculars to observe the females without disturbing them. Immediately after oviposition the exact spot was marked, and the distance to the edge of the nearest glade was measured. Oviposition sites were grouped in zones 1 m wide in relation to the distance to the edge. Most of the observations (48 out of 84 egg-layings) were made in the largest population and the rest in nine other populations. 2.3. Larval habitat utilization and occurrence of Carex montana
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2.4. Egg survival in the ®eld Eggs were obtained in the laboratory from freshly collected females. To estimate egg survival in the ®eld 176 newly laid eggs from 13 females and two populations were placed in three dierent environments in a glade where ovipositing females had been observed. Fifty-eight eggs were placed in a sun-exposed position 3±6 m from the edge of the glade, 61 along the edge, 0.2±0.5 m under the tree and bush canopy, and 57 in the shade under the tree/bush canopy, 2±5 m from the edge. Females drop their eggs on the ground, so the eggs were placed singly on hazel leaves attached as close to the ground as possible with a needle and touching the surrounding vegetation to mimic natural conditions and to allow predation. The eggs were checked daily. Hatching was considered to have de®nitely occurred in cases where the larva was found or small pieces of eggshell, typical of hatched eggs, were observed. Hatching was considered probable where the egg remained, with the larva visible through the shell until the due hatching date, but no egg-shell remains were found. Predation was assumed where pieces of egg were found before it should have hatched. Predation was considered probable in cases where an egg disappeared before the estimated time of hatching, but no pieces of egg were found. Egg losses through factors other than predation were considered to be small. Eggs were considered to have died from dehydration if their shells crumpled.
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Anity for edges was found for the larvae with 60 out of 97 found in this 2-m zone in the autumn and 38 out of 86 (44%) in the spring. These distributions dier signi®cantly from even distributions along the transects perpendicular to the edges ( w2=188.4 and 112.4, respectively, df=11, p=0.0001). To test the distribution of ovipositions against the larval distribution across the edges of the glades, the data were grouped into ®ve zones: 0±6 m from the edges in the open area of the glade and 0±1, 1±2, 2±3 and 3±6 m from the edge in the woodland area. The distribution of ovipositions did not dier signi®cantly from that of larvae in either spring or autumn ( w2=8.26, df=4, NS and w2=2.01, df=4, NS). However, the distributions of autumn and spring larvae diered signi®cantly from each other ( w2=14.74, df=4, p=0.005) (Fig. 2). The density of the host plant C. montana was highest around the edges of the glades (Fig. 3). There were signi®cant dierences in the cover of C. montana between
2.5. Egg survival and relative humidity Egg hatching in the laboratory was followed at four dierent relative humidities (RH 50, 80, 90, 100%) controlled by adjusting the concentration of aqueous KOH-solutions in sealed containers (Solomon, 1951). Thirty 2-day-old eggs were placed in each container.
Fig. 2. Number of ovipositions and numbers of larvae of Lopinga achine during September±October 1990 and May±June 1991, at different distances from the nearest edge of glades. The area >6 m into the closed wood was checked for eggs but not for larvae. ``Single bush'' refers to single bushes in the open glade.
3. Results 3.1. Oviposition, larval habitat utilization and occurrence of C. montana Eighty-four ovipositions were observed in the ®eld. All females observed ovipositing did so sitting on plants, even though they drop the eggs to the ground without attaching their eggs to any plant. The females showed a strong anity for the edges of the glades. Forty-four (52%) of the ovipositions occurred in a 2-mwide zone from the edge of the tree/bush (Fig. 2). Only 10 (12%) ovipositions occurred in the open part of the glades, and three occurred under single bushes. This frequency distribution diers signi®cantly from an even distribution in relation to the distance from the edge of the glade (w2=122.9, df=11, p=0.0001).
Fig. 3. Ground cover of Carex montana at dierent distances from edges of glades. ``Single bush'' refers to single bushes in the open glade.
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quadrats along the transects (one-way ANOVA: F=3.929, df=11,564, p<0.0001). Correlations between C. montana cover and numbers of ovipositions and larvae, respectively, were tested separately for the open areas and closed areas. Numbers of ovipositions and the occurrence of autumn and spring larvae were each closely correlated with the cover of C. montana within the 6-m section of transect under the tree/bush canopy (r=0.95, p=0.0029; r=0.96, p=0.0027; r=0.82, p=0.046). There was no correlation between C. montana cover and ovipositions or autumn larvae in the open area stretching 6 m outwards from the edge, whereas the number of spring larva was correlated with the cover of C. montana (r=0.97, p=0.0008). However, only 13 (15%) of the spring larva and 3 (3%) of the autumn larva occurred in the open area (Fig. 2). Numbers of ovipositions and larvae under isolated bushes in the open glades were not analyzed statistically. 3.2. Egg survival in the ®eld and laboratory The survival of eggs placed along the edges (48%) diered signi®cantly from that of the sun-exposed eggs (14%) and eggs in the shade (12%) (Fig. 4) (w2=25.33, df=2, p=0.0001). Mortality factors also diered between areas. The proportion of eggs that had died from desiccation was higher in the sun-exposed areas (48%) than at the edge (9%) and in the shade (0%). The high mortality in the shade was due, instead, to predation (98% of the dead eggs), whereas predation accounted for 84% of the egg mortality along the edge and 48% in the sun (Fig. 4). The mean time to hatching diered signi®cantly between the three environments and was longest in the shade (17.1 days), intermediate at the edge (15.6 days) and shortest in the sun (14.6 days) (one-way ANOVA: F=11.86, df=2,41, p<0.0001).
