Regional Dynamics of a Patchily Distributed Herbivore Along an Altitudinal Gradient

Ecological Entomology (2005) 30, 706–713

Regional dynamics of a patchily distributed herbivore along an altitudinal gradient

ADELA GONZA´LEZ-MEGIÁS, JOSE´M. GO´MEZ and FRANCISCO SAŃCHEZ-PIN˜ERO Departamento de Biologıá Animal y Ecologıá, Facultad de Ciencias, Universidad de Granada, Granada, Spain

Abstract. 1. Metapopulation dynamics should be more important at the borders of species distributions due to two main factors: (1) populations are less abundant and fluctuate more at the borders than in the centre of their distributions, and (2) resources in the range margins of species distributions are often more scarce and fragmented. 2. Most metapopulation studies have been performed in a fraction of the entire distribution of species. The main goal here is to study the population dynamics of a narrowly distributed species including both the borders and the centre of the distribution, and to test the predictions described above. 3. The density and extinction events in a patchily distributed species, Timarcha lugens, was quantified for 5 years along an altitudinal gradient including the upper and lower limits of the species distribution. The dispersal ability of Timarcha was also studied using a mark–release–recapture study. 4. Extinction events and empty patches were only found at the borders of Timarcha distribution. The fluctuation in beetle density was greater in patches suffering extinction events. Resource abundance was negatively related to beetle density and positively related to extinction events. In addition, the dispersal rate among patches was very low and beetles moved distances of no further than 25 m. 5. Population density governs the extinction events in this system, and its fluctuation was more evident near the border of the distribution. Both factors together with the relative population stability in patches at medium and high altitudes, and the low dispersal rate of the individuals support the idea of a source–sink metapopulation structure in T. lugens. Key words. Extinction, high mountain, population fluctuation, Sierra Nevada, source–sink dynamics, Timarcha lugens.

Introduction these fragmented habitats, resources are patchily distributed and surrounded by unsuitable habitats (Rhodes et al., Great efforts to understand the distribution of species in 1996; Hanski, 1999; Hutchings et al., 2000). Most land- fragmented landscapes have been conducted in the last scapes have been modified and highly fragmented in the decades (Hanski & Gilpin, 1997; Hanski, 1999). This last years, threatening the persistence of many species of increased interest can be explained because many species plants and animals (Edwards et al., 1994; Samways, 1994). live in habitats that are highly heterogeneous, whether Consequently, these studies of fragmented habitats have naturally or human-induced (Hutchings et al., 2000). In implications for many different disciplines including population and landscape ecology, and also conservation and management. Correspondence: Adela Gonza´lez Megıás, Departamento de Species living in patchy habitats can exhibit a variety of Biologıá Animal y Ecologıá, Facultad de Ciencias, Universidad population structures with different implications for persis- de Granada, E-18071 Granada, Spain. E-mail: [email protected] tence and coexistence of populations (Harrison & Taylor,

706 # 2005 The Royal Entomological Society Distribution limits and population stability 707

