Environmental correlates of life history pattern in ground-beetles on Tenerife (Canary Islands)

Acta Oecologica 35 (2009) 355–369

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Original article

Environmental correlates of life history pattern in ground-beetles on Tenerife (Canary Islands) Antonio de los Santos Go´mez* Department of Ecology, University of La Laguna, Spain

a r t i c l e i n f o

a b s t r a c t

Article history: Received 28 July 2008 Accepted 3 March 2009 Published online 21 March 2009

The spatial and temporal structure of Carabus (Nesaeocarabus) interruptus Dejean, 1831 populations and the independent effects of climate along altitudinal gradients in the island of Tenerife, especially whether environmental preferences constrains the species breeding patterns at local and regional scales were evaluated. Ground-beetles were sampled with twenty-one pitfall traps in each of the forty-one plots during one year study. Some sampled specimens were dissected and dried to determine sex, weight and ovarian maturation. The populations were restricted to the middle climatic zone (600–1700 m). There was a long adult activity period from October to June and the changes in the weekly capture success were strongly correlated with the rainfall and temperature. Overall the males during winter were more active than the females. The emergence of new adults occurred only in spring and the body dry weight peaked in April–May. From start of autumn the weight was recovered to the initial values of the cycle, increased and peaked in January. The females prolonged its oviposition period from mid-autumn to the starting of spring. The species showed a winter breeding pattern and the seasonal variations in multiple life history traits could correspond with the changing conditions of the microclimatic variables. An evolutionary ecological model could help explain the life history pattern variability among the Carabus species in South-western Europe. The species could tackle the geographic dispersion of their populations for the single purpose of seeking a suitable hydrothermal environment (high rainfall and mild temperatures) if the food was insured. Ó 2009 Elsevier Masson SAS. All rights reserved.

Keywords: Gound-beetles Altitudinal and latitudinal gradients Breeding patterns Hydrothermal environment Canary Islands South-western Europe

1. Introduction Since the Eighteenth Century, several approaches were made by well-known naturalists (e.g. Humboldt, Webb and Berthelot) and coleopterists (e.g. Brulle´, Dejean and Wollaston) to describe the effects of the broad altitudinal climatic gradient on the island of Tenerife, within which the microenvironments changed in terms of topoclimate, soil and vegetation (de los Santos et al., 2000, 2002). In addition, the Tenerife island environments registered high levels of general desertification. So over here it was expected that beetle populations could show particular altitudinal distributions in terms of their physiological optima (hydric and thermal) and tolerance limits (de los Santos et al., 2006). It was known that ground-beetles are more sensitive to rainfall or moisture in low latitude environments (de los Santos et al., 1985, 1991), and to temperature in high altitudes and latitudes (Greenslade, 1968; Butterfield, 1996). By monitoring chemical habitat cues

* c/ Astrofı´sico Fco. Sa´nchez, s/n. 38206-La Laguna, Sta. Cruz de Tenerife, Canary Islands, Spain. Fax: þ34 22 318311. E-mail address: [email protected] 1146-609X/$ – see front matter Ó 2009 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.actao.2009.03.001

and reacting kinetically to temperature and humidity gradients (Evans, 1983), foraging adults could find the habitat to which they were physiologically adapted. The habitat preference seems to be the most important variable in the distribution patterns (Do¨ring and Krompb, 2003). The occurrence of vulnerable stages must be timed to avoid periods of physical extremes and activity of natural enemies at the height of the season and, in addition, their presence and abundance are always related to the increase in prey density, with higher values in sites with greater herbaceous cover (Lenski, 1982; Lo¨vei and Sunderland, 1996; Guillermain et al., 1997; Cole et al., 2002; Dennis, 2003; Brandmayr et al., 2004; Migliorini et al., 2002). The ground-beetles form the speciose beetle family Carabidae and, since their emergence in the Tertiary, have populated all habitats except deserts (Lo¨vei and Sunderland, 1996). However, there are a lot of Carabidae species which colonized some ‘‘moist’’ habitats in hot deserts like Sahara, Namibe, Kalahari and so on (e.g. Anthia spp., Graphipterus spp., Cypholoba spp.) (see for instance Paarmann, 1979a; Cloudsley-Thompson, 2001). In the present work, emphasis was placed on the colonization of Tenerife by an ancestral species of the ground-beetle Carabus (Nesaeocarabus) interruptus Dejean, 1831 (Coleoptera, Carabidae) a large endemic species belonging to a subgenus related with the North African

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Eurycarabus Ge´hin, 1885 (Pru¨ser et al., 2000). It was hypothesized that a group of beetles descended from a single ancestral species that arrived at the Canary Islands millions of years ago began displaying a certain propensity for hydrothermal environments especially with that they claimed its survival and increase. As time progresses, the descendant species occupied same or very similar climatic niches in different locations over larger geographical areas. Island distributional patterns were supposed to result from differences in life history characteristics (Mayr and Diamond, 2001). Biological characteristics of the species, type and size of local landscape elements and their spatial arrangements were important for the dispersal of epigeic arthropods (Joppa and Reuterb, 2005). However, the effects of life history traits on island distributions were directly evaluated in few studies. The present study departed from the aim of providing an evolutionary ecology model to explain the incredibly rich life history of ground-beetle species in general, most of which were found in the tropics (Lo¨vei and Sunderland, 1996), and Carabus species in particular. The genus Carabus – Linnaeus, 1758, a large group of flightless groundbeetles is one of the most widely distributed carabid genus of the temperate zones at middle latitudes, ranging from subtropical mountains and Mediterranean environments to alpine and arctic environments (Deuve, 2004). Seasonal weather patterns determine the breeding activity of carabids in the tropics because their gonads remain dormant until stimulated by rain (Paarmann, 1979b). These beetles also respond to the rains, mainly in subtropical and Mediterranean regions (de los Santos et al., 1985, 1991). Higher latitude environments display very short summer growing season and it could ultimately impose limits to their growth and reproduction (Ottesen, 1985; Niemela¨ et al., 1989; Lo¨vei and Sunderland, 1996; Sota, 1996; Filippov, 2006). Ground-beetles react to seasonal environments by changes in the life history patterns (Paarmann, 1990; Sparks et al., 1995; Butterfield, 1986; Ribera et al., 1999), mainly by the diapause’s syndrome. Thiele (1977) divided the annual rhythms of groundbeetle into five categories, but flexibility in the life cycle had

probably been one of the main causes to the dispers and colonization success of many Carabus species (Benest and Cancela da Fonseca, 1980; Houston, 1981; Refseth, 1984; Jørum, 1985; Loreau, 1985; Butterfield, 1986). For instance, spring breeders on organic fields benefit from the increased availability of overwintering habitats in their close surroundings (Purtauf et al., 2005). Trade-offs encompass multiple simultaneous traits, but, indeed, even the evolutionary trade-offs could be changed by temperature and rainfall variations (Ernsting and Isaaks, 2000). This report outlines the results of one part of an extensive study regarding the life cycle and environmental relationships of the endemic ground-beetles in the island of Tenerife. The great abundance of some species made possible a comprehensive research about activity density, reproductive characteristics, and climatic (thermal and hidric) environment along elevation gradients. It was hypothesized that the Carabus species were able to preserve the climatic preferences in evolutionary time. Therefore, the fundamental hydrothermal environment used by the species changed slowly over time by natural selection (see Peterson et al., 1999). In order to define the ecological relations among space, time and hydrothermal habitat axes of the C. interruptus populations, specifically linked to its dispersal and island colonization abilities, the beetles were sampled over a range of altitudes in Tenerife Island and the results were compared with ground-beetles species occurring at different latitudes. In this regard, it has been consulted two works (Turin et al., 2003; Serrano, 2003) concerning the genus Carabus for synonymies and valid names since it is well known the controversy about the taxonomy of this genus. 2. Materials and methods 2.1. Study area The research was carried out along elevational gradients on the SE (leeward) slope of the island of Tenerife (Fig. 1). The groundbeetle sampling started at sea level and extended up to 2360 m a.s.l.

3600

Tenerife

5 km

31400 31440

31420

Slope of Arafo

31400

31380

31360

31340

31320

Ravine of Badajoz

31300

Hillside of Anocheza 31280 3500

3520

3540

3560

3580

3600

3620

3640

3660

3680

3700

Fig. 1. Location of study sites in Tenerife: Ravine of Badajoz, Hillside of Anocheza and Slope of Arafo. The numbers in abscissas (Easting in hectometers) and ordinates (Northing in hectometers) are used to identify locations on the Earth and those are referenced in the Universal Transverse Mercator (UTM) coordinate system (Huse 28; Zone R; Datum Pico de la Nieves).

