ARTICLE IN PRESS
Journal of
Arid
Environments
Journal of Arid Environments 65 (2006) 363–385
www.elsevier.com/locate/jnlabr/yjare
Thermal habitat and life history of two
congeneric species of darkling beetles
(Coleoptera: Tenebrionidae) on Tenerife
(Canary Islands)
A. De Los Santosa,, F. Ferrera, J.P. De Nicolása, T.O. Cristb
a
Department of Ecology, University of La Laguna. c/Astrofı´sico Fco. Sánchez, s/n. 38206-La Laguna. Sta.
Cruz de Tenerife, Canary Islands, Spain
b
Department of Zoology, Miami University. Oxford, OH 45056, USA
Received 19 July 2004; received in revised form 13 July 2005; accepted 2 August 2005
Available online 21 September 2005
Abstract
Relationships among minimum temperature, activity density, and life history were
examined in two species of the genus Pimelia (Coleoptera: Tenebrionadae) on two extreme
sites along an elevation range on Tenerife. On highest site, P. ascendens presented a 2-year life
cycle with larvae and adults overwintering, spring breeding, and emergence of adults in
summer. Changes in adult activity density were directly proportional to the minimum
temperature. On lower site, P. canariensis was characterized by a 1-year life cycle, without
larval or adult overwintering, winter breeding, and emergence of adults throughout the year.
In this species, changes in adult activity density were inversely proportional to the minimum
temperature. However, both species were eurythermic, displaying considerable overlap in
adult preferred temperatures, which were 12–13 1C. In addition, the activity density patterns
were different when analysed at broad scale and fine scales.
Our results suggest conservatism of thermal optima over broad-scale environmental
changes that occur with elevation. The stabilization in a constant thermal environment is
Corresponding author. Tel.: +34 22 318362; fax: +34 22 318311.
E-mail addresses: [email protected] (A. De Los Santos), [email protected] (F. Ferrer), [email protected]
(T.O. Crist).
0140-1963/$ - see front matter r 2005 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jaridenv.2005.08.001
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achieved by behavioral, physiological, and developmental adjustments in the two species
of Pimelia.
r 2005 Elsevier Ltd. All rights reserved.
Keywords: Environmental correlates; Life cycle and reproductive traits; Population abundance; Spatial
and temporal scales
1. Introduction
Climatic extremes are often avoided by burrowing habits coupled with circadian
and seasonal-activity rhythms, as well as reproductive phenology. Several species of
desert darkling beetles (Family Tenebrionidae) are nevertheless able to withstand
thermal extremes that would rapidly cause the death of most other arthropods
(Cloudsley-Thompson, 2001). The lethal temperatures for some darkling beetles
encountered in extreme environments are frequently very high (CloudsleyThompson and Crawford, 1970). Furthermore, microhabitat selection may be
substantially influenced by each species’ preference and tolerance of field
temperature regimes (Parmenter et al., 1989). Tenebrionids select microhabitats
and activity times based on the thermal regimes rather than humidity (Hamilton,
1971; Whicker and Tracy, 1987; Parmenter et al., 1989; de los Santos et al., 2002b).
Physiological and morphological adaptations affect their temperature relationships
(Hamilton, 1973; Bartholomew et al., 1985).
In arid and semi-arid environments where temperature is highly variable, darkling
beetles select optimal thermal environments in relation to their life-history features
(Hamilton, 1971; Henwood, 1975; McClain and Seely, 1985; Røskaft et al., 1986;
Ward and Seely, 1996). Darkling beetle populations have adaptation syndromes to
live in arid and semi-arid ecosystems and their life histories are linked to hot seasons in
those areas with fluctuating climates (Brun, 1970; Knor, 1975; Allsopp, 1980a; de los
Santos et al., 1988). Adult emergence, individual vagility, and population sizes are all
related with the environmental temperature (Nicolson et al., 1984; Whicker and
Tracy, 1987; Parmenter et al., 1989; Crist and Wiens, 1995; de los Santos et al., 2002a).
In darkling beetles, different life cycle patterns have been identified in different
arid and semi-arid zones according to daily and seasonal activity as well as ecological
affinities (Brun, 1970; Knor, 1975; Allsopp, 1980a; de los Santos et al., 1988). There
are two broad classes of thermal strategies employed by darkling beetles in desert
areas. Almost all of the diurnal forms so far studied are living a maxithermal
strategy. The individuals are highly mobile, and it is primarily the ability to rapidly
seek out proper thermal microhabitats that allows them to maintain their body
temperature at high levels for much of the day (Hamilton, 1973; Henwood, 1975).
Maxithermic behavior would enhance foraging activity and increase the rates of
important metabolic functions (Bursell, 1964; Crawford, 1988). The nocturnal forms
operate in a thermal environment that is 10–20 1C cooler (Hamilton, 1971; Holm and
Edney, 1973; Henwood, 1975). Hence the necessity for thermal shelters provided by
vegetation structure (Parmenter et al., 1989) or by actively digging into sand during
the day (Cloudsley-Thompson, 1975).