1997). One of these possibilities is a metapopulation, defined same plant. Flowering occurs after the larvae have buried as a group of patchy populations connected by immigration under the plant to pupate. As adults live longer than one events (Harrison & Taylor, 1997). Metapopulation can be breeding season, both new adults and older individuals are interpreted as the equilibrium outcome of extinction and found throughout the summer (Gonza´lez-Megıás et al., 2004). colonisation processes (Hanski & Simberloff, 1997; Hormathophylla spinosa is a long-lived stunted shrub Harrison & Taylor, 1997; Hanski, 1999). Different types of occurring in high mountains of the western Mediterranean, metapopulation have been defined, classical metapopulation from southern France to North Africa, and occurs in Sierra (Levins metapopulation), mainland–island, or source–sink Nevada mountains from 1600 to 3100 m a.s.l. This thorny dynamics (Hanski & Simberloff, 1997; Harrison & Taylor, mass-flowering shrub is typically hemispherical in shape 1997). However, as Thomas and Kunin (1999) pointed out, when reproductive. In the Sierra Nevada high mountains, sometimes it is impossible to fit a system to a particular plants grow aggregated in patches, and are surrounded by category, and it is more common to find systems that show alpine dry grasslands and rocky bare soil. elements of different types of metapopulation. Some authors suggest that metapopulation dynamics would be more important near the borders of species dis- Study area tribution (Thomas et al., 1999). This can be explained by several factors: first, populations located at the border of the The field work was carried out in the San Juan Valley distribution are less abundant and fluctuate more than (Sierra Nevada National Park, Granada, Spain) from 2474 populations located in the centre of their geographical dis- to 2940 m altitude during the summers of 1998–2002 tribution (Randall, 1982; Brown, 1995; Lawton, 1995). (about 4 3 km, 3740N, 3220W, Fig. 1). Most Fluctuating populations have been observed to show higher H. spinosa patches found in the study area were used for extinction rates than stable populations (Pimm et al., 1988; this study (a total of 20 populations, Fig. 1). A patch was Sjo¨gren, 1991). Second, resources in the range margins of defined as a group of H. spinosa plants separated by at least species are often more scarce and fragmented (Thomas et al., 25 m from another group of plants. If two patches were 1999). Most metapopulation studies have been performed in closer but a cliff, the river or a big group of boulders were a small portion of the whole distribution of species (Hanski between them, they were considered as different popula- & Gilpin, 1997; Hanski, 1999; Hanski & Gaggiotti, 2004). tions. Three patches with less than 15–20 plants were This occurred because species used in most studies show a excluded from the annual survey because of their small wide distribution. To test the above predictions, the popula- size (patches A, B, and C, Fig. 1). They were only used tion dynamics of a species including both the borders and for mark–recapture experiment (see below). the centre of the distribution has been studied. For this, for 5 years the density of a patchily distributed species, Timarcha lugens (Coleoptera, Chrysomelidae) was quanti- Data collection fied, and the extinction events of this beetle were estimated along an altitudinal gradient that include the upper and The density of T. lugens on each of the H. spinosa patches lower altitudinal limits, the range margins for this species. occurring in the study area over 5 years (1998–2002) was The specific predictions are: (1) fluctuations in beetle density determined. Every year two 10 2 m transects per patch and extinction events will be greater at the borders of the were established. These transects were not permanent and distribution, (2) there will be a relationship between extinc- were established at random every year. In each transect, the tion events and fluctuation in beetle density in local popula- number of beetles were counted, recording their sex and tions, and (3) beetle density will be positively related to stage (adult or larva). Those patches in which no beetle resource abundance, measured as plant density and size, was found were visited periodically throughout the breeding and negatively related to extinction events. season in order to assure the absence of individuals. In addition, the number of host plants per transect was counted, and their heights and two perpendicular widths Methods were measured in order to estimate their size using the for- mula of a hemisphere (Gonza´lez-Megıás & Go´mez, 2003). Natural history of the system Because there are differences in altitude among patches, to avoid differences in phenology among populations of both Timarcha lugens is a high-altitude, apterous, medium-sized the host plant and the beetles the censuses were made at the (43.1 2.07 mg dry weight, n ¼ 130) beetle, endemic to the same phenological stage of the host plant, just after the Sierra Nevada mountains (Spain), occurring from approxi- snowmelt (between late June and early July). mately 2450 to 3200 m a.s.l (Gonza´lez-Megıás et al., 2004). It Four descriptors of the beetle populations were used for is monophagous on Hormathophylla spinosa (Cruciferae), the analyses: (1) beetle density, calculated as the average feeding by chewing leaves as well as flowers and fruits number of beetles per m2, (2) extinction, defined as a binary (Gonza´lez-Megıás & Go´mez, 2001). It is active soon after variable, one for populations that became extinct at least snowmelt (late June at the study site) until the end of one of the study years (the patch was occupied the previous September. Larvae and adults can be found sharing the year), and zero for those populations without any