´ mez / Acta Oecologica 35 (2009) 355–369 A. de los Santos Go

Mean annual temperature decreases up the slope and the mean annual rainfall increased until 1500 m a.s.l., decreasing again from this level up to the upper end of the Island. The heterogeneity marked by the height at which the dew point temperature was reached induced a division between two large types of habitats: a xeric and hot one located between shoreline and 600 m a.s.l. (seaboard), and a humid one, with thermal contrasts, in the montane zone. Secondly, the montane environment could be partitioned into cloud belt located between >600 and 1700 m a.s.l. (Ravine of Badajoz, Hillside of Anocheza and Slope of Arafo) and island summit located between 1700 and 2360 m a.s.l. (Canarian pinewood and summit scrub) due to the existence of the trade wind inversion. Thirdly, the annual variation of the upper level of the trade wind inversion zone (>900–1200 m a.s.l. in summer and 1700 m a.s.l. in winter; see Font Tullot, 1956) further split the elevational cloud belt into a summer-xeric zone (Anocheza and Arafo) and one that is cloudy (or humid) almost all the year round (humid bed of the Ravine of Badajoz). Mean annual temperature values in the lower part of the Island (0–600 m a.s.l.) showed only little changes in annual fluctuations (16.5–21  C), and the mean annual precipitation was about 300 mm. The dominant vegetation type was xerophytic scrub, rich in succulents, especially cactiform or dendroid spurges (e.g. Euphorbia canariensis L., Euphorbia balsamifera Ait., Euphorbia obtusifolia Poir.), and Plocama pendula Ait. The orographically induced uplift of the trade winds in the middle part of the Island

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(Arafo, Badajoz and Anocheza) resulted in (1) high cloudiness below the temperature inversion, especially on the windward slope, and (2) decreasing radiation that contributed to (3) a higher level of moisture. The mean annual temperature was quite constant, between 14.5  C and 16.5  C, although there were seasonal fluctuations, and the mean annual rainfall was 700 mm. The vegetation (xeric laurel forest) was mainly composed of Ilex canariensis Poir., Arbutus canariensis Veill. and Erica arborea L. In the upper part of the Island (summit), two representative zones were sampled. The first (>1700–2000 m a.s.l.) was a woodland composed of Pinus canariensis Chr. Sm. ex DC. in Buch, with an understory dominated by the shrub legume Chamaecytisus proliferus (L.fil.) Link. Mean annual temperature was between 12.5  C and 14.5  C, and mean annual rainfall was between 400 and 650 mm. The second zone, between >2000 and 2360 m a.s.l., was a summit scrub with Spartocytisus supranubius (L.fil.) Webb et Berth., Adenocarpus viscosus (Willd.) Webb et Berth. and Descurainia bourgaeana (Fourn.) O.E. Schulz. The mean annual temperature was low, between 9.5  C and 12.5  C, and mean annual rainfall varied between 200 and 450 mm. 2.2. Fieldwork Along the altitudinal gradients, forty-one study plots were chosen (Table 1). Ground-beetles on each plot were sampled with pitfall traps for one year. Grids of 21 traps in each study plot were

Table 1 ˜ adas), landscape (sandy lava, xerophytic scrub, Sites studied (1–5) with indication of zone (seaboard, Ravine of Badajoz, Hillside of Anocheza, Slope of Arafo, Summit and Can semiarid bed, humid bed, xeric laurel forest, Canarian pinewood, open field-pinewood, madrone forest and summit scrub), plot (1–41), elevation (meters above sea level) and sampling period. Site

Zone

Landscape

Plot

Elevation (m a.s.l)

Sampling periods

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 2 2 2 2 2 2 2 3 3 3 3 4 4 4 4 5 5 5 5 5 5 5 5

Seaboard Seaboard Seaboard Seaboard Seaboard Seaboard Seaboard Seaboard Seaboard Seaboard Seaboard Seaboard Seaboard Seaboard Seaboard Seaboard Seaboard Ravine of Badajoz Ravine of Badajoz Ravine of Badajoz Ravine of Badajoz Ravine of Badajoz Ravine of Badajoz Ravine of Badajoz Hillside of Anocheza Hillside of Anocheza Hillside of Anocheza Hillside of Anocheza Slope of Arafo Slope of Arafo Slope of Arafo Slope of Arafo Summit Summit Summit Summit Summit Summit ˜ adas Can Summit

Sandy lava Sandy lava Sandy lava Sandy lava Sandy lava Sandy lava Sandy lava Sandy lava Sandy lava Sandy lava Sandy lava Sandy lava Sandy lava Sandy lava Xerophytic scrub Xerophytic scrub Xerophytic scrub Semiarid bed Semiarid bed Semiarid bed Semiarid bed Humid bed Humid bed Humid bed Xeric laurel forest Xeric laurel forest Canarian pinewood Canarian pinewood Open field-pinewood Open field-pinewood Madrone forest Canarian pinewood Canarian pinewood Canarian pinewood Summit scrub Summit scrub Summit scrub Summit scrub Summit scrub Summit scrub

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41

36 46 51 50 54 53 56 59 70 73 76 79 83 90 95 135 175 425 450 550 575 600 650 700 950 1200 1500 1700 900 1100 1500 1700 1925 1950 2050 2100 2150 2225 2250 2360

21 May 01–20 May 02 21 May 01–20 May 02 21 May 01–20 May 02 21 May 01–20 May 02 21 May 01–20 May 02 21 May 01–20 May 02 21 May 01–20 May 02 21 May 01–20 May 02 25 Mar 85–03 May 86 21 May 01–20 May 02 21 May 01–20 May 02 21 May 01–20 May 02 21 May 01–20 May 02 08 Jan 84–11 Dec 84 11 Feb 84–11 Dec 84 12 Apr 85–03 May 86 12 Apr 85–03 May 86 19 Mar 85–17 Apr 86 19 Mar 85–17 Apr 86 19 Mar 85–17 Apr 86 19 Mar 85–17 Apr 86 19 Mar 85–17 Apr 86 19 Mar 85–17 Apr 86 19 Mar 85–17 Apr 86 19 Oct 88–01 Nov 89 19 Oct 88–01 Nov 89 18 Nov 88–01 Nov 89 05 Nov 88–01 Nov 89 09 May 88–08 May 89 02 May 88–01 May 89 02 May 88–01 May 89 02 May 88–01 May 89 03 Feb 85–09 May 86 03 Feb 85–09 May 86 03 Feb 85–09 May 86 03 Feb 85–09 May 86 03 Feb 85–09 May 86 03 Feb 85–09 May 86 01 May 88–30 Apr 89 03 Feb 85–09 May 86

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killing–preserving agents were used; these traps were emptied weekly. Ground-beetles were identified, counted and after released within 2 m of each trap, except a fraction of the specimens captured weekly which was taken to the laboratory for analysis, within a plastic container labelled according to date and plot. During the sampling period, temperatures and rainfall were recorded using a maximum–minimum thermometer and pluviometer placed on the soil surface at each site. The precipitation could not be recorded for Hillside of Anocheza.

2.3. Laboratory processing

Fig. 2. Altitudinal distribution (meters above sea level) Carabus (Nesaeocarabus) interruptus population. Mean activity density and 95% CI (vertical bars).

laid. Each grid contained three rows of traps, the rows were 5 m apart and the traps were 10 m apart. Pitfall trapping took factors affecting efficiency of capture into account (Gist and Crossley, 1973; Luff, 1975; Jansen and Metz, 1979). A funnel trap was used (de los Santos et al., 1982; Quintana et al., 1985) in which neither baits nor

The sample was transferred into 70% alcohol until further dissection to determine sex and ovarian maturation using established criteria (Gilbert, 1956; Barlow, 1973; Luff, 1973; Heerdt et al., 1976). Even though normally male and female of Carabus can be easily determined by the observation of anterior tarsomeres (dilated in males, more thin in females), this was only done in the laboratory, and confirmed by dissection, in order to expedite the field work. Testis maturation was not assessed. Ovarioles were extracted under a stereoscopic microscope and oocytes were measured with an ocular calibrated micrometer. Subsequently, each dissected individual was dried in an oven at 60  C for 24 h.