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The description of the physical location of an organism is influenced by the
observational scale of the investigator (McIntyre, 1997). In this study of tenebrionid
beetles, we distinguish between fine-scale habitat concepts (i.e. microhabitat) that are
relevant to individual activity (Cloudsley-Thompson, 1974) and broad-scale
concepts of geographic range that are relevant to population distribution and
abundance (Brown, 1984). The island of Tenerife shows a broad altitudinal climatic
gradient (broad scale) within which the microenvironments (fine scale) change in
terms of soil, vegetation and topography, as has previously been shown for other
ecosystems (Tanner and Packham, 1965; Rickard, 1970). It is expected that darkling
beetle populations would show particular altitudinal distributions in terms of their
physiological optima (thermal) and tolerance limits, whereas individual movements
among microenvironments affects the distribution and daily activity of individuals
within a habitat (Hadley, 1970; Robinson and Seely, 1980; Crist et al., 1997).
Our report outlines the results of one part of an extensive study concerning the
biology and ecology of the endemic darkling beetles of ecosystems located on the
S.E. (leeward) slope of the island of Tenerife. The great abundance of two congeneric
species (Family Tenebriondae: Pimelia ascendens Wollaston and Pimelia canariensis
Brullé) made possible our comprehensive research about activity density, life-history
characteristics, and thermal habitat of darkling beetles along elevational gradients.
Taxonomic studies identify them as different species (Español, 1961; Oromı́, 1982),
but molecular evidence from mitochondrial genes suggests that the two species may
comprise as many as co-occurring species on the island of Tenerife (Juan et al., 1996,
1997). The population of P. canariensis was distributed exclusively in the coastal
environments of the Island and the population of Pimelia ascendens occupied the
upper level of the Island (de los Santos et al., 2002b).
We explored the relationships between minimum temperature and activity density
in relation with the variability of life histories of these two species at two extreme
sites along an elevation range on Tenerife. To analyse the relationships with the
activity density, we selected the minimum temperature as a predictor variable
because both species are nocturnal (Ottesen and Sømme, 1987). However, our
studies of their circadian rhythms suggest that when the minimum temperature is
o0 1C in early spring at higher elevations then P. ascendens is active during the day.
We hypothesize that these two species show conservatism of ecological niches in
evolutionary time (Peterson et al., 1999; Peterson and Vieglais, 2001). This
hypothesis predicts that fundamental environmental preferences of a species change
slowly over time by natural selection. Peterson et al. (1999) concluded that
conservatism of environmental preference over several million years indicates
that speciation takes place in geographic instead of ecological dimensions and that
ecological differences evolve later. Thus, during speciation of the genus Pimelia
along the environmental gradient in the island of Tenerife, the thermal 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.
These broad-scale patterns imposed by geographic, environmental, and phylogenetic constraints are complicated by fine-scale patterns of activity and habitat use.
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Perhaps not surprisingly, observations at different scales reach different conclusions
on darkling beetle associations and the environmental factors (McIntyre, 1997; de
los Santos et al., 2002b). Our approach assumes that spatial variation in activity
density is primarily reflected by the variation in the thermal environment (e.g.
Christian and Tracy, 1981), but our analysis considers biotic and climatic variables
at different spatial and temporal scales.
2. Materials and methods
2.1. Study sites
Fieldwork was undertaken along an altitudinal transect, located on the SE
(leeward) slope of the island of Tenerife. Our study was restricted to the lower site
(0–100 m asl) and the upper site (1100–2400 m asl) because these were the distribution
areas of two species of the genus Pimelia (de los Santos et al., 2002b). The climate for
the two sites is dry temperate (Fernandopullé, 1976), and the higher site has more
severe winters.
In the lower site, the dominant vegetation type is xerophytic scrub, rich in
succulents, especially cactiform or dendroid spurges (e.g. Euphorbia canariensis L.,
E. balsamifera Ait., E. obtusifolia Poir.), and Plocama pendula Ait. In the upper site
of the island, two representative zones were chosen. The first (1500–2000 m asl) is
woodland composed of Pinus canariensis Chr. Sm. ex DC. in Buch, with an
understory dominated by the shrub legume Chamaecytisus proliferus (L.fil.) Link.
The second zone, between 2000 and 2300 m, is dominated by broom Spartocytisus
supranubius (L. fil.) Webb et Berth., laburnum Adenocarpus viscosus (Willd.) Webb
et Berth., and an annual mustard Descurainia bourgaeana (Fourn.) O.E. Schulz.
2.2. Beetle sampling
A total of 21 plots were sampled, 12 plots (Malpaı́s de Güı́mar) in the lower site
and nine plots (Izaña, Arafo and Cañadas del Teide) in the upper site (Table 1).
Beetle populations in each plot were sampled with pitfall traps for 1 year. In each
plot, a rectangular grid at 3 8 traps was established, with each trap 10 m apart.
A funnel trap was used (de los Santos et al., 1982a) in which neither baits nor
killing–preserving agents were used; these traps were emptied weekly.
During the sampling period, temperatures, humidity, and rainfall were recorded
using a maximum–minimum thermohygrometer and pluviometer placed on the soil
surface at each plot. A volcanic stone roof protected each thermohygrometer.