# 2005 The Royal Entomological Society, Ecological Entomology, 30, 706–713 708 Adela Gonza´lez-Megı´as, Jose´ M. Go´mez and Francisco Sa´nchez-Pin˜ero

(a) (b)

2400 16 2600 7 6 2 14 13 2500 12 20 m 8

2700 40 m 15 2 11 9 8 40 m

9 10 2800 20 20 A B C 4 3 1 400 m 19 75 m

A 17 5 2900 B 18 18.5 m 100 m

25 m C N 100 m 250 m 3 1

Fig. 1. (a) Map of the study area showing the location of each patch of Hormathophylla spinosa. Squares indicate patches that became extinct on at least one of the study years. The star indicates an empty patch. Black circles indicate patches inhabited by Timarcha lugens every year. (b) Map of the populations where beetles were marked (1, A, 8, shaded patches), and closer patches. Hatching indicate patches that received marked beetles from another patch. Numbers indicate the distances between patches. extinction event, (3) coefficient of variation of local popu- study was carried out from July to August in 2002, during lation density, calculated as SD/mean. This variable has the peak of the species density. Beetles were marked during been strongly recommended as one of the best descriptors the first 2 weeks of July in three patches located in the of population variability (McArdle et al., 1990; Schoener & centre of the study area (Fig. 1). These patches were Spiller, 1992; Kindvall, 1996), and (4) sex ratio, defined as selected in order to ensure that there were sufficient beetles the number of males/number of females. for marking. The density of beetles in patches near the The following characteristics were estimated for each border of the distribution was very low for this purpose. H. spinosa patch: (1) altitude; (2) area (m2); (3) isolation, Beetles were individually marked with numbers using a estimated in two ways – the distance to the nearest occupied waterproof pen (Penol 52 Paint-Marker X-Fine). After patch and the distance to the three nearest occupied patches being marked, beetles were released on the same plant (because the same results were obtained in all the analysis where they were found, and the gender and position were for both isolation measures, in this study only the results recorded. The 23 patches were then visited every 4 days based on the second measure are shown for brevity); (4) until the beginning of August plant density (number of plants per m2); and (5) average plant size per patch (cm3).

Data analysis

Beetle movements among plant patches Linear and quadratic regressions were used to examine the relationship between continuous variables (altitude, To evaluate the dispersal ability of T. lugens and the beetle density, coefficient of variation, etc.), whereas migration events among patches, a mark–release–recapture logistic regressions were used for binomial variables

# 2005 The Royal Entomological Society, Ecological Entomology, 30, 706–713 Distribution limits and population stability 709