Fig. 3. Seasonal distribution of activity density of Carabus (Nesaeocarabus) interruptus adults, minimum and maximum temperature and precipitation at Ravine of Badajoz. Monthly average and 95% CI (vertical bars) for all studied variables.

´ mez / Acta Oecologica 35 (2009) 355–369 A. de los Santos Go

2.4. Statistical analyses Population estimates for pitfall traps method were expressed in terms of activity density (Tretzel, 1955; Heydemann, 1957). Different spatial and temporal levels could be considered for regression analysis. At the broad scale, captures must be pooled among plots within a site, and at the fine scale analyses could be conducted separately for each plot. Different levels of temporal aggregation could be also considered: the plot catch during the weekly period as mean number of beetles captured per trap and sampling day  100 (weekly level), and the monthly mean values of the weekly estimates (monthly level). In this paper, it is only considered the estimates at monthly mean levels for each site on which the ground-beetles were found. All statistical calculations were performed using the Statistical Package for the Social Sciences version 15 (SPSS, 2006).

3. Results 3.1. Altitudinal distribution The activity density distribution of ground-beetle populations along the studied altitudinal gradient is shown in Fig. 2. The

359

populations of C. interruptus were restricted to the middle climatic zone (600–1700 m). This population reached their maximum activity densities between 1200 and 1500 m, where the rainfall increases noticeably. The activity density values increased from the lower part of the cloud belt to the upper part of this zone.

3.2. Seasonal patterns of activity density, temperature and rainfall The maximum estimates recorded of activity density of C. interruptus and precipitation consistently occurred during the same seasons of cycle for both high and low zones (Figs. 3–5). The populations showed a long adult activity period from October to June. The emergence of adults was quite predictable. The first beetles were captured in early October (average soil surface temperature 22.5  C; range ¼ 15–30  C). Within a few weeks, the population had reached a high activity density. The population reached its first monthly maximum of the activity density after the fall in other words, the last part of autumn and the onset of winter (November and December): (1) Ravine of Badajoz – average soil surface temperature 18.5  C, range ¼ 12–25  C; (2) Hillside of Anocheza – average soil surface temperature 12  C, range ¼ 6–18  C; (3) Slope of Arafo – average soil surface temperature 20  C, range ¼ 4–16  C. In January the activity density decreased in most

Fig. 4. Seasonal distribution of activity density of Carabus (Nesaeocarabus) interruptus adults, minimum and maximum temperature and precipitation at Hillside of Anocheza. Monthly average and 95% CI (vertical bars) for all studied variables.

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Fig. 5. Seasonal distribution of activity density of Carabus (Nesaeocarabus) interruptus adults, minimum and maximum temperature and precipitation at Slope of Arafo. Monthly average and 95% CI (vertical bars) for all studied variables.

sampling plots. Subsequently, the activity density was recovered to the initial values of the seasonal cycle, increased and peaked again in February and March, when the thermal environment was fresher, though a small increase of the maximum temperature happens. Note that the seasonal-activity density pattern and seasonal-rainfall pattern were synchronous (Figs 3 and 5). Two main periods of activity density were clear from the successive peaks. These peaks were unrelated to the mean monthly temperature but each of the two periods of rising and falling activity density appeared to be related to relatively discrete periods of rainfall. Because activity density declined during dry periods and

increased after rain, it is suggested that the former caused a decline in activity, and the latter (rainfall) might then have triggered renew activity. The second peak was not observed through the seasonal changes in monthly average of activity density (95% CI) on the Ravine of Badajoz. From March to July, when temperature increased, the population reached its monthly minimum of the activity density. By July (Ravine of Badajoz – average soil surface temperature 25  C, range ¼ 12–38  C; Hillside of Anocheza – average soil surface temperature 19.5  C, range ¼ 11–28  C; Slope of Arafo – average soil surface temperature 20.75  C, range ¼ 12.5–29  C) the beetles were

Table 2 Values R, R squared, adjusted R squared, and the standard error in the correlation between the observed and predicted values of the dependent variable (activity density) for the three studied sites. Site

Variables entered

R

R Square

Adjusted R Square

Std. error of the estimate

Ravine of Badajoz 600–700 m

Minimum temperature ( C) Maximum temperature ( C) Precipitation (mm)

0.642 0.724 0.583

0.413 0.524 0.339

0.347 0.471 0.266

0.62040 0.55830 0.65789

Hillside of Anocheza 900–1700 m

Minimum temperature ( C) Maximum temperature ( C)

0.634 0.648

0.403 0.420

0.317 0.337

2.63138 2.59379

Slope of Arafo 900–1700 m

Minimum temperature ( C) Maximum temperature ( C) Precipitation (mm)

0.705 0.712 0.787

0.497 0.507 0.620

0.446 0.458 0.582

0.58843 0.58239 0.51157

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Table 3 Regression values of the analysis of variance for the three studied sites. The sum of squares, degrees of freedom, and mean square are displayed for two sources of variation, regression and residual. (Abbreviations: F – ANOVA F-test; df – degrees of freedom; Sig – probability; bold values indicate statistical significance at the 95% level or higher). Site

Variables entered

Ravine of Badajoz 600–700 m

Minimum temperature ( C)

Regression Residual Total

2.433 3.464 5.898

1 9 10

2.433 0.385

6.322

0.033

Maximum temperature ( C)

Regression Residual Total

3.092 2.805 5.898

1 9 10

3.092 0.312

9.920

0.012

Precipitation (mm)

Regression Residual Total

2.002 3.895 5.898

1 9 10

2.002 0.433

4.626

0.060

Minimum temperature ( C)

Regression Residual Total

32.662 48.469 81.131

1 7 8

32.662 6.924

4.717

0.066

Maximum temperature ( C)

Regression Residual Total

34.037 47.094 81.131

1 7 8

34.037 6.728

5.059

0.059

Minimum temperature ( C)

Regression Residual Total

3.416 3.462 6.879

1 10 11

3.416 0.346

9.867

0.010

Maximum temperature ( C)

Regression Residual Total

3.487 3.392 6.879

1 10 11

3.487 0.339

10.281

0.009

Precipitation (mm)

Regression Residual Total

4.262 2.617 6.879

1 10 11

4.262 0.262

16.285

0.002

Hillside of Anocheza 900–1700 m

Slope of Arafo 900–1700 m

Sum of squares

no longer active at the soil surface and entered diapause. During the warm, dry months (July–September) captures of ground-beetles in pitfall traps were rare. The parameter estimates from linear regression analysis between activity density, minimum and maximum temperature, and precipitation changed across different sampling sites (Tables 2–4). In general relatively high values were obtained for the coefficients of correlation. In the Slope of Arafo, the R was noticeably higher for the three variables, emphasizing the importance of rainfall. Consequently, the proportion of variation in the dependent variable (activity density) explained by the regression model (sample R2) was bigger, and therefore the model fits well the population. Even, higher values for the adjusted R squared were obtained. As it might be expected for a univariant model, a small regression sum of squares in comparison to the residual sum of

df

Mean square

F

Sig.

squares indicated that the model not accounts for most of variation in the dependent variable (Table 3). Very high residual sum of squares indicated that the model failed to explain a significant proportion of the observed variation in the activity density variable, and it might look for additional factors that help account for a higher proportion of the variation in the activity density variable. Only with the samples gathered in the zone of the Slope of Arafo, were obtained acceptable results in the analysis, especially for the rainfall and, in minor degree, the minimum temperature. In the Ravine of Badajoz also acceptable results were obtained for maximum temperature. The significance value of the F statistic to all variables of Slope of Arafo data was smaller than 0.05, then the temperature and rainfall variables explain well the variation in the activity density variable to this site. It was found in the present work that this quantity was

Table 4 Regression Coefficient estimated values between the observed and predicted values of the dependent variable (activity density) for the three studied sites. (Abbreviations: B – unstandardized coefficients; beta – standardized coefficients; t – Student’s t-test; Sig – probability; bold values indicate statistical significance at the 95% level or higher). Site

Variables entered

Ravine of Badajoz 600–700 m

Minimum temperature Maximum temperature Precipitation (mm)

Hillside of Anocheza (900–1700 m)

Minimum temperature Maximum temperature

Slope of Arafo 900–1700 m

Minimum temperature Maximum temperature Precipitation (mm)

B

Std. Error

(Constant) Minimum temperature (Constant) Maximum temperature (Constant) Precipitation

1.928 0.121 2.320 0.059 0.268 0.010

0.554 0.048 0.566 0.019 0.257 0.005

(Constant) Minimum temperature (Constant) Maximum temperature

8.554 0.622 12.791 0.381

1.872 0.287 3.587 0.169

(Constant) Minimum temperature (Constant) Maximum temperature (Constant) Precipitation

1.470 0.122 2.563 0.085 0.176 0.008

0.292 0.039 0.598 0.026 0.201 0.002

Beta 0.642 0.724 0.583

0.634 0.648 0.705 0.712 0.787

t

Sig.