2.3. Laboratory processing
A fraction of the specimens captured weekly was taken to the laboratory for
analysis. The specimens were separated on the same day by species in a humid
outdoor insectary. Part of the sample was fixed and dissected in 70% alcohol to
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Table 1
Collection plots refer to site, zone, elevation and sampling periods
Site
Zone
Plot
Elevation (m asl)
Sampling periods
1
1
1
1
1
1
1
1
1
1
1
1
2
2
2
2
2
2
2
2
2
Malpaı́s
Malpaı́s
Malpaı́s
Malpaı́s
Malpaı́s
Malpaı́s
Malpaı́s
Malpaı́s
Malpaı́s
Malpaı́s
Malpaı́s
Malpaı́s
Arafo
Izaña
Izaña
Izaña
Izaña
Izaña
Izaña
Cagadas
Izaña
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
36
46
51
50
54
53
56
59
73
76
79
83
1100
1700
1925
1950
2050
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
21 May 01–20 May 02
21 May 01–20 May 02
21 May 01–20 May 02
21 May 01–20 May 02
9 May 88–l May 89
16 Dec 88–31 Oct. 89
10 Jun 85–14 Feb 86
10 Jun 85–14 Feb 86
10 Jun 85–14 Feb 86
10 Jun 85–14 Feb 86
10 Jun 85–9 May 86
7 May 88–30 Apr 89
10 Jun 85–14 Feb 86
The site 1 ‘lower site (0–100 m)’ refers to distribution area of P. canariensis and site 2 ‘upper site
(1100–2400 m)’ refers to distribution area of P. ascendes in Tenerife. Zones refer to the habitat types where
a set of plots were located along the altitudinal transect in the Southeast of Tenerife.
determine sex and ovarian maturation using established criteria (Gilbert, 1956;
Barlow, 1973; Luff, 1973; Heerdt et al., 1976; Allsopp, 1980b). 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 1C for 24 h.
The remaining beetles were segregated into copulating pairs and placed in
individual plastic pots (5 cm diameter, 10 cm deep) with a mesh cover, holes in the
base, and half-filled with sieved soil and abundant food (bran, moist bread, fruit). At
weekly intervals, each female was transferred to a fresh pot, and egg-laying rate in
each pot was counted by using a stereoscopic micrometer.
2.4. Statistical analyses
Population estimates for pitfall traps method were expressed in terms of activity
density (Tretzel, 1955; Heydemann, 1957), which reflects the number of beetles that
were more through the study area. We conducted an analysis of linear regression
between activity density and the minimum temperature. Different spatial and
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temporal levels were considered in the analysis. At the broad scale, captures were
pooled among plots within a site, and at the fine scales analyses were conducted
separately for each plot. Different levels of temporal aggregation were 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). The number of beetles in pitfall traps
is function of both individual activity and population density; thus, the analysis
focuses on how the activity density changes weekly and seasonally within the life
cycle of both species.
The monthly average variation of life-history features was analysed using a oneway ANOVA test and post hoc procedures (Program SPSS for Windows Version
12.0). Monthly pairwise comparisons have been made with LSD or Tamhane’s T2
post hoc procedures depending upon the result of homogeneity test (Hochberg and
Tamhane, 1987). When the variances of the dependent variable are not equal across
groups, the results of the ANOVA are questionable. In this case, the Welch and
Brown–Forsythe statistics are alternatives to the usual F-test in such a case (Welch,
1951; Brown and Forsythe, 1974).
3. Results
3.1. Life histories features
The two Pimelia species differed in seasonal patterns of emergence, adult weight
in females and males, sex ratio, average egg production, and laying rates (Figs. 1
and 2). The results of the one-way ANOVA analysis and the pairwise comparisons of
the months for post hoc procedures are presented in Table 2.
In P. canariensis, emergence of new adults began in spring and peaked in October,
both female and male dry weights during the months of summer were significantly
smaller than those in autumn and winter (Table 2). The average number of immature
and mature eggs found in females was greatest in fall and winter, and mature eggs
peaked in February and March (Fig. 2). In both cases, the average number of eggs
differs significantly among almost every month (Table 2). Mature egg production was high in winter when egg laying began. This species prolonged its oviposition period until end of spring and peaked in June. The sex ratio was close to 1:1
during most months and the F-test showed that the differences were not significant
(Table 2).
In P. ascendens, emergence occurred only in summer (Fig. 1). From midsummer
to the starting of autumn, the weight decreased in most females (it begins the period
of diapause). From start of spring the body weight was recovered to the initial values
of the cycle, increased and peaked in July (F-test showed significant differences;
Table 2). The monthly variation of dry weight in males was quite high and F-test was
not significant. The average number of immature eggs found in females was greatest
in April, and mature eggs peaked in July (Fig. 2). In both cases the Welch and
Brown–Forsythe statistics was significant (Table 2). The egg-laying rate increased
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Pimelia canariensis
369
Pimelia ascendens
35
New emergence
(no. of individuals)
30
25
20
15
10
5
0
Average dry weight (g)
0·30
males
males
Females
Females
0·28
0·26
0·24
0·22
0·20
0·18
0·16
Average dry weight (g)
0·30
0·28
0·26
0·24
0·22
0·20
0·18
0·16
Jan Mar May July Sept Nov
Feb April June Aug Oct Dec
Jan Mar May July Sept Nov
Feb April June Aug Oct Dec
Fig. 1. Seasonal patterns of life-history features: adult emergence, and average dry weight in males and
females of P. canariensis (left column) and P. ascendens (right column). Vertical lines are the 95% CI for
each mean.