(extinction). The spatio-temporal variability in beetle density was analysed by Generalised Linear Models (Proc 0.4 GLZ, Statistica v6.0, Statsoft), introducing patch and year 13 16 0.3 2 as independent variables, fitting the dependent variable to a 0.2 1 Poisson distribution, and using log as link function. For 0.1 extinction, sex ratio, and the coefficient of variation, a 0 0 patch never colonised by beetles was excluded from the 2475 m 2550 m 0.09 0.9 analysis. 14 7 The variables were log- (for linear measurements) or 0.07 0.7 0.05 2560 m 0.5 2600 m angular-transformed (for percentages) when necessary to 0.03 0.3 normalise them (Zar, 1996). Values are given as means 0.01 0.1 and SE. 1.2 2 15 4 3 0.8 Results 2 0.4 1 2625 m 0 Description of host-plant patches 2630 m 20 3 2 1.5 The H. spinosa patches in the San Juan Valley differed 1.5 1 greatly in most traits. Patches ranged from 2474 to 2940 m 1 in altitude (Fig. 1). The mean paired distance between 0.5 0.5 2800 m 2810 m patches was 206 22.21 m, but ranged from 18.5 to 0.05 0.175 432 m. There were also differences among patches in their 6 12 2640 m size, the area ranging from 250 to 14000 m2. Plant density 0.03 0.125 2 0.075 varied between 0.43 0.07 and 3.11 0.46 plants per m , 0.01 and the average size of H. spinosa shrubs from 366.20 to 0.025 2630 m 6844.61 cm3. 9 11 There was no relationship between altitude and area 0.75 (F 0.26; P 0.62) or isolation (F 0.00; 2 1,19 ¼ ¼ 1,19 ¼ 0.5 P ¼ 0.99); however, plant density was negatively related Beetle density 1 2 0.25 to altitude (F1,18 ¼ 6.25; P ¼ 0.02, R ¼ 0.22, plant density ¼ 2700 m 2710 m 10.89 3.07 altitude). There was also a negative quadratic 10 19 relationship between altitude and the average size of the 0.75 4 2 3 plants (F2,17 ¼ 7.39; P ¼ 0.005, R ¼ 0.40, plant size ¼ 0.5 2730 m 23.47 5.84 altitude þ 45.49E2 altitude2. 2 0.25 1 2790 m 4 8 Spatial and temporal variability in Timarcha lugens density 7 4 5 2.5 A total of 3436 T. lugens was found during the study 3 2800 m 2630 m 1 period (1320 males, 1303 females, and 813 larvae). The 1 average density of beetles was 0.95 0.20 beetles per m2. 10 117 In 15 out of the 20 H. spinosa patches there were T. lugens 8 3 every year of study, whereas one patch was not occupied by 6 2 4 beetles during the study period. In addition, extinction 1 2 events in five patches were registered, four located in the 2760 m 2850 m lower limit of the T. lugens distribution and one in the 5 18 upper boundary (Fig. 1). Patches closer to the lowest 4 1.5 boundary were occupied at least two of the study years, 2875 m some of them showing extinction and colonisation events 2 0.5

(Fig. 2). No larva was found in any of these patches. The 2940 m 0 –0.5 patch on the upper boundary became extinct in the last 1998 2000 2002 1998 2000 2002 year because all host plants died. 1999 2001 1999 2001 There was significant spatial and temporal variability in Year the density of beetles (total, males and females; Table 1). The interaction between the two factors was also significant Fig. 2. Density of Timarcha lugens (mean SE) in every patch in the analysis, indicating that the among-year variation in during the five study years. Numbers inside each graph indicate beetle density differed among patches (Table 1). For altitude (m).

# 2005 The Royal Entomological Society, Ecological Entomology, 30, 706–713 710 Adela Gonza´lez-Megı´as, Jose´ M. Go´mez and Francisco Sa´nchez-Pin˜ero

Table 1. Results of the generalised linear general model using the total number of individuals, males, and females as dependent variables, and population, year, and the interaction between them as independent variables.

Model d.f. w2 P

Total Population (A) 19 1482.54 0.0001 Year (B) 4 73.00 0.0001 A B 76 1139.61 0.0001 Males Population (A) 19 568.14 0.0001 Year (B) 4 33.38 0.0001 A B 76 354.19 0.0001 Females Population (A) 19 666.78 0.0001 Year (B) 4 27.19 0.0001 A B 76 332.51 0.0001

example, in some patches beetle density gradually between sex ratio and altitude (F1,18 ¼ 19.59; P ¼ 0.0004, decreased during the 5 years of the study, whereas in sex ratio ¼ 0.44 0.0012 altitude, R2 ¼ 0.52), the propor- other patches the density increased, or even fluctuated tion of males increasing at lower altitudes (Fig. 3). However, around several peaks (Fig. 2). the coefficient of variation of beetle density was not related to However, beetle density not only varied among patches beetle density (F1,18 ¼ 1.56; P ¼ 0.22) or altitude and years but also with altitude; beetle density initially (F1,18 ¼ 0.03; P ¼ 0.87). increased with altitude and then started to decrease at higher The probability of extinction was negatively related to 2 2 altitudes (F1,17 ¼ 6.69; P ¼ 0.007, R ¼ 0.44, beetle beetle density (w 1 ¼ 15.82; P ¼ 0.000, logistic slope: density ¼25.81 þ 0.18 altitude – 3.24E6 altitude2, 4.37 3.02), and positively related to the coefficient of 2 Fig. 3). A significant negative correlation was also found variation (w 1 ¼ 8.37; P ¼ 0.004, logistic slope: 9.58 4.53).

