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Marine Ecology.

ISSN 0173-9565

ORIGINAL ARTICLE

Environmental niche of the smut lizard population


on a sandy coastal ecosystem of Southeastern
Tenerife (Canary Islands)
Antonio de los Santos & Juan Pedro de Nicolás
Department of Parasitology, Ecology and Genetics, University of La Laguna, La Laguna, Tenerife, Canary Islands, Spain

Keywords Abstract
Disturbances; lizard population size; sandy
beach; seasonal and interyearly variability; Relationships among environmental patterns and population size of the smut
thermal and adaphic environment. lizard Gallotia galloti galloti Oudart, 1839 (Sauria Lacertidae) were examined in
the context of longer time-scale variability on a sandy beach and adjacent envi-
Correspondence ronments of Southeastern Tenerife. Seasonal and yearly patterns in the popula-
Antonio de los Santos, Department of
tion size were likewise analyzed in relation to climatic and anthropic variables.
Parasitology, Ecology and Genetics, University
of La Laguna, C ⁄ Astrofı́sico Fco. Sanchez,
Six sampling plots (coastal, sweet tabaiba, tuff, lava, sandy lava and crater)
s ⁄ n. 38206 La Laguna, Sta. Cruz de Tenerife, were selected following a perpendicular transect to the sandy fringe that
Canary Islands, Spain. extends from the beach toward the volcanic interior. Pitfall trapping was con-
E-mail: asantos@ull.es ducted from 1984 to 2005, and capture–mark–recapture technique and the
Jolly–Seber method were used to estimate population sizes. The highest popu-
Conflict of interest lation size estimates were shown on the sandy lava plot and the neighboring
The authors declare no conflict of interests.
lava plot, reaching values of about 3500 individuals ha)1 during the spring.
The population was active almost the whole year, with seasonal patterns of
activity from March to October. Seasonal temperature and population size pat-
terns were correlated but the ‘calima’ episodes produced some disturbance.
Gallotia galloti galloti was one of the most abundant lizards of all the species
studied and its population size has not remained stable over the study period,
probably because of the absence of predation and competition, and because of
human interference and environmental instability.

and as a frugivorous, pollinator and an effective seed


Problem
disperser in volcanic habitats (Barquı́n & Wildpret 1975;
The sandy beach and dunes of the Special Natural Reserve Valido & Nogales 1994; Nogales et al. 1998; Olesen &
of the Malpaı́s of Güı́mar, and their assemblage will be Valido 2003). We explore how isolation in time or space
on high risk levels over the next decades by impacts may affect the population dynamics and the risk of
caused by town planning development schemes in the extinction. Although isolation can be the result of many
surrounding environment. To manage, understand, and ecological processes, its role in affecting the structure and
restore the ecological assemblages, the roles of individual dynamics of populations is not often acknowledged
keystone species have to be understood and considered directly.
(Paine 1969). We have carried out a monitoring of the The study of the population size variability should con-
pattern and the population dynamics of the smut lizard sider several factors that influence the interpretation of the
since 1984 to assess the environment impact of anthropic obtained estimates (Xia & Boonstra 1992). We explored the
activities. This insular species of lizard performs a key- influence of the substrate on the spatial population-size
stone species role as a predator of many of insect species variability by means of environment availability to support

2 Marine Ecology 29 (Suppl. 1) (2008) 2–11 ª 2008 The Authors. Journal compilation ª 2008 Blackwell Publishing Ltd
de los Santos & de Nicolás Environmental niche of the smut lizard population