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Pimelia canariensis
Pimelia ascendens
Jan Mar May July Sept Nov
Feb April June Aug Oct Dec
Jan Mar May July Sept Nov
Feb April June Aug Oct Dec
90
Females (%)
80
70
60
50
40
30
20
Average number of
inmature eggs
10
9
8
7
6
5
4
3
2
1
0
Laying rate
(mean no. of eggs per week)
10
9
8
7
6
5
4
3
2
1
0
Average number of
mature eggs
10
12
10
8
6
4
2
0
Fig. 2. Seasonal patterns of life-history features: sex ratio, number of immature and mature eggs in
females, and egg-laying rate of P. canariensis (left column) and P. ascendens (right column). Vertical lines
are the 95% CI of the means.
from April to June and decreased significantly during the summer. In relation to sex
ratio in active individuals, this species showed that the frequency of females was
significantly higher in August and September (Table 2).
Lev. stat
dfl
d£2
Sig.
% Females
2.222
11
30
0.041
3.552
11
923
0.000
26.007
0.000
19.655
0.000
Lev. stat
dfl
df2
Sig.
Welch
Sig.
Brown–Forsythe
Sig.
Average dry weight in females
2
3
4
5
6
7
8
9
10
11
12
5
11
7
8
9
10
11
12
1 2 3
*
*
**
**
** ** **
** ** **
** ** **
**
**
Tamhane’s T2 Lev. stat.
dfl
df2
Sig.
Tamhane’s T2 Lev. stat.
dfl
df2
Sig.
F
** **
Sig.
** **
** **
** ** **
** ** ** **
* ** ** **
4 5 6 7 8 9
Tamhane’s T2 Lev. stat.
dfl
df2
Sig.
F
Sig.
** ** **
* ** **
1 2 3 4 5 6 7 8
*
** ** **
** ** ** **
** ** ** **
1.051 5
5
6
30
7
0.406 8 *
** ** **
**
** **
6 7 8
LSD
LSD
Monthly pairwise comparisons
Post hoc procedures
0.541 5
5
6
77
7 ** *
0.744 8
4.242 9 * *
0.002 4 5
0.598
4
72
0.665
1.748
0.135
Lev. stat
2.043
dfl
6
df2
916
Sig.
0.022
F-Welch
11.562
Sig.
0.000
F-Brown-Forsythe
9.768
Sig.
0.000
Average dry weight in males
Monthly pairwise comparisons
One-way ANOVA
One-way ANOVA
Life history
Post hoc procedures
Pimelia ascendens
Pimelia canariensis
Table 2
One-way ANOVA analysis of the life history features
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371
Average number of mature eggs
1.192
0.397
1.181
0.368
2
3
4
5
6
7
8
9
10
11
12
37.1043 3
10
4
883
5
0.000 6
174.880 7
0.000 9
36.283 10
0.000 11
12
Lev. stat
21.755
dfl
11
df2
941
Sig.
0.000
Welch
159.588
Sig.
0 000
Brown–Forsythe
65.156
Sig.
0 000
Average number of Immature eggs Lev. stat
dfl
df2
Sig.
Welch
Sig.
Brown–Forsythe
Sig.
Welch
Sig.
Brown–Forsythe
Sig.
**
1
**
**
**
**
**
**
*
**
**
**
**
**
**
**
**
**
**
2
**
**
**
**
**
**
**
**
**
3
4 5
** **
** **
** **
** **
** **
*
** **
** **
** ** ** ** **
** ** ** ** **
*
**
**
**
**
1 2 3 4 5
** **
Tamhane’s T2 Lev. stat.
12.804
dfl
5
df2
245
Sig.
0.000
Welch
10.299
*
Sig.
0.000
Brown-Forsythe 16.117
*
Sig.
0.000
** ** **
* ** ** ** **
** ** ** ** **
6 7 8 9 10
5
*
7
**
**
**
6 7
*
6
8
Tamhane’sT2
8
5
Tamhane’s T2
6
7 ** ** **
8
**
9
**
4 5 6 7 8
**
*
**
**
** *
4 5
5.641 9
0.001 4
Tamhane’s T2 Lev. stat.
2.433 5
dfl
5
6
df2
245
7
Sig.
0.036 8
Welch
19.117 9
Sig.
0.000
** ** **
Brown-Forsythe 19.808
** ** **
Sig.
0.000
** ** **
6 7 9
F
Sig.
Monthly pairwise comparisons
Post hoc procedures
372
Monthly pairwise comparisons
One-way ANOVA
Post hoc procedures
Life history
One-way ANOVA
Pimelia ascendens
Pimelia canariensis
Table 2 (continued )
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Lev. stat
dfl
df2
Sig.
Welch
Sig.
Brown–Forsythe
Sig.
10.745 11 *
8
4
103
0.000
7.323
0.000
6.388
0.000
Tamhane’s T2 Lev. stat.
6.683
dfl
5
df2
231
Sig.
0.000
Welch
28.327
Sig.
0.000
Brown-Forsythe 29.490
Sig.