3.483 2.514 4.099 3.150 1.044 2.151

0.007 0.033 0.003 0.012 0.324 0.060

4.568 2.172 3.566 2.249

0.003 0.066 0.009 0.059

5.035 3.141 4.288 3.206 0.877 4.036

0.001 0.010 0.002 0.009 0.401 0.002

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typically in the range 2  103–5  102, indicating that the success of a given model in reproducing the variation in the data was rather unlikely to be due to chance. Weakly superior values, to limit that it has been established, were only obtained in the Hillside of Anocheza, most likely due to an inadequate sampling frequency. The coefficient values of the estimated regression model between the observed and predicted values of the activity density can be observed in Table 4. The unstandardized coefficients B were the coefficients of the estimated model. For instance, the model parameters were estimated for the Ravine of Badajoz: activity density ¼ 1.928–0.121 minimum temperature; activity density ¼ 2.320–0.059 maximum temperature; activity density ¼ 0.268 þ 0.010 precipitation. The independent variables were measured in different units; consequently the standardized coefficients or betas were an attempt to make the regression coefficients more comparable. This way, it was possible to value and, consequently, compare the influence of our three independent variables (minimum and maximum temperature, and precipitation) on the dependent variable (activity density). The observed results emphasized the positive influence of rainfall on the activity density, with the highest value of beta and, in minor measure, of the temperature. The t statistics could help to determine the relative significance of each variable in the model. As a guide regarding useful predictors, most of the t values are well below 2 or above þ2. In general the results confirmed the statistical significance of the regression study: the relationship between activity density and precipitation was more consistent on the Slope of Arafo, and generally the relationships were noticeably higher for the three variables. 3.3. Seasonal variability of sex ratio The seasonal evolution of sex ratio over the experimental period is exhibited in Fig. 6, and Fig. 7 shows monthly distribution of male and female dissected number for the two sites considered in this part of the study. The parameter estimates from linear regression analysis between life history features and environmental variables are presented in Table 5. There was a significant negative relationship between males and females activity density and temperature. The male activity density increased up to the end of winter, after which estimates remained moderately stable until its entry into dormancy during the summer. The female activity density showed a similar pattern but fluctuated more widely and standard errors were larger. Overall the males were more active than the females during winter, and females were more active than males during spring, but these differences were not significant. Overall, the activity of males was higher than that of females, especially in Ravine of Badajoz, but females became more active in Hillside of Anocheza. However, the data did not show the range of male and female captures to be very different, although a higher relative proportion of females occurred in the plots of Anocheza. 3.4. Seasonal patterns of adult weight and egg production The two analyzed populations of C. interruptus, Ravine of Badajoz and Hillside of Anocheza, showed typical seasonal patterns of average dry weight in males and females and average number of eggs (Figs. 8 and 9). Analysis by dissection and palpation by pressing on the surface of the body indicated that the emergence of new adults (teneral females with soft elytra and light coloration, no trace of oocyte development or fat reserves; immature stages and female pre-reproductive periods with fully hardened cuticle but without eggs in ovaries; ovaries compact and white; often with well developed fat reserves; teneral males have no trace of testes, accessory glands or fat reserves; immature males with accessory

glands white; testes poorly developed; fat reserves often well developed; see Wallin, 1989a,b) occurred only in spring and the body dry weight peaked in April–May in both populations of C. interruptus. The weight decreased in most females and males from midspring to early summer. Both female and male dry weights were significantly small during the months of summer signalizing the outset of the diapause period. At start of autumn the weight recovered to the initial values of the cycle, increased and peaked in January. Again, the weight decreased in most females and males in February and early March. Relatively high monthly variation in the dry weight of males and females was recorded throughout the study period. Results of linear regression analysis indicated no statistically significant relationships among the dry weight and the climatic variables. In October females were considered mostly immature individuals and individuals in state of maturity. The maturation was almost completed during the months of November and December, and most of females dissected in January are mature. However, some of them exhibited empty ovaries, a state which becomes more frequent from December to March. Finally, during the spring, most dissected individuals were immature forms, indicating the origin of a new generation. This species prolonged its oviposition period from mid-autumn to early spring. The average number of eggs (in the Adephaga ovariole type – stage IV – we can find a few mature eggs but a great lot of immature eggs – or more correctly ovules) found in females was maximum in winter, and mature eggs peaked for January– March trimester when egg laying probably began (Figs. 8 and 9). There was therefore a negative relationship with seasonal fluctuations in temperature, with a maximum maturity period to average temperature of 12  C in Ravine of Badajoz and 8  C in Hillside of Anocheza. A significant linear regression between average number of eggs and temperature was observed (Table 5). The maximum number of eggs found within the ovaries of C. interruptus for each month in two sampling sites is presented in Table 6. The greatest maturation occurred from December to March, registering an absolute maximum of 6 eggs in January and March. The female’s abdomen became very swollen with eggs in this period. The eggs had a length of 4.9  0.127 mm (n ¼ 31). 4. Discussion Hutchinson (1957) presented a general framework for developing and evaluating habitat preference models of populations along environmental gradients. The models sought to explain why a species was present in some areas, but absent in others, and it was well established that there was an optimum value for each species in relation with the parameters that defined the habitats. The method consists on the identification of those environmental axes along which the species distribution curve best fitted a Gaussian response function (Fig. 10). Any well established population is equipped with distinct genetic adaptations that enable organisms to survive and reproduce in geographical ranges to which the population was exposed (Dobzhansky, 1948; Thompson, 2005; Moore et al., 2006). So, the phylogenetic assemblages must be adjusted to the model of adaptive radiation and selection of new habitats. The model involves specific morphological, physiological and behavioural modifications which enable them to live on adverse conditions, and therefore the ecological niche conservatism in evolutionary time would not be supported. The main evolutionary centre of Carabidae was probably the western and central part of what is nowadays the Equatorial Africa and, successive dispersals through geographic space ran from the tropics to areas with temperate and cold climates (Darlington,

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363

Fig. 6. Distribution of sex ratio (observation means of % females 95% confidence interval) of Carabus (Nesaeocarabus) interruptus during the reproductive cycle: (A) Ravine of Badajoz; (B) Hillside of Anocheza.

Fig. 7. Monthly distribution of dissected male and females of Carabus (Nesaeocarabus) interruptus for Ravine of Badajoz (A, B) and Hillside of Anocheza (C, D). Mean number  95% CI (vertical bars).

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364

Table 5 Regression Coefficient estimated values – summery – between the observed and predicted values of the dependent variables (life histories) for the two studied sites. (Abbreviations: F – ANOVA F-test; B – unstandardized coefficients; beta – standardized coefficients; Sig – probability; bold values indicate statistical significance at the 95% level or higher; n –number of cases). Site

Environmental variable

Life history feature

R2

F

Sig.

B

Sig.