0.6 Movement of Timarcha lugens among Hormathophylla spinosa patches 0.5 A total of 516 beetles, 276 males and 240 females, were 0.4 marked (168 in patch 8, 220 in patch A, and 128 in patch 1, 0.3 Fig. 1). The number recaptured was relatively low, only 17.6% of marked individuals were recaptured at least 0.2 once. Most beetles were recaptured in the same patch where marked and only 4% moved to a different patch, 0.1 Beetle density (log) most immigrants being males (75%). The mean inter-patch 0 distance beetles moved was 21.75 1.88 m and the longest distance recorded in the study area was 25 m. All movements occurred within the first 2 weeks after the individual was captured and marked. Once a marked individual was 0.16 recaptured in a different patch no more movement for this individual to a different patch was observed.

0.14 Discussion

0.12 Extinction events only occurred on patches located near the distribution range of T. lugens, whereas patches in the centre of the distribution suffered no extinctions during the Sex ratio (arcsin) 0.1 study period. This result supports the idea of the instability of the species near the border of the distribution against a 0.08 more stable scenario in the centre of the area (Randall, 2450 2550 2650 2750 2850 2950 1982; Brown, 1995; Lawton, 1995). Moreover, these mar- Altitude (m) ginal patches had lower beetle densities, which fluctuated more intensely during the study period, as indicated by the Fig. 3. The relationship between beetle density and sex ratio with higher coefficient of variation. This also agrees with the altitude. High values of sex ratio indicate a higher proportion of general idea that extinction risk is greater in populations males. with high temporal fluctuations than in populations that