0.000
5
6 *
7 **
8
9 **
4
**
**
**
5
**
**
**
6 7
*
8
Tamhane’s T2
When the variances dependent variable are not equal across groups, the Welch and Brown-Forsythe statistics was used instead of the F-test. Monthly pairwise
comparisons were made wilh LSD or Tamhane’s T2 post hoc procedures in function of the result of homogeneity test. The numerator (dfl) and denominator
(df2) degrees of freedom were used to calculate the significance of Levene test.
Laying rate
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3.2. Seasonal patterns of activity density and minimum temperature at site level
The temporal distribution of the monthly means of activity density differed
between P. canariensis (Fig. 3A) and P. ascendens (Fig. 3B). P. canariensis was active
nearly all the year in the coastal environment, and P. ascendens restricted its activity
to spring and summer in the montane environment.
P. canariensis emerged on the soil surface toward the midsummer (August) when
minimum average soil surface temperature was E21 1C. In winter (January), the
population reached its monthly maximum of the activity density when temperature
decreased. From February to July, when temperature increased, the population
reached its monthly minimum of the activity density.
P. ascendens emerged on the soil surface early in spring (March) when minimum
average soil surface temperature was E2 1C. By August, the population reached its
monthly maximum of the activity density, when temperature increased. From
September to October, when temperature decreased, the population reached its
monthly minimum of the activity density. During the cold, humid months
(November–February), captures in pitfall traps were rare.
3.3. Linear regression analysis
The parameter estimates from linear regression analysis between activity density
and minimum temperature changed across different sampling scales (Tables 3 and 4).
The monthly means at the site level were very different for the two species in the case
of all months combined (global) and in analyses where the activity density increase
period and decrease period were analysed separately (Table 3). In P. canariensis the
R2 was low and not significant for the global analysis, whereas in P. ascendens, this
was highly significant, and b1 regression coefficient was near unity. The values of the
coefficients of determination of the seasonal periods were greater than the global
analysis. During periods of increasing activity density the regression coefficient b1
was negative for P. canariensis and positive for P. ascendens. In the decrease period,
the R2 in P. canariensis was the highest.
The global regression line at the site level about the relationship of the monthly
mean of activity density of P. canariensis (Fig. 4A) had a more shallow slope than
regressions for the activity density increase and decrease periods: frequent high
values of activity density occurred during the decrease period (13–14 1C) and low
values occurred during the increase period (20–21 1C). However, in P. ascendens
(Fig. 4B), the global straight line was parallel to the straight line of the increase
period: low values of activity density occurred during the decrease period and high
values occurred during the increase period.
The parameters of the linear regression for monthly mean of activity density and
minimum temperature at plot level were very different for the two species (Table 4).
Only some of the plots showed significant values of the R2 when the activity density
reached highest values. In general, for both species, in the increase period most plots
showed more consistent regression coefficients than in the decrease period. The
slopes of regression line (b1) for both periods were greater in the plot numbers 9 and
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22
4
20
3
18
2
16
1
14
Activity Density
Temperature
0
Minimum Temperature (°C)
Activity Density
Increase period of activity density
5
12
(A)
Increase period of activity density
14
30
Activity Density
10
20
8
6
15
4
10
2
5
0
-2
0
(B)
Minimum Temperature (°C)
12
25
Jan Mar May July Sept Nov
Feb April June Aug Oct Dec
Fig. 3. Seasonal changes in monthly average of activity density (95% CI) and minimum temperature at
site level: (A) P. canariensis and (B) P. ascendens.
10 (Fig. 4C shows plot number 10) for P. canariensis and in plot number 20 for
P. ascendens (Fig. 4D) the ecological optimum for the two species shifts along the
elevational gradient (P. canariensis 14 1C; P. ascendens 10 1C) and the range of
activity was extended from 13.4 to 20.6 1C in P. canariensis and from 8.5 to 9.6 1C
in P. ascendens.
At weekly time-scale, the relationship between activity density and minimum
temperature was more consistent during the increase period (Table 4). P. canariensis
showed more significant regression coefficients in each plot during the increase
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Table 3
Summary of regression analyses of density activity on minimum temperature at site level considering life
cycle stages (increase, decrease and global activity density periods) and two time scales (monihly and
weekly) for P. canariensis and P. ascendens
Time scale Period
Pimelia canariensis
R2
F
P
Pimelia ascendens
b0
P
4.10 o0.05
8.80 o0.01
5.33 o0.01
b1
R2
n
P
b0
P
12 0.51 10.20 o0.01 0.55 NS
7 0.73 13.53 o0.05 2.52 NS
5 0.67 6.04 NS
0.41 NS
Monthly
Global
0.13 1.48 NS
Increase 0.78 17.60 o0.01
Decrease 0.90 26.52 o0.05
Weekly
Global
0.06 29.62 o0.001 5.27 o0.001 0.18 465 0.00
Increase 0.16 60.74 o0.001 8.69 o0.001 0.34 317 0.00
Decrease 0.17 29.22 o0.001 4.85 o0.001 0.22 148 0.10
0.13
0.35
0.27
F
0.19 NS
0.06 NS
1.34 NS
b1
n
1.00 12
1.09 7
0.30 5
14.81 o0.001 0.19 71
19.55 o0.001 0.13 57
3.34 NS
0.31 14
R2: coefficient of determination; F: ANOVA F-test; P: probability; b0 and b1: regression coefficients and n:
number of cases.
period than in the monthly analysis, especially in the study plots 6 and 10. The
estimated ecological optimum increases 1.5 1C and the range is enlarged 2.9 1C
compared to those estimated for the monthly regression values (cf. Figs. 4C and E).