the incubation of lizard eggs (Bons 1972; Heatwole The climate for the study area is dry temperate (Fer-
1977) or by means of the food availability, especially nandopullé 1976). The dominant vegetation type in the
psammophilous insects, which may play a role in the insec- volcanic laundries is xerophytic scrub, rich in succulents,
tivore juveniles distribution patterns (de los Santos et al. especially cactiform or dendroid spurges (such as Euphor-
2000, 2002b, 2006). We also examined the potential effects bia canariensis L., E. balsamifera Ait., E. obtusifolia Poir.
of seasonal changes in the thermal environment on the and Ceropegia fusca Bolle). On the sandy fringe, it settles
temporal population-size variability in the most visible ec- a pseudo-steppe gramineous formation of thatching-buffel
tothermic vertebrate group, lizards. Similar to that of other grass, characterized by high cover of several hemicryptó-
ectothermic vertebrates (Hutchison & Dupré 1992), nearly fites: Hyparrhenia hirta (L.) Stapf in Oliver, Cenchrus cili-
all aspects of the biology of smut lizards depend on thermal aris L., Aristida adscensionis L. and Tetrapogon villosus
environment (a biophysical aggregate of air temperature, Desf. In their more typical aspect, they are accompanied
wind speed, relative humidity, and radiation) (Tracy & by gorse (Launaea arborescens (Batt.) Murb.), bleats (Plo-
Christian 1986). cama pendula Ait.) and good firewood (Neochamaelea
In this study, we also explored the extent of the density pulverulenta (Vent.) Erdtm.).
compensation hypothesis (DC) on islands (MacArthur
et al. 1972). The islands often show extreme DC (Schoen-
er 1989), possibly caused by a lack of interspecific compe- Material and methods
tition and predation (Schoener & Schoener 1980).
Sampling methods
We predicted a long-term decrease in the lizard’s niche
resources (environmental and bionomics) because of the Six sampling plots were selected following a perpendicular
anthropic interferences, and consequently a decrease in transect to the sandy fringe (Fig. 1). Lizard population on
their abundance. The lizard population size is substan- each plot was sampled periodically using pitfall traps for
tially less variable through time (Schoener 1985) than three annual periods (1984, 1993, 2004–2005). The aver-
most of Connell and Sousa’s populations (Connell & age radius of individual activity in G. galloti galloti is
Sousa 1983). We need to understand the role of habitat ca. 12.5 m (personal observations not published; likewise
and microhabitat use in lizard ecology to be able to assess see Molina-Borja 1985, 1987, 1991). In 1984, a square
the potential impact of such environmental changes and grid of five traps was established on each sampling plot,
to suggest possible conservation measures (Smith & Bal- one in each corner 25 m apart, plus one in the center
linger 2001). Lastly, for a long term, we outline the (2500 m2 spacing). A square grid of 3 · 3 traps (10 m
hypothesis that impeding or slowing down the energy apart, 2025 m2 spacing) was established in the tuff and
flow and matter from the beach will make the Malpaı́s lava plots during 1993, and a rectangular grid of 4 · 5
enter in a degenerative phase with the consequent traps (10 m apart, 3575 m2 spacing) was established in
decrease in the population size of the keystone species the sandy lava plot (1993 and 2004 ⁄ 2005) and the lava
G. galloti galloti. plot (2004 ⁄ 2005). Traps were processed weekly. Pitfall
traps were designed to increase capture efficiency using
tin cans (diameter 20 cm; height 50 cm), with banana
Study area
and tomato bait, and roofs of volcanic flagstone placed
Field work was undertaken in the sandy beach and adja- several centimeters over the top of the tin, to avoid heat-
cent environments of the Special Natural Reserve of the ing. The time of operation of the traps was 4 h, always
Malpaı́s of Güı́mar on the coast of the Southeastern (lee- beginning at 8 am on the summer solstice and at 9 am
ward) Tenerife. This relatively new geological environ- on the winter solstice.
ment was formed about 10,000 years ago (Araña & Captured lizards were marked by amputating some fin-
Carracedo 1978). Lava erupted from Montaña Grande gers at the level of the last joint and released within 2 m
Volcano and flowed downhill from the volcanic cones of each trap. The mutilation of fingers is the most exten-
reaching the ocean where much of it was broken into tiny sively used individual-specific marking technique (Wood-
pieces by the surf. The resulting black sand was deposited bury 1956; Broadley 1974), and allows the
by long-shore currents and wave action into ephemeral characterization of a great number of individuals.
pocket beaches that later on, was transported toward the
interior primarily by winds blowing NE and deposited
Statistical analyses
forming small dunes onto the lava fields (Fig. 1). Nowa-
days, for reasons of urban development the Malpaı́s of Population sizes were estimated using the capture–mark–
Güı́mar is being isolated from these environmental pro- recapture method and considering the category Y (Jolly
cesses that formed it. 1965; Seber 1965). Jolly’s modification of trellis type II