# 2005 The Royal Entomological Society, Ecological Entomology, 30, 706–713 Distribution limits and population stability 711 remain more stable (Pimm, 1991; Lawton, 1995; Kindvall, 1997; Quinn et al., 1997; Cowley et al., 2000; Meneńdez & 1996). Both the temporal variability and the extinction risk Thomas, 2000), these species are usually more abundant are affected by several factors such as the environmental where their resources are more abundant or of better qual- stochasticity, inter-patch dispersal, and population density ity (Harrison, 1997; Hodkinson, 1997; Quinn et al., 1997; (Sjo¨gren, 1991; Eber & Brandl, 1996; Hill et al., 1996; Cowley et al., 2000; Meneńdez & Thomas, 2000; James Kindvall, 1996; Lima et al., 1996; Hanski, 1997; Dennis & et al., 2003). Other insect species have shown a similar Eales, 1997; Lawes et al., 2000). In this study, beetle density pattern such as the psyllid Strophingia ericae (Hodkinson did not affect the coefficient of variation, although it et al., 1999) and the moth Yponomeuta mahalebella affected negatively the probability of extinction. This result (Alonso, 1999). In these cases, herbivores and host plants has also been observed in other species such as Metrioptera have different ecological requirements (Hodkinson, 1997; bicolor, a grasshopper with very low dispersal rates Cowley et al., 2000). Consequently, the quality of the (Kindvall, 1996). Timarcha lugens dispersal rates were also patches can be related not only to the amount of resources very low which may have limited the rescue effects on but also to the abiotic conditions. Preferences for patches in sparsely populated patches. In addition, there were fluctua- relation to more suitable microclimatic conditions have tions in beetle density among years, although there were been observed in other species of insects (Wilson et al., variations in these fluctuations among patches. This prob- 1999; Roland et al., 2000). In this case, patches of lower ably supports the statement that local population processes quality are those located near the border of the distribu- are the major determinants of population sizes (Lewis et al., tion. Therefore, the fluctuation in beetle density, as well as 1997; Stacey et al., 1997; Hanski, 1999). Therefore, spatial the concentration of the extinction events on patches variability can be determined both by the inter- and intra- located close to the borders suggest source–sink dynamics, specific interactions of species in each population (Hassel & in which patches of higher quality would support more Wilson, 1997; Pacala & Levin, 1997; Wiklund et al., 1998; stable populations, probably in or near the equilibrium Wilson et al., 1999), and, by changes in habitat quality, due (Pulliam, 1988, 1996; Watkinson & Sutherland, 1995), and to extrinsic and intrinsic factors (Pulliam, 1988, 1996; provide new individuals to other patches of lower quality Fryxell, 2001). Indeed, extinction events in the upper and (Pulliam, 1988, 1996). In this system, patches located at low lower margins were provoked by different mechanisms. The altitude behaved as sinks unable to support populations extinction event in patch 18, located near 3000 m a.s.l., was of T. lugens. The use of density as a predictor of the quality a consequence of the extinction of the host plant, the patch of the patches has been used in other studies in which disappearing in the last year of the study. Moreover, the data on mortality or reproduction are not available distribution of T. lugens was limited on the upper margin (Foppen et al., 2000). Moreover, during the 5 years of by the upper altitudinal distribution of its host plant. In study the reproduction in those patches, if it occurred, contrast, extinction events registered in the lower margin, was unsuccessful, because no larva was found in any of where the host plant is very abundant, are probably due to the patches in which extinction events were observed. T. lugens’ tolerance to abiotic conditions. Although mortality rate was not measured in this study, Up to this point, predictions have been supported by the the high rates of extinction can be an indicator of high results obtained in this study. Nevertheless, more fragmen- mortality rates. ted and smaller patches near the border of the distribution In source–sink dynamics, the occupancy of sinks, which have failed to be found, which would have favoured a lie outside the fundamental niche of the species, depends on metapopulation structure (Thomas et al., 1999). Along the the dispersal ability of the species (Boughton, 1999). entire study area of the beetle, the host plant shows a Indeed, a high rate of movement of individuals between patchy distribution, and thereby there was no relationship patches can prevent populations becoming extinct, a phe- between altitude and patch area and isolation. Moreover, nomenon known as the rescue effect (Appelt & Poethke, both plant density and plant size showed a negative rela- 1997; Stacey et al., 1997). Some simulation models have tionship with altitude. Therefore, there is an unusual rela- shown that only five or six immigrants per year are neces- tionship between the beetle and the host plant – beetle sary to prevent extinctions even in stochastic environments abundance increasing with altitude but plant abundance (Stacey et al., 1997). The flow of emigrants could explain decreasing with altitude. This occurs because T. lugens is the colonisation events in our system. However, the low distributed along the upper altitudinal boundary of its host beetle density in the sink patches and the frequent extinc- plant. Furthermore, T. lugens is locally very abundant and tion events can be a consequence of the low rate of migra- narrowly distributed but feeds on a plant that is locally tion found in this study (4%), and the short distances that abundant and has a wide distribution (see Natural history beetles moved among patches (less than 25 m). This low of the system). Therefore, these results do not support the migration rate has been observed not only in other wingless resource availability hypothesis, which predicts that species species such as the weta Hemideina maori (Leisnham & that are locally rare and narrowly distributed use resources Jamieson, 2002) or the bush cricket Metrioptera bicolor that are locally rare and narrowly distributed (Gaston, (Kindvall & Ahleń, 1992), but also in winged species such 1994; Quinn et al., 1997). Although herbivorous species as the butterfly Plebejus argus (Lewis et al., 1997) and the tend to show a narrower distribution than their host plants moth Zygaena filipendulae (Meneńdez et al., 2002). Because (Hill & Hodkinson, 1992; Harrison, 1997; Hodkinson, patches at the border of the distribution were, in general,