In P. ascendens (Fig. 4F, plot number 20) the ecological optimum increases 3 1C and
the range is enlarged 3.4 1C compared to those estimated from the monthly
regressions (cf. Figs. 4D and F). In the analysis of P. canariensis site level data,
significant results were always obtained although with lowest values of the R2 and
the regression coefficients (b1), perhaps due to the higher sampling size and
variability (see Table 3). The slope of regression straight lines were also lowest (Figs.
4G and H), because the distribution of density activity points along thermal gradient
seems to define a bell-shaped optimum.
4. Discussion
4.1. Environmental variability and species activity
At fine scales, several ecological factors can affect the local abundance of darkling
beetles (de los Santos et al., 2002b). In each habitat, regardless the local abundance,
we would still predict a positive or negative response of population abundance and
activity with changes in environmental temperature, showing a characteristic pattern
of activity density. However, if the variation in temperature and population
abundance is estimated across broader scales, for example among several plots
within an attitudinal position, then we would expect great variability in the
temperature–abundance relationship because at fine-scale other ecological factors
can affect. To further understand among-site or among-plot variation in activity
density with temperature, it is necessary to know the spatial pattern of the
population (Greig-Smith, 1964; Elliot, 1977; Southwood, 1978; de los Santos et al.,
1982b; Crist and Wiens, 1995; McIntyre, 1997). In the present study, we can only
Increase
1
2
3
4
5
6
7
8
9
10
11
12
Decrease
Weekly
1
2
3
4
5
6
7
8
9
10
11
12
Increase
Monthly
1
2
3
0.52
0.60
0.60
0.89
0.00
0.17
0.27
0.41
0.24
0.93
0.75
0.87
0.93
0.55
0.33
0.61
0.42
0.80
0.46
0.06
0.74
0.90
0.75
0.73
0.65
0.85
0.73
21.81
27.11
34.14
24.10
0.00
0.62
1.86
2.13
1.57
42.79
9.12
20.16
42.55
4.97
2.49
7.81
3.59
19.46
2.60
0.31
8.52
45.49
14.66
13.76
9.49
22.50
8.24
F
b0
7.01
4.31
6.24
4.07
0.75
26.93
13.99
7.74
18.59
19.44
11.38
13.37
5.70
2.06
2.26
0.74
1.03
5.97
10.25
12.11
14.71
14.12
2.54
5.24
6.93
5.01
6.29
P
o0.05
NS
o0.01
NS
NS
NS
o0.01
o0.05
o0.05
o0.05
o0.01
NS
o0.05
NS
NS
NS
NS
NS
o0.01
NS
o0.05
o0.01
NS
NS
o0.001
o0.001
o0.001
o0.001
o0.001
o0.001
o0.01
NS
NS
NS
NS
NS
o0.01
o0.05
o0.05
o0.01
o0.05
NS
o0.05
o0.05
o0.01
NS
NS
o0.05
0.001
o0.01
o0.01
o0.01
o0.01
o0.05
P
0.27
0.16
0.25
0.28
0.01
0.11
0.03
0.05
0.28
0.56
0.71
0.83
0.75
0.11
0.22
0.27
0.14
0.25
0.18
0.01
1.08
0.67
0.33
0.81
0.76
0.50
0.55
b1
22
20
25
5
5
5
7
5
7
5
5
5
5
6
7
1
1
7
5
7
5
7
7
7
7
6
5
n
13
14
15
15
20
13
14
15
18
19
20
21
Plot
0.08
1.00
0.18
0.38
0.81
0.13
1.00
0.85
0.02
0.00
0.83
1.00
NS
NS
0.60
0.64
NS
o0.05
NS
NS
NS
o0.01
5.67
0.02
0.01
23.93
0.61
12.70
NS
p
0.45
F
R2
Plot
R
Pimelia ascendens
2
Period
Time scale
Pimelia canariensis
1.35
0.95
0.57
0.07
5.29
0.58
1.01
0.34
1.30
1.80
28.53
7.83
b0
0.03
0.13
0.04
0.01
1.06
0.02
0.12
0.11
0.08
0.01
3.61
1.33
b1
9
2
5
3
5
5
2
3
3
5
7
2
n
A. De Los Santos et al. / Journal of Arid Environments 65 (2006) 363–385
NS
o0.05
NS
o0.05
NS
NS
o0.05
o0.01
NS
P
Table 4
Summary of regression analyses of density activity on minimum temperature at the plot level considering life cycle stages (increase and decrease activity density
periods) at two time scales (monthly and weekly) for P. canariensis and P. ascendens
ARTICLE IN PRESS
377
Decrease
Period
n
1
2
3
4
5
6
7
8
9
10
11
12
0.55
0.05
0.09
0.09
0.23
0.45
0.68
0.45
0.54
0.64
0.26
0.35
19.31
0.94
1.12
1.51
5.24
14.67
33.26
13.06
17.76
28.35
7.21
11.29
30.05
0.50
38.99
52.42
38.96
53.01
60.82
109.29
46.48
6.63
0.18
26.37
13.99
8.36
17.96
21.41
13.43
16.94
4.14
2.92
1.50
0.00
0.92
6.11
7.53
7.23
9.00
11.32
2.49
6.18
o0.001
NS
o0.001
o0.001
o0.001
o0.001
o0.001
o0.001
o0.001
o0.001
NS
NS
NS
o0.05
o0.01
o0.001
o0.01
o0.01
o0.001
o0.05
o0.01
o0.001
o0.05
NS
NS
o0.01
o0.001
o0.001
o0.001
o0.001
o0.001
o0.001
o0.001
o0.001
NS
o0.001
o0.001
o0.001
o0.001
o0.001
o0.001
o0.001
0.16
0.08
0.06
0.03
0.03