Marine Ecology 29 (Suppl. 1) (2008) 2–11 ª 2008 The Authors. Journal compilation ª 2008 Blackwell Publishing Ltd 3
Environmental niche of the smut lizard population de los Santos & de Nicolás

Fig. 1. Geographical localization of the study


area (Malpaı́s de Güı́mar) and sampling plots
(black circles), in the island of Tenerife
(Canary Islands).

lists recaptures of animals according to their most recent


Results
mark. The notation used follows that of Seber (1982) and
Jolly (1982). Capture–recapture data for males and Table 1 summarizes the population parameters for the
females on each sampling occasion are tabulated in modi- capture–recapture analysis according to Jolly’s model
fied trellis type II and rearrangement data in trellis type II for 1984 sampling year. The population size estimates
for Zi. Hence, the first number of each column is ni, and of G. galloti galloti were significantly different among
the subsequent numbers are recaptures of each sampling the different sampling plots, although these were some-
day. The sum of all entries in columns gives sums of suc- what variable between the serial sampling periods. The
cessive recaptures of animals released on a given day (Ri). maximum estimates recorded for the population size of
By summing the rows from the left, Zi animals are accu- G. galloti galloti consistently occurred on the sandy lava
mulated in the columns and the mi animals are summed plot reaching values of about 3500 individuals ha)1
in the hypotenuse cells. The total number of animals in during the spring. As expected for this species, changes
the population at the time the ith sample is taken (Pi) in the weekly capture success are assumed to be a con-
presents a standard error that is calculated as the square sequence of differences in activity and density, which
root of the variance for population estimates at day i are correlated with the temperature. In general, the
(ESPi). highest population size estimates were associated with

4 Marine Ecology 29 (Suppl. 1) (2008) 2–11 ª 2008 The Authors. Journal compilation ª 2008 Blackwell Publishing Ltd
de los Santos & de Nicolás Environmental niche of the smut lizard population

Table 1. Capture–recapture analysis of


population parameters of Gallotia galloti plot date Ri mi Zi Mi Pi ESPi
galloti on six sampling plots (0.25 ha) for coastal 25 ⁄ 2 ⁄ 1984 2
February–April 1984 according to Jolly’s 3 ⁄ 3 ⁄ 1984 0 0 2
stochastic model. 17 ⁄ 3 ⁄ 1984 0 0 0
24 ⁄ 3 ⁄ 1984 2 2 0 2.00 6.00 0.00
31 ⁄ 3 ⁄ 1984 2 2 0 2.00 3.00 0.00
7 ⁄ 4 ⁄ 1984
sweet tabaiba 25 ⁄ 2 ⁄ 1984 0
3 ⁄ 3 ⁄ 1984 4 0 0 0.00
17 ⁄ 3 ⁄ 1984 7 1 3 4.43 35.43 29.92
24 ⁄ 3 ⁄ 1984 3 6 4 32.67 108.89 71.04
31 ⁄ 3 ⁄ 1984 1 4 3 37.00 101.75 107.01
7 ⁄ 4 ⁄ 1984 4
tuff 17 ⁄ 3 ⁄ 1984 1
24 ⁄ 3 ⁄ 1984 1 0 1 5.00
31 ⁄ 3 ⁄ 1984 1 1 1 17.00 272.00 433.77
7 ⁄ 4 ⁄ 1984 2
lava 25 ⁄ 2 ⁄ 1984 7
17 ⁄ 3 ⁄ 1984 2 1 6 46.00 690.00 835.43
24 ⁄ 3 ⁄ 1984 2 2 6 56.00 504.00 498.83
31 ⁄ 3 ⁄ 1984 2 6 2 21.00 52.50 37.62
7 ⁄ 4 ⁄ 1984 4
sandy lava 25 ⁄ 2 ⁄ 1984 2
17 ⁄ 3 ⁄ 1984 7 1 2 8.71 235.29 260.48
24 ⁄ 3 ⁄ 1984 5 3 6 37.80 365.40 266.60
31 ⁄ 3 ⁄ 1984 1 7 4 159.00 863.14 954.82
7 ⁄ 4 ⁄ 1984 5
crater 25 ⁄ 2 ⁄ 1984 0 3
3 ⁄ 3 ⁄ 1984 1 0 3
17 ⁄ 3 ⁄ 1984 1 1 2 3.00 3.00 0.00
24 ⁄ 3 ⁄ 1984 1 0 2
31 ⁄ 3 ⁄ 1984 1 0 1
7 ⁄ 4 ⁄ 1984