Beta

n

Ravine of Badajoz

Minimum temperature

Average dry weigth(g)\ Average dry weigth(g)_ Average number of eggs % Females Number of males Number of females

0.260 0.002 0.424 0.043 0.573 0.735

1.409 0.006 2.947 0.178 10.74 22.22

0.301 0.944 0.161 0.695 0.011 0.002

0.152 0.098 3.427 20.19 13.03 7.396

0.016 0.069 0.055 0.734 0.002 0.001

0.510 0.044 0.651 0.206 0.757 0.858

6 5 6 6 10 10

Maximum temperature

Average dry weigth(g)\ Average dry weigth(g)_ Average number of eggs % females Number of males Number of females

0.000 0.519 0.034 0.036 0.629 0.846

0.001 3.242 0.143 0.149 13.59 43.81

0.981 0.170 0.725 0.719 0.006 0.001

0.107 0.043 2.025 17.73 14.68 8.458

0.111 0.237 0.364 0.803 0.001 0.001

0.013 0.721 0.186 0.190 0.793 0.920

6 4 6 6 10 10

Precipitation (mm)

Average dry weigth(g)\ Average dry weigth(g)_ Average number of eggs % Females Number of males Number of females

0.046 0.006 0.381 0.065 0.214 0.316

0.194 0.017 2.457 0.277 2.180 3.694

0.682 0.904 0.192 0.626 0.178 0.091

0.103 0.094 0.655 51.73 2.479 1.423

0.003 0.008 0.265 0.068 0.184 0.108

0.215 0.075 0.617 0.255 0.463 0.562

6 5 6 6 10 10

Minimum temperature

Average dry weigth(g)\ Average dry weigth(g)_ Average number of eggs % Females Number of males Number of females

0.285 0.155 0.413 0.024 0.001 0.280

2.785 1.103 4.915 0.175 0.004 2.725

0.139 0.334 0.062 0.689 0.954 0.143

0.108 0.097 0.591 54.65 1.814 3.252

0.001 0.001 0.014 0.009 0.046 0.001

0.534 0.394 0.642 0.156 0.023 0.529

9 8 9 9 9 9

Maximum temperature

Average dry weigth(g)\ Average dry weigth(g)_ Average number of eggs % Females Number of males Number of females

0.054 0.013 0.586 0.212 0.098 0.034

0.403 0.082 9.195 1.885 0.757 0.244

0.546 0.785 0.019 0.212 0.413 0.637

0.107 0.093 1.126 24.87 3.025 3.045

0.002 0.009 0.007 0.380 0.066 0.042

0.233 0.116 0.754 0.461 0.312 0.183

9 8 9 9 9 9

Hillside of Anocheza

1971; Erwin, 1979). Generalist groups occupy equatorial wetland centres and underwent special adaptations and geographic movements through time (Erwin, 1981). Ground-beetles in the tropics can present summer breeding and/or rainy season breeding, depending on soil humidity and/or soil temperature (Paarmann, 1979b, 1986). From this area, the different waves of dispersants moved both north- and southwards (see Walter and Lieth’s climatic diagrams to illustrate climates dealt with in this work; Walter and Lieth, 1967), including the Canary Islands (Erwin, 1981), where they found extensive environmental gradients, with mild temperatures and dry zones. The process of colonization of the island of Tenerife by groundbeetle species involved the search of favourable hydrothermal environments, both along the spatial axis as the seasonal axis. The population of C. interruptus was restricted to the middle climatic zone (600–1700 m, Fig. 2). The activity density values increased from the lower part of the cloud belt, to the upper part of the same zone. As expected for these species (de los Santos et al., 1985), there was a long adult activity period from October to June. Changes in activity density were strongly correlated with the temperature and humidity variations. The population reached its first monthly maximum of activity density after the fall in temperature by late autumn and early winter. The activity density recovered to the initial values of the cycle in January–March. During the warm, dry months (July–September) captures were rare. The weight increased from start of autumn and peaked in January. The maturation was completed during the months of November and December, so that in January the most dissected females were at a mature state. Finally, during the spring most dissected individuals (males and females) were immature forms, resulting from the eclosion of a new generation. Accordingly to our results, this species should be addressed to a winter breeder type.

Other species of genus Carabus studied in a similar habitat, but geographically separated, close to Canary Islands, was Carabus (Mesocarabus) riffensis Fairmaire, 1872 (Ruiz, 1998). The species was described for the western Rif Mountains in North-western Africa, including the population around the Ceuta city. In this region the climate is Mediterranean with a subhumid ombroclimate and the usual fogs (winter temperature average 12  C, range ¼ 8.7–15.2  C). C. riffensis was caught into winter (December–February), and continued to be caught during the spring and autumn at higher altitude. Consequently this species was characterized as a winter breeder, too. Life history studies done (field and laboratory) with Carabus (Rhabdotocarabus) melancholicus costatus Germar 1824, Carabus (Macrothorax) rugosus boeticus Deyrolle 1852 and Carabus (Mes˜ ana National ocarabus) lusitanicus latus Dejean 1826 near Don Park (southwest Spain) in typical Mediterranean grassland and pinewood areas (Lower Guadalquivir, 10–60 m a.s.l.) indicated that the main breeding period for these populations was winter and its maximum development during December and January (c. 15  C), coinciding with a high proportion of males in the average population (de los Santos et al., 1985). During the summer populations of the three species entered in aestivation dormancy. Similar life history patterns were found along the coastal zones of Iberian Peninsula both Mediterranean and Atlantic. Carabus (Macrothorax) rugosus celtibericus Germar, 1824 showed a winter breeding pattern in the Reserva Natural do Sapal de Castro Marim in Algarve, Portugal’s southernmost province (Serrano, 1988). Carabus (Macrothorax) rugosus boeticus Deyrolle, 1852 showed a possible autumn breeding pattern in the plain or to middle altitude of Tarragona province (northeast Spain) with a dry Mediterranean climate and an average daytime temperature for winter of

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Fig. 8. Seasonal patterns Carabus (Nesaeocarabus) interruptus life-history features in Ravine of Badajoz level site: dry weight (A) females, (B) males; average number of eggs (C). Average and 95% CI (vertical bars).

˜ ol, 1960). However, C. rugosus celtibericus showed 16  C (Espan a pattern of summer breeding (Salgado, 1978) across the flat and medium altitude of the Leon province (northwest Spain) characterized by a continental climate. Similarly, Carabus (Mesocarabus) lusitanicus Fabricius, 1801 showed an autumn breeding pattern on the lowland and the upper areas (1000 m a.s.l.) of the Tarragona province (northeast Spain) ˜ ol, 1960). Carabus (Mesocarabus) lusitanicus brevis Dejean, (Espan 1826, a widespread ground-beetle from lowlands to upper mountainous or subalpine regions of the Guadarrama Mountains (Central Mountain range), showed a trend similar in phenological phases. The climate is continental Mediterranean characterized by hot, sunny summers and winter rainy season, exhibiting great seasonal contrast in temperature (average temperature at 800–1.400 m a.s.l., 4  C winter, 15  C spring and autumn, 25  C summer). As the altitude increases the breeding time of the species and the corresponding peak of activity shifted from autumn to spring (Novoa, 1975). C. lusitanicus latus has also been captured in South-western of Leon province, from the lowlands to the upper areas (1000 m a.s.l.), i.e. continentalised Mediterranean climate to simply continental climate, so that the breeding pattern shifted from autumn to spring, respectively. Moreover, C. melancholicus costatus showed a winter breeding pattern in the Reserva Natural do Sapal de Castro Marim (Serrano, 1988). However, these subspecies showed a possible autumn breeding pattern in the Sierra de Bejar, at western part of the

Central Mountain range (Zaballos, 1986). This subspecies shifted the autumn breeding pattern to spring from stony and flooded riverside ground to high altitude in the Sierra de Guadarrama (eastern part of the Central Mountain range) (Novoa, 1975). Finally, this subspecies showed a pattern of autumnal breeding in the area of the banks of irrigation canals or swamps in Leon (Salgado, 1978). The Betic Mountain range (1000–1200 m a.s.l.) at South of the Iberian Peninsula presents a Mediterranean climate, but with a certain continental influence and the average temperature reached c. 15  C for mid-autumn. In this area, the results gained with the study of C. (Mesocarabus) dufouri Dejean, 1829 (Cardenas and Hidalgo, 2000) indicated that the species is a typical autumn breeder. The temporal activity of adult showed two maxima, the first between April and June and the second between October and December. The ovaries started differentiation and development after aestivation, the oviposition period began at the end of September and continued until the middle of January, and spent females were present in February and March. In addition, these results were supported by Gonza´lez et al. (1988) in Sierra Nevada National Park located in the Penibetic Mountain range (South-east Spain), although a bias toward summer was observed. Northward of Iberian Peninsula and consistent with the drop in the average temperature, especially in mountain areas, it could expect a more intense rainfall (amount also) over a larger annual period. Northern species changed their life cycles and consequently the breeding period. C. (Ctenocarabus) galicianus Gory, 1839 was

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366

Fig. 9. Seasonal patterns Carabus (Nesaeocarabus) interruptus life-history features in Hillside of Anocheza level site: dry weight (A) females, (B) males; average number of eggs (C). Average and 95% CI (vertical bars).

analysed in the Pontevedra province (Northwest of the Iberian Peninsula) at medium altitude (Andrade, 1980). The main activity period was from early March to the beginning of October, presence of teneral adults in July and August, eggs were mainly deposited from April to June period and first stage larvae occurred from April to August, but most frequently in May. Andrade (1980) classified