0.30
0.37
0.35
0.44
0.55
0.10
0.27
0.31
0.02
1.05
0.66
0.35
0.75
0.83
0.59
0.72
18
20
14
17
20
20
18
18
17
18
22
23
16
17
20
21
21
22
22
17
17
20
16
17
18
19
20
21
Plot
0.82
1.00
1.00
0.08
0.00
0.65
1.00
37.46
0.16
0.00
40.96
F
0.68
0.03
0.68
0.73
0.67
0.73
0.75
0.88
0.76
b1
4
5
6
7
8
9
10
11
12
P
R2
b0
P
R2
Plot
F
Pimelia ascendens
Pimelia canariensis
o0.001
NS
NS
o0.001
p
5.74
0.33
0.71
0.73
1.65
31.58
6.26
b0
o0.01
NS
o0.05
o0.001
P
1.25
0.05
0.03
0.14
0.00
2.93
1.19
b1
10
2
2
4
6
24
2
n
378
R2: coefficient of determination; F: ANOVA F-test; P: probability; b0 and b1 : regression coefficients and n: number of cases.
Time scale
Table 4 (continued )
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A. De Los Santos et al. / Journal of Arid Environments 65 (2006) 363–385
Pimelia canariensis
Activity density
14
10
Activity density
Period:
increase
decrease
global
60
8
6
1
4
2
2
14
3
30
12 11
4
5
6
7
7
5 6
4
12 3 11 10 9
12
10 9 8
0
90
(C)
8
(D)
12
8
10
1
8
60
11
12
6
2
4
2
14
7
56
8
30
10
3
4
7
4
9
9
5 6
0
0
Activity density
(B)
12
0
90
(E)
2 112 113 10
(F)
12
10
60
8
6
30
4
2
0
0
14
Activity density
Pimelia ascendens
90
(A)
379
90
(G)
(H)
12
10
60
8
6
30
4
2
0
10 12
14 16
18 20
22 24
Minimum Temperature (°C)
0
-10
-5
0
5
10
15
20
Minimum Temperature (°C)
Fig. 4. Regression analyses of density activity on minimum temperature of Pimelia canariensis (left) and
Pimelia ascendens (right). (A, B) Mean monthly values at site level. (C, D) Mean monthly values of the plot
numbers 10 and 20. (E, F) Values at the weekly time-scale for plot numbers 6 and 20. (G, H) Weekly
values at the site level. Numbers for points data in (A)—(D) indicate sample month (1 ¼ Jan to 12 ¼ Dec).
conclude that the effect of the spatial variation was larger in P. ascendens (due to
wide elevation distribution) than in P. canariensis which occurred only at lower
elevation.
4.2. Relationship between minimum temperature and activity density
In darkling beetles, little attention is given to the life-history patterns and,
although different life cycle patterns have been identified (Knor, 1975), they are valid
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only for those geographical areas with warm and cold seasons rather than wet and
dry ones (Allsopp, 1980a).
In Tenerife, the two species of the genus Pimelia had different life-history
characteristics. P. ascendens presented a 2-year life cycle with larvae and adults
overwintering. The activity period of adults lasted from March to October, with
emergence occurring from the end of July to the beginning of August. P. canariensis
had a 1-year life cycle, without larval or adult overwintering. Note that the 1-year
cycle model of P. canariensis has not been described by Knor0 s (1975) classification.
P. canariensis adults were active throughout the year, although a preference exists
for the wet season, and adults emerged over a relatively long period of time
(May–October).
Consequently, in the analysis of relationship between activity density of darkling
beetles and minimum temperature, outlier points with high levels of activity density
can be related to the massive emergence of individuals, both from overwintering and
eclosion, and possibly with a change of movement behavior (vagility). The adult
emergence process could be gradual with respect to adult aging of the old generation.
Hence, depending on the mortality of individuals of the old generation, the
combined densities of both generations may vary more widely until the individuals of
the old generation die and the population size is comprised almost entirely of the
younger adult cohort. If there is a massive emergence of new adults in a study area at
the same time that older adults are present, then there is a disproportionate increase
of population size. Hence, if the increase period of the population defined a
significant linear regression between activity density and minimum temperature, then
this would show a high value of activity density that would not be possible to predict
for a certain value of the environmental temperature.