# 2005 The Royal Entomological Society, Ecological Entomology, 30, 706–713 712 Adela Gonza´lez-Megıás, Jose´ M. Go´mez and Francisco Sańchez-Pin˜ero surrounded by other patches with low beetle density, the moths in a fragmented landscape. Journal of Applied Ecology, probability of receiving an immigrant was very low. 37, 60–72. An additional problem for establishing a population in Dennis, R. & Eales, H. (1997) Patch occupancy in Coenonympha sink patches is the bias in sex ratio. In this system, the tullia (Mu¨ller, 1764) (Lepidoptera: Satyrinae): habitat quality proportion of males was higher at the borders than in the matters as much as patch size and isolation. Journal of Insect Conservation, 1, 167–176. centre of the altitudinal distribution. This has been also Eber, S. & Brandl, R. (1996) Metapopulation dynamics of the observed for other animals such as Microtus voles, in tephritid fly Urophora cardui: an evaluation of incidence-func- which females are more abundant in sink patches tion model assumptions with field data. Journal of Animal (Gundersen et al., 2001). The sex bias in the study area Ecology, 65, 621–630. can be explained because males move more than females, as Edwards, P.J., May, R.M. & Webb, N.R. (1994) Large-scale shown in the mark–recapture experiment, but probably Ecology and Conservation Biology. Blackwell Science, Oxford. also because there are different requirements between Foppen, R.P.B., Charton, J.P. & Liefveld, W. (2000) sexes, with females being constrained more than males by Understanding the role of sink patches in source–sink metapo- microclimatic conditions (probably related to optimal pulations: Reed Warbler in an agricultural landscape. places for oviposition). Sex-biased dispersal has been Conservation Biology, 14, 1881–1892. Fryxell, J.M. (2001) Habitat suitability and source–sink dynamics observed in many different species of insects, birds, mam- of beavers. Journal of Animal Ecology, 70, 310–316. mals, and sharks (Greenwood, 1980; Clark et al., 1997; Gaston, K.J. (1994) Rarity. Chapman & Hall, London. Gundersen et al., 2001; Caudill, 2003). Gonza´lez-Megıás, A. & Go´mez, J.M. (2001) Adult and larval plant In conclusion, as the theory predicts, variability in popu- range and preference in Timarcha lugens (Coleoptera: lation density governs extinction events in our system. Chrysomelidae): strict monophagy on an atypical host. Annals Moreover, the instability in population density was more of the Entomological Society of America, 94, 110–115. evident near the border of the distribution. Both factors Gonza´lez-Megıás, A. & Go´mez, J.M. (2003) Consequences of together with a relative stability in patches at medium and removing a keystone herbivore for the abundance and diversity high altitude, and the low dispersal rate of the individuals of arthropods associated with a cruciferous shrub. Ecological support the idea of a source–sink metapopulation structure Entomology, 28, 299–308. Gonza´lez-Megıás, A., Go´mez, J.M. & Sańchez-Pin˜ero, F. (2004) in T. lugens. The biology of the high-mountain chrysomelid Timarcha lugens. New Contributions to the Biology of Chrysomelidae (ed. by P. H. Acknowledgements Jolivet, J. A. Santiago-Blay and M. Schmitt), pp. 553–563. SPB Academic Publishing, The Netherlands. Greenwood, P.J. (1980) Mating systems, philopatry and dispersal We thank two anonymous referees for their valuable com- in birds and mammals. Animal Behaviour, 28, 1140–1162. ments and advice. We thank Enrique Doblas for his help in Gundersen, G., Johannesen, E., Andreassen, H.P. & Ims, R.A. the field. 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# 2005 The Royal Entomological Society, Ecological Entomology, 30, 706–713