C. gallicianus as a spring breeder with adult and larvae overwintering in Galicia. Information was available on phenology of three Carabus species in the central region of the Peninsula. C. (Oreocarabus) amplipennis gestchmanni Vaucher de Lapouge, 1924 showed a summer breeding

Gaussian response curves: evolutionary inference

Table 6 Maximum number of mature eggs found in the ovaries of female Carabus (Nesaeocarabus) interruptus along its period of activity in two level sites studied. Capture month Numbers of Maximum number of dissected females mature eggs per female

Ravine of Badajoz

November January February March April June

7 8 4 8 7 2

3 3 4 6 5 0

Hillside of Anocheza October November December January March April May June July

4 24 11 8 9 15 9 10 1

0 1 1 6 5 2 0 1 0

Opt2

Opt3

Opt4

Population size

Site

Opt1

Environmental gradient Lower and upper tolerance limits:

ancestor

descendents

Fig. 10. The Gaussian response function: evolutionary inference across the environmental gradient. Based on the Gaussian response function of the ancestor, descendent species could potentially move their physical optima and tolerance limits of the response on the environmental gradient.

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Hidrothermal choice

Temperature

Pattern 4 Spring breeder

Pattern 2 Winter breeder

Pattern 5 Summer breeder

Pattern 3 Autumn breeder

Thermal increase Between zones 2-3

Thermal increase between zones 1-2

3. Hottest seasonal pattern

Pattern 1 Rainy season breeder

2. Cold-warm seasonal pattern Lowland

Lowland

Highland

1. Coldest seasonal pattern

Environmental gradients S

Latitudinal

Winter

Spring

N

E

Summer

Longitudinal

Autumn

W

367

normally preferred a hydrothermal environment of about 15–20  C (Thiele and Kolbe, 1962; Thiele, 1977; Ottesen, 1985, this study) and the typical mass of clouds (c. 1000 m a.s.l.) or the riverside environments. Perhaps the most obvious explanation for geographical differences in the patterns of Carabus species life history was the propensity in the evolution of the rhythms to preserve their preferred hydrothermal environment. Therefore, speciation took place in geographic instead of ecological dimensions and ecological differences might evolve later. Thus, the hydrothermal habitat preferences of a common ancestor could be conserved over time during dispersal by the genus Carabus, and changes in life history and seasonal activity among populations could result in vicariant species distributed over altitudinal and latitudinal geographic ranges (Fig. 11).

Winter

Seasonal period Fig. 11. The hydrothermal habitat preferences of a common ancestor would be conserved over time but changes in life history and seasonal activity among populations could result in vicariant species that are distributed at different altitudes and latitudes ranges.

pattern in the region of the Sierra de la Culebra (Zamora province) in the North-western Meseta Central (plateau), North-central Iberian Peninsula (Ferna´ndez and Salgado, 2004), boundary between the Atlantic climate and Mediterranean climate (average temperature around 15  C during spring–summer season). Farther North, this species showed a pattern of spring breeding in the eastern part of the Cantabrian Mountain range, but in greatest elevations of the Picos de Europa Mountain range (North of the Cantabrian Mountain range) the population shows a summer breeding pattern (Argibay and Salgado, 1991). Two more examples of Carabus life history studies were done in central and eastern Pyrenean Mountain range. C. (Archicarabus) pseudomonticola Vaucher de Lapouge, 1908 showed a spring breeding pattern and C. (Chrysocarabus) splendens Olivier, 1790 a summer breeding in several localities (c. 1000–1500 m a.s.l.) of the central Pyrenean Mountain range (Palanca, 1981; Jover et al., 1991). On the other hand, the last species showed a spring breeding pattern in forests of eastern Pyrenean Mountain range, Plateau de Sault, Aude, France (Brouat et al., 2006). Thiele (1977) defined summer breeders as ground-beetles with larval overwintering and no adult dormancy. Adaptations to short, cool summers include selection of warm habitats and microhabitats, melanism and cold hairiness coupled with basking behaviour, cryoproctectant and antifreeze agents, daily activity rhythm changes, and prolonged or abbreviated life cycles (Luff, 1978; Baust and Morrissey, 1977; Zachariassen and Husby, 1982; Matalin, 2007). Some summer breeding species were able to breed in two successive years (Luff, 1973), or breed in the early summer in the following year after that of adult emergence at high altitude (Butterfield, 1986, 1996), with imago and wintering larvae. It was suggested that summer reproduction with the wintering imagoes is a consequence of species adaptation to mountain environments (Khobrakova and Sharova, 2005). ‘‘Pulse’’ was the term that Erwin adopted (1981) for the combined natural history shifts through altitudinal and geographic environmental gradients experienced by a lineage of carabids. It was known that these species must lack the ability to evolve or change their hydrothermal environment in response to changing surrounding climate (Atkinson et al., 1987). According to Coope (1978), ground-beetles had not evolved morphologically over the last half million years but in most cases their temperature requirements had also remained the same. The Carabus species

Acknowledgements To all researchers of carabids that provided relevant information, without which it would have been possible to design and test the model worked in this article. To my colleagues of the University of La Laguna, Paco, Juan and Domingo for the help in the work field. Thanks to the Anonymous Reviewer for helpful suggestions and critical renew of my manuscript and for the suggested statistical analysis. I wish to thank Consejerı´a de Medio Ambiente for giving us permission to conduct the research on the Parque Nacional del Teide, Reserva Natural del Malpaı´s de Gu¨ı´mar and Barranco de Badajoz. The research was supported in part by grants through the University of La Laguna and Canary Govern. References Andrade, J., 1980. Notas sobre la biologı´a de Ctenocarabus galicianus Gory. Nouv. Rev. Entomol. 10, 19–28. Argibay, M., Salgado, J.M., 1991. Estudio faunı´stico y biogeogra´fico de la tribu Carabini (Coleoptera Carabidae) en la provincia fitogeogra´fica orocanta´brica. Elytron 5 (1), 275–283. Atkinson, T.C., Briffa, K.R., Coope, G.R., 1987. Seasonal temperatures in Britain during the past 22,000 years, reconstructed using beetle remains. Nature 325, 587–592. Barlow, C.A., 1973. Phenology and distribution of Carabus nemoralis (Mu¨ller) (Col. Carabidae) in Eastern Canada. Nat. Can. 100 (4), 361–369. Baust, J.G., Morrissey, R.E., 1977. Strategies of low temperature adaptation. In: Proc. XV Int. Congr. Entomol. Washington, D.C., 1976. American Society of Entomology, pp. 173–184. Benest, G., Cancela da Fonseca, J.P., 1980. Etude d´un peuplement de carabiques forestiers (Heˆtraie de La Tillaie, foreˆt de Fontainebleu). Pedobiologia 20, 343–359. Brandmayr, T.Z., Bonacci, T., Massolo, A., Brandmayr, P., 2004. Peace in ground beetle larvae: non-aggressive outcome in Chlaenius spp. larvae interactions. Ethol. Ecol. Evol. 16, 351–361. Brouat, C., Meusnier, S., Veyrier, R., Streiff, R., 2006. Haldane’s rule in Carabus: interspecific mating between Carabus punctatoauratus and Carabus splendens using experimental tests and molecular markers. Entomol. Exp. Appl. 120, 189–194. Butterfield, J.E.L., 1986. Changes in life-cycle strategies of Carabus problematicus over a range of altitudes in Northern England. Ecol. Entomol. 11, 17–26. Butterfield, J., 1996. Carabid life-cycle strategies and climate change: a study on an altitude transect. Ecol. Entomol. 21, 9–16. Cardenas, A.M., Hidalgo, J.M., 2000. Seasonal activity and reproductive biology of the ground beetle Carabus dufouri (Coleoptera, Carabidae). Eur. J. Entomol. 97, 329–338. Cloudsley-Thompson, J.L., 2001. Thermal and water relations of desert beetles. Naturwissenschaften 88 (11), 447–460. Cole, L.J., McCracken, D.I., Dennis, P., Downie, I.S., Griffin, A.L., Foster, G.N., Murphy, K.J., Waterhouse, T., 2002. Relationships between agricultural management and ecological groups of ground beetles (Coleoptera: Carabidae) on Scottish farmland. Agr. Ecosyst. Environ. 93 (1), 323–336. Coope, G.R., 1978. Constancy of insect species versus inconstancy of Quaternary environments. In: Mound, L.A., Waloff, N. (Eds.), Diversity of Insect Faunas. Symposia of the Royal Entomological Society of London, Number 9. Blackwell Scientific Publications, Oxford, pp. 176–187. Darlington, P.J., 1971. Interconnected patterns of biogeography and evolution. Proc. Natl. Acad. Sci. U.S.A. 68 (6), 1254–1258.