4.3. Trade-offs in the temperature responses and life cycle patterns
Knor (1975) concluded that the fundamental characteristics of darkling beetle life
history show generic constancy and are practically the same in conspecific
populations inhabiting climatically different regions of the distribution range. The
differences are associated only with differences in phenology. Our study shows
that these two congeners have very different life histories that likely evolved in response to conservatism of thermal optima across a highly variable temperature
environment.
Studies on temperature preferences of darkling beetles have shown that several
species are eurythermic, displaying considerable overlap in preferred temperatures
(Rickard, 1971; Kramm and Kramm, 1972; Slobodchikoff and Pedersen, 1975;
Zachariassen, 1977; Parmenter et al., 1989). Optimal temperature preferences for
several darkling beetles are in the range 15–20 1C. Slobodchikoff and Pedersen (1975)
investigated the temperature preference in adults of two congeneric species of
darkling beetles. Both showed a mean preference for 26 1C, but the distributions of
their responses to temperature were quite different.
The temperature optimum in Canarian darkling beetles appears to be lower than
the optima registered in other studies, perhaps because researchers use different
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A. De Los Santos et al. / Journal of Arid Environments 65 (2006) 363–385
381
methods to measure the thermal environment of the species. However, our values
may also be lower because we defined the optimum as the maximum value of activity
density and not the means as other authors have considered (Parmenter et al., 1989).
Finally, we also used minimum temperature in microclimatic conditions because it
consistently provided the best predictor of activity density. Linear regression analysis
showed a close correspondence between the monthly minimum temperature
obtained from our field thermohygrometer readings and those meteorological
observatories of Izaña and La Planta. The results showed a difference of 4.2 1C
(y ¼ 0.93x+4.24; R2 ¼ 0:94, po0:01) between the micro and meso-climatic data in
the summits of the island (Izaña), while in the lowest zones of the island (La Planta)
the difference was only of 1.8 1C (y ¼ 1.53x+1.8; R2 ¼ 0:79, po0:01). However, the
values of standardized coefficient b1 in La Planta were highest than in Izaña because
the heat is accumulated below the stones during the warm seasons. All this would
explain the differences between the thermal preferences found in this study compared
to the range of values reported by other authors.
Because the two species live in different ecological systems they need to
synchronize their life histories with climatic fluctuations of different intensity. These
conditions give rise to diachrony in life cycles although they maintain the tendency of
the two species to have the same thermal optimum. Thus, although the two species
differ in many life-history parameters, their preferred temperature is similar. This
suggests that the hypothesis of the conservative evolution in ecological niches
(Peterson et al., 1999) may apply to these two species: different selective pressures
have probably led to the development of different life cycles (behavior, diapause, egg
maturation, etc.) in these two related species, in order to synchronise their life cycles
with environmental fluctuation at low and high altitudes. The environmental
constraints leading to inactive periods in the two sites would be desiccation stress at
low altitudes and suboptimal temperatures at high altitudes.
Taken together, our findings and the phylogenetic history of Pimelia suggest
that speciation takes places in geographic instead of ecological dimensions and
that ecological differences evolve later (Peterson et al., 1999). We also suggest
that the speciation may be directly related with the divergence in life-history
strategy of the two species while conserving similar preferred environmental
temperatures.
If we assume that the beetles follow a maxithermic strategy as rule, we would
predict a positive relationship between activity and temperature. The positive
relationship between activity density with temperature for P. ascendens is consistent
with this hypothesis. But, why does not P. canariensis showed the same relationship
with temperature? Temperature and moisture can have a major influence on behavior and on microhabitat selection by darkling beetles (Seely, 1979; Slobodchikoff,
1983). The reactions of desert beetles to heat are largely behavioral whilst their
responses to water shortage are primarily physiological (Cloudsley-Thompson,
2001). Likewise, circadian and seasonal rhythms of darkling beetles are assumed to
be related to availability of water when thermal tolerances are otherwise appropriate
(Hamilton, 1971; Holm and Edney, 1973; de los Santos et al., 1988; Parmenter et al.,
1989). Seasonal-activity patterns or microhabitat selection has been primarily
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attributed to species-specific differences in water conservation abilities (CloudsleyThompson, 1964; Smith and Whitford, 1976; Marino, 1986). This would explain that
P. canariensis was active during the winter (humid period), since the temperature
remained around its inferior limit of tolerance (12–14 1C). Accordingly, we would
predict that P. canariensis would have more efficient water conservation abilities
than P. ascendens, which presumably has been subjected to less desiccation stress.
The high darkling beetle abundance at different times of year and their overlap in
habitat use suggests that these two species provide functional redundancy in their
roles as detritivores in the Canarian ecosystems (Thomas, 1979; de los Santos et al.,
2002a). Nevertheless, the fact that peak seasonal abundance and distribution along
elevational gradient differs between the two species suggests that each have
important functional roles in these semi-arid ecosystems.
Acknowledgments
We wish to thank Ministerio de Medio Ambiente for giving us permission to
conduct the research on the Parque Nacional del Teide and the Reserva Natural del
Malpaı́s de Güimar. Eustaquio Hernández provided assistance in the field. The
research was supported in part by a grant through the University of La Laguna. Two
anonymous referees also provided several valuable suggestions on the paper, one
referee suggested the use of some statistics to show the differences between months in
the life-history features.
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