Fig. 4. Survival and mortality of Lopinga achine eggs in ®eld experiments in three dierent environments in partly open woodland (sun exposed, 58 eggs; glade edges, 61 eggs; inside wood, 57 eggs).
These hatching times diered signi®cantly from each other in all three pairwise combinations (sun exposed vs edge, p=0.047; sun exposed vs shade, p<0.0001; edge vs shade, p=0.004; ScheeÂ's F post-hoc test). In the laboratory, egg survival diered between dry and humid conditions ( w2=63.44, df=3, p=0.0001). Almost all of the eggs survived (>93%) at 80, 90 and 100% relative humidity, whereas survival was only 27% at 50% relative humidity. 4. Discussion In north-western Europe L. achine inhabits partly open woodland where it ¯ies in the glades (Lepidopterologen-Arbeitsgruppe, 1988; Ebert and Rennwald, 1991; Bink, 1992; van Helsdingen et al., 1996). My study suggests that it has speci®c habitat requirements that in most cases can only be met along the edges of the glades where the females prefer to lay their eggs (Fig. 2). Even though its primary host plant, Carex montana, also occurs in the open areas of the glades (Fig. 3) only 3±15% of the ovipositions and larva occur there. The fact that there was a good correlation between C. montana cover and number of ovipositions and autumn larval occurrence for the transect section under the tree/ bush canopy, and no correlation in the open area, indicates that factors other than host plant abundance also govern habitat utilization. This is in line with the results of other studies where threatened or rare butter¯ies depend on host plants growing under speci®c conditions. For instance, some species depend on close-cropped swards and warm microclimates (Thomas, 1983a; Thomas et al., 1986), whereas others depend on longer swards (Thomas, 1983b) or dierent levels of tree and bush cover (Pollard, 1979; Warren, 1987a; Sparks et al., 1994). Butter¯y numbers in a given area are often related to the abundance of host plants growing under the right conditions rather than to the total abundance of host plants (Bourn and Thomas, 1993). This may explain extinctions on sites where host plants are still abundant. In Suolk, 42% of the butter¯y species have become extinct as compared with ``only'' 5% of the vascular plants (Thomas, 1991). Five populations of L. achine in OÈstergoÈtland disappeared during the 1960s and 1970s, probably because the sites became too overgrown, resulting in the disappearance of glades and edges. The host plant, C. montana, is still present at these sites. Similarly, in OÈstergoÈtland L. achine has not been found colonizing areas with C. montana where trees and bushes are absent. Therefore, it is probable that the abundance of L. achine is related to the area of edge habitat suitable for egg-laying and that the butter¯y is sensitive to speci®c successional stages in the vegetation. Declines of L. achine in Baden-WuÈrttemberg and
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Switzerland have also been attributed to vegetational succession, the closure of open woodlands and the establishment of spruce plantations (LepidopterologenArbeitsgruppe, 1988; Ebert and Rennwald, 1991). The extinction of Carterocephalus palaemon in England, another butter¯y preferring edges, was attributed to canopy closure in the woodland (Warren, 1991; Ravenscroft, 1994a). One reason for the dependence of L. achine on edges may be that egg survival is higher at edges than in the sun or under the shade of a closed bush/tree canopy, according to my ®eld experiments (Fig. 4). The main mortality factor for the sun-exposed eggs seemed to be desiccation. However, some of the naturally dropped eggs may fall into crevices with greater humidity than the experiment eggs experienced, so the desiccation mortality may be somewhat overestimated. Laboratory experiments con®rmed that the eggs of L. achine are sensitive to dry conditions and they have been shown to be more vulnerable to desiccation than the eggs of four other satyrines at 30% relative humidity (Karlsson and Wiklund, 1985): 100% in L. achine, up to 15% in three Lasiommata species and 29% in Pararge aegeria. The eggs of L. achine have a high number of aeropyles (tiny openings in the egg shell) (GarcõÂa-Barros and MartõÂn, 1995), which may be the reason for the low resistance to desiccation (GarcõÂa-Barros, pers. comm.). Judging from my results it seems that even commonly occurring relative humidities of 50±60% can cause considerable egg mortality. Although predation was high in all three environments, it was highest within the wood, where it was the main egg mortality factor (Fig. 4). The longer development time there may be one reason for the higher predation rate, but other factors, such as predator abundance, are probably also involved. However, no observations were done on the predators involved. These results suggest that the anity of L. achine for glade edges may be ascribed to two factors: (1) host plant abundance in the shade under the tree and bush canopy is highest near the edge of the glades; and (2) selection against oviposition in the sun as well as in the shade due to high egg mortality. In a similar way, Stephanitis pyrioides (Hemiptera) avoids low survival in open sunny habitats and in shaded habitats by preferentially colonizing plants growing in partial shade (Trumbule and Denno, 1995). 4.1. Conservation implications Detailed ecological studies that identify key environmental variables are a prerequisite for success of butter¯y conservation eorts (Murphy et al., 1990). To preserve L. achine it is clearly important to maintain suitable glades containing C. montana by grazing or clearing at regular intervals to prevent closure. To
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improve overgrown sites of L. achine, I suggest that small clearings (10±30 m in diameter) should be created, wide enough to allow the sun to reach ground and with C. montana at the edges. On the other hand, areas with few trees and bushes are not suitable for L. achine either, so too many clearings may be harmful. Thus it may be necessary to maintain a delicate balance in this respect. To provide more eective management guidelines than described here for preserving L. achine populations, it may be necessary to study the structure of trees and bushes to understand the optimal openness of a site for L. achine. Long-term population dynamics are probably determined by the degree of openness of the site and the amount of suitable edge habitat.
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