368

A. de los Santos Go´mez / Acta Oecologica 35 (2009) 355–369

˜ o de trampa de de los Santos, A., Montes, C., Ramı´rez-Dı´az, L., 1982. Un nuevo disen caı´da para el estudio de poblaciones de coleo´pteros terrestres de superficie. Mediterra´nea 6, 93–99. de los Santos, A., Montes, C., Ramı´rez-Dı´az, L., 1985. Ciclos de vida de algunas poblaciones de Cara´bidos (Col. Carabidae) de dos ecosistemas del bajo Gua˜ a) con especial referencia a Steropus globosus ebenus Quens, dalquivir (S.O. Espan 1806. Rev. Ecol. Biol. Sol. 22 (1), 75–95. de los Santos, A., Estefanı´a, Y., Lo´pez, R.J., de Nicola´s, J.P., 1991. Variacio´n de la diversidad de Cara´bidos (Col. Carabidae) sobre un gradiente ambiental en Tenerife (Islas Canarias). In: Pineda, F.D., Casado, M.A., de Miguel, J.M., Montalvo, J. (Eds.), Diversidad Biolo´gica. Biological Diversity. Fundacio´n Ramo´n Areces, ADENA-WWF. Madrid and SCOPE, Paris, pp. 131–134. de los Santos, A., Go´mez-Gonza´lez, L.A., Alonso, C., Arbelo, C.D., de Nicola´s, J.P., 2000. Adaptive trends of darkling beetles (Col. Tenebrionidae) on environmental gradients on the island of Tenerife (Canary Islands). J. Arid Environ. 45 (1), 85–98. de los Santos, A., Ferrer, F.J., de Nicola´s, J.P., 2002. Habitat selection and assemblage structure of darkling beetles (Col. Tenebrionidae) along environmental gradients on the island of Tenerife (Canary Islands). J. Arid Environ. 52, 63–85. de los Santos, A., Ferrer, F.J., de Nicola´s, J.P., 2006. Thermal habitat and life history of two congeneric species of darkling beetles (Coleoptera: Tenebrionidae) on Tenerife (Canary Islands). J. Arid Environ. 65, 363–385. Dennis, P., 2003. Sensitivity of upland arthropod diversity to livestock grazing, vegetation structure and landform. J. Food Agr. Environ. 1 (2), 301–307. Deuve, Th., 2004. Illustrated catalogue of the genus Carabus of the world (Coleoptera: Carabidae), Entomology Faunistica No. 34, Pensoft Series Faunistica No 34. Pensoft Publishers, Sofia. Dobzhansky, T., 1948. Genetics of natural populations. XVI. Altitudinal and seasonal changes produced by natural selection in certain populations of Drosophila pseudoobscura and Drosophila persimilis. Genetics 33, 158–176. Do¨ring, T.F., Krompb, B., 2003. Which carabid species benefit from organic agriculture?dA review of comparative studies in winter cereals from Germany and Switzerland. Agric. Ecosys. Environ. 98, 153–161. Ernsting, G., Isaaks, A., 2000. Ectotherms, temperature, and trade-offs: Size and number of eggs in a carabid beetle. Am. Nat. 155, 804–813. Erwin, T.L., 1979. Thoughts on the evolutionary history of ground beetles: hypotheses generated from comparative faunal analyses of lowland forest sites in temperate and tropical regions. In: Erwin, T.L., Ball, G.E., Whitehead, D.R., Halpern, A.L. (Eds.), Carabid Beetles: Their Evolution, Natural History and Classification. Dr. W. Junk bv Publishers, The Hague, pp. 539–592. Erwin, T.L., 1981. Taxon pulses, vicariance, and dispersal: an evolutionary synthesis illustrated by carabid beetles. In: Nelson, G., Rosen, D.E. (Eds.), Vicariance Biogeography: A Critique. Columbia University Press, New York, pp. 159–196. ˜ ol, F., 1960. Los Carabus de la provincia de Tarragona (Col. Carabidae). Graellsia Espan 18, 51–58. Evans, W.G., 1983. Habitat selection in the Carabidae. Coleopts. Bull. 37 (2), 164–167. Ferna´ndez, M.M., Salgado, J.M., 2004. Recolonization of a burnt pine forest (Pinus pinaster) by Carabidae (Coleoptera). Eur. J. Soil Biol. 40, 47–53. Filippov, B. Yu., 2006. Seasonal aspects of the life cycles of Carabus granulatus and C. glabratus (Coleoptera, Carabidae) in the northern taiga. Entomol. Rev. 86 (7), 751–759. Font Tullot, I., 1956. El tiempo atmosfe´rico en las Islas Canarias, Servicio Meteorolo´gico Nacional. Ministerio de Educacio´n y Ciencia and Gobierno de Canarias, Madrid. Gilbert, O., 1956. The natural histories of four species of Calathus (Coleoptera, Carabidae) living on sand dunes in Anglesey, North Wales. Oikos 7 (1), 22–47. Gist, C.S., Crossley, D.A., 1973. A method for quantifying pitfall trapping. Environ. Entomol. 2, 951–952. Gonza´lez, A.L., Tinaut, J.A., Go´mez, R., 1988. Evolucio´n estacional de la entomofauna del suelo en un robledal (Quercus pyrenaica Willde) de Sierra Nevada. Acta III Congr. Ibe´rico Entomol., 557–576. Granada. Greenslade, P.M.J., 1968. Habitat and altitude distribution of Carabidae (Coleoptera) in Argyll, Scotland. T. Roy. Ent Soc. London 120, 39–54. Guillermain, M., Loreau, M., Daufresne, T., 1997. Relationships between the regional distribution of carabid beetles (Coleoptera, Carabidae) and the abundance of their potential prey. Acta Oecol. 18, 465–483. Heerdt, P.F. Van, Blokhuis, B., Haaften, C. Van, 1976. The reproductive age cycle composition of a population of Pterostichus oblongopunctatus (Fabricius) in the Netherlands (Col. Carabidae). Tijdschr. Entomol. 119, 1–13. Heydemann, B., 1957. Die Biotopstruktur als Raumwiderstand und Raumfu¨lle fu¨r die Tierwelt. Verh. Dtsch. Zool. Ges. 1956, 332–347. Houston, W.W.K., 1981. The life cycles and age of Carabus glabratus Pykull and C. problematicus Herbst (Col. Carabidae) on moorland in northern England. Ecol. Entomol. 6, 263–271. Hutchinson, G.E., 1957. Concluding remark. Cold Spring Harb. Sym. Quant. Biol. 22, 415–427. Jansen, M.J.W., Metz, J.A.J., 1979. How many victims will a pitfall make? Acta Biotheor. 28, 98–122. Joppa, F., Reuterb, H., 2005. Dispersal of carabid beetlesdemergence of distribution patterns. Ecol. Model 186, 389–405. Jørum, P., 1985. Life cycle and phenology of Carabus problematicus Herbst, 1786 in Denmark (Coleoptera, Carabidae). Entomol. Medd. 53, 27–30. Jover, L., Ascaso, C., Pedrochi, C., 1991. Diversidad de cara´bidos en los sistemas ˜ a (Jaca, Huesca). In: Pineda, F.D., Casado, M.A., de forestales de San Juan de la Pen

Miguel, J.M., Montalvo, J. (Eds.), Diversidad Biolo´gica. Biological Diversity. Fundacio´n Ramo´n Areces, ADENA-WWF. Madrid and SCOPE, Paris, pp. 135–137. Khobrakova, L.T., Sharova, I.K., 2005. Life cycles of ground beetles (Coleoptera, Carabidae) from the mountain taiga and mountain forest–steppe in the Eastern Sayan. Biol. Bull. 3 (6), 571–575. Lenski, R.E., 1982. Effects of forest cutting on two Carabus species: evidence for competition for food. Ecology 63 (5), 1211–1217. Loreau, M., 1985. Annual activity and life cycles of carabid beetles in two forest communities. Holarctic Ecol. 8, 228–235. Lo¨vei, G.L., Sunderland, K.D., 1996. Ecology and behaviour of ground beetles (Coleoptera: Carabidae). Annu. Rev. Entomol. 41, 231–256. Luff, M.L., 1973. The annual activity pattern and life cycle of Pterostichus madidus (F.) (Coleoptera, Carabidae). Ent. Scand. 4, 259–273. Luff, M.L., 1975. Some features influencing the efficiency of pitfall traps. Oecol. Berlin 19, 345–357. Luff, M.L., 1978. Diel activity patterns of some field Carabidae. Ecol. Entomol. 3, 53–62. Matalin, A.V., 2007. Typology of life cycles of ground beetles (Coleoptera, Carabidae) in Western Palaearctic. Entomol. Rev. 87, 947–972. Mayr, E., Diamond, J.M., 2001. The Birds of Northern Melanesia. Oxford University Press, Oxford. Migliorini, M., Petrioli, A., Bernini, F., 2002. Comparative analysis of two edaphic zoocoenoses (Oribatid mites and Carabid beetles) in five habitats of the Pietraporciana’ and ‘Lucciolabella’ Nature Reserves (Orcia Valley, central Italy). Acta Oecol. 23, 361–374. Moore, L.G., Shriver, M., Bemis, L., Vargas, E., 2006. An evolutionary model for identifying genetic adaptation to high altitude. Adv. Exp. Med. Biol. 588, 101–118. Niemela¨, J., Haila, Y., Halme, E., Pajunen, T., Punttila, P., 1989. The annual activity cycle of carabid beetles in the southern Finnish taiga. Ann. Zool. Fennici. 26, 35–41. Novoa, F., 1975. Los Carabidae de la Sierra de Guadarrama. I. Inventario de especies y biogeografı´a. Bol. Real Soc. Esp. Hist. Nat., (Biol.) 73, 99–147. Ottesen, P.S., 1985. Diel activity patterns of South Scandinavian high mountain ground beetles (Coleoptera, Carabidae). Holarctic Ecol. 8, 191–203. Paarmann, W.,1979a. A reduced number of larval instars, as an adaptation of the desert carabid beetle Thermophilum (Anthia) sexmaculatum F. (Coleoptera, Carabidae) to its arid environment. Miscell. Papers, L.H. Wageningen, vol. 18, pp. 113–117. Paarmann, W., 1979b. Ideas about the evolution of the various annual reproduction rhythms in carabid beetles of the different climatic zones. In: den Boer P.J., Thiele H.U., Weber, F. (Eds.), On the evolution of behaviour in Carabid beetles. Miscell. Papers L.H. Wageningen 18, pp. 119–132. Paarmann, W., 1986. Seasonality and its control by environmental factors in tropical ground beetles (Col. Carabidae). In: den Boer, P.J., Luff, M.L., Mossakowski, D., Weber, F. (Eds.), Carabid Beetles. Their Adaptations and Dynamics. Proc. XVII Int. Congr. Entomol. Hamburg 1984. Gustav Fischer, Stuttgart, New York, pp. 157–171. Paarmann, W., 1990. Poecilus lepidus Leske (Carabidae, Coleoptera), a species with the ability to be an spring and autumn breeder. In: Stork, N. (Ed.), The Role of Ground Beetles in Ecological and Environmental Studies. Intercept Limited, Andover, Hampshire, pp. 259–275. Palanca, A., 1981. Aspectos faunı´sticos y ecolo´gicos de los cara´bidos altoaragoneses, Serie Universitaria Fundacio´n Juan March, No. 147, Madrid. Peterson, A.T., Sobero´n, J., Sa´nchez-Cordero, V., 1999. Conservatism of ecological niches in evolutionary time. Science 285, 1265–1267. Purtauf, T., Roschewitz, I., Dauber, J., Thies, C., Tscharntke, T., Wolters, V., 2005. Landscape context of organic and conventional farms: influences on carabid beetle diversity. Agric. Ecosyst. Environ. 108, 165–174. Pru¨ser, F., Bru¨ckner, M., Mossakowski, D., 2000. Colonisation of Canary Islands by Carabus species: evidence from different character complexes. In: Brandmayr, P., Casale, A., Lo¨vei, G.L., Vigna Taglianti, A. (Eds.), Natural History and Applied Ecology of Carabid Beetles. Pensoft, Sofia, pp. 45–52. Quintana, M., de los Santos, A., Montes, C., Ramı´rez-Dı´az, L., 1985. Modificaciones al modelo de trampa de caı´da ‘‘sistema de embudos compartimentados’’ para el estudio de comunidades de coleo´pteros terrestres de superficie. Bolm. Soc. Port. Entomol. 4 (1), 25–30. Refseth, D., 1984. The life cycles and growth of Carabus glabratus and C. violaceus in Budalen, central Norway. Ecol. Entomol. 9, 449–455. Ribera, I., Foster, G.N., Downie, I.S., McCraken, D.I., Abernethy, V.J., 1999. A comparative study of the morphology and life traits of Scottish ground beetles (Coleoptera, Carabidae). Ann. Zool. Fennici 36, 21–37. Ruiz, J.L., 1998. Chorological and autoecological notes on the Riffian endemic Carabus (Mesocarabus) riffensis Fairmaire, 1872 (Coleoptera: Carabidae). Giorn. Ital. Entomol. 9 (48), 123–125. Salgado, J.M., 1978. Los Carabus de la provincia de Leo´n (Col. Carabidae). Bol. Estac. Cent. Ecol. 7 (13), 73–86. Serrano, A.R.M., 1988. Contribuiça˜o para o conhecimento dos coleo´pteros da Reserva Natural do Sapal de Castro Marim – Vila Real de Santo Anto´nio. II. Os carabı´deos. (Coleoptera, Carabidae), Colecça˜o Naturaleza e Paisagem n 5, Serviço Nacional de Parques, Reservas e Conservaça˜o da Natureza, Lisboa. Serrano, J., 2003. Cata´logo de los Carabidae (Coleoptera) de la Penı´nsula Ibe´rica. Monografias SEA, Sociedad Entomolo´gica Aragonesa, 9, Zaragoza. Sota, T., 1996. Altitudinal variation in life cycles of carabid beetles: life-cycle strategy and colonization in Alpine Zones. Arctic Alpine Res. 28 (4), 441–447. Sparks, T.H., Buse, A., Gadsden, R.J., 1995. Life strategies of Carabus problematicus (Coleoptera, Carabidae) at different altitudes on Snowdon, North Wales. J. Zool., Lond. 236, 1–10.

´ mez / Acta Oecologica 35 (2009) 355–369 A. de los Santos Go SPSS, 2006. SPSS for Windows 15. SPSS Inc., Chicago, Illinois, USA. Thiele, H.-U., 1977. Carabid Beetles in their Environments. Spinger Verlag, Berlin. Thiele, H.-U., Kolbe, W., 1962. Beziehungen zwischen bodenbewohnenden Ka¨fern und Pflanzengesellschaften in Wa¨ldern. Pedobiologia 1, 157–173. Thompson, J.N., 2005. The Geographic Mosaic of Coevolution. University of Chicago Press, Chicago. Tretzel, E., 1955. Technik und Bedeutung des Fallenfages fu¨r o¨kologische Untersuchungen. Zool. Anz. 155, 276–287. Turin, H., Penev, L., Casale, A. (Eds.), 2003. The Genus Carabus in Europe. A Synthesis. Pensoft Publishers & European Invertebrate Survey, Sofia & Leiden.

369

Wallin, H., 1989a. Habitat selection, reproduction and survival of two small carabid species on arable land: a comparison between Trechus secalis and Bembidion lampros. Holarct. Ecol. 12, 193–200. Wallin, H., 1989b. The influence of different age classes on the seasonal activity and reproduction of four medium-sized carabid species inhabiting cereal fields. Holarct. Ecol. 12, 201–212. Walter, H., Lieth, H., 1967. Klimadiagram-Weltatlas. VEB Gustav Fischer Verlag, Jena. Zaballos, J.P., 1986. Notas fenolo´gicas sobre los Carabidae (Coleoptera) de la Penı´nsula Ibe´rica. An. Biol. 7(Biol. Anim. 2), 11–15. Zachariassen, K.E., Husby, J.A., 1982. Antifreeze effect of thermal hysteresis agents protects highly supercooled insects. Nature 298, 865–867.