Ri is the total of recaptured animal marked on day i and recaptured subsequently; mi is the
number of marked animals in the ith sample; Zi is the total number of animals captured on a
day previous to i, not captured at day i, and captured again later; Mi is the number of marked
animals in the population at the time the ith sample is taken; Pi is the total number of animals
in the population at the time the ith sample is taken; ESPi, standard error at day i.

the interface sand-lava, which is related with the trans- ranges of temperature. When the temperature was stabi-
port and dispersion of marine sand over the coastal lized inside the ranges or thermal categories, the popula-
volcanic laundries. tion size decreased temporarily.
The population size variation during the 1993 and The emergence of individuals after a short period of
2004–2005 sampling years is shown in Fig. 2, in relation inactivity (brumation) was quite predictable. First, lizards
to maximum and minimum temperatures. The maximum were mostly captured in early February (average soil sur-
estimates recorded for the population size of G. galloti face temperature 15–16 C, range = 13.5–20.5 C; maxi-
galloti consistently occurred during the same season on mum temperature 19–23 C; minimum temperature
each sampling plot. As expected for this warm environ- 11–12 C). Within a few weeks, the population size
ment, there was a long individual activity period from reached high numbers. During March with a weak
February to November. A narrow relationship between increase in the temperatures (average soil surface temper-
the minimum temperature variation and the population ature 19.5 C; range = 13.5–23 C), lizards showed a
size variation was observed, although it is not obtained maximum population size. Later on, a remarkable descent
unless the variables are categorized by year cycle periods. of the population size took place during April. Neverthe-
The categories are more or less coincident with seasonal less, an increment of the average soil surface temperature

Marine Ecology 29 (Suppl. 1) (2008) 2–11 ª 2008 The Authors. Journal compilation ª 2008 Blackwell Publishing Ltd 5
Environmental niche of the smut lizard population de los Santos & de Nicolás

Fig. 2. Population size variation of Gallotia


galloti galloti during the 1993 (a, b, c, f, g, h)
and 2004–2005 (d, e, i, j) sample years, in
relation to the maximum (right column) and
minimum (left column) temperatures, on
sandy lava (a, f, d, i), lava (b, g, e, j) and tuff
(c, h) plots in the Special Natural Reserve of
the Malpaı́s of Güı́mar. Population size (black
dots); temperature (white dots).

during May–June (average soil surface temperature 22 C; ulation sizes were correlated but the calima episodes
range = 18–25 C), allows to register the biggest popula- considerably modified this correlation. The calima phe-
tion size. This peak in the population size corresponds to nomenon happens at any time of the year but is usually
equally high standard error, which indicated that individ- associated with the hot air found over the islands during
ual surface activity were the greatest within this range of the summer months, ranging from a few hours up to a
temperatures. By November (average temperature 19 C; week. In addition, the fine sand particles cause the air to
range = 15.5–23 C), lizards were no longer active at the become thick and visibility becomes rather like that expe-
soil surface. Finally, during the cold, humid months of rienced during a thick fog, depending on the severity.
December and January, captures were rare. Other climatic episodes, such as rainfall, clouds and heat
The microvariations observed in the population size shocks, also modify this correlation.
curve appear to be of a different character from those of Figure 3 shows the temporal distribution during three
the year interval. Seasonal temperature patterns and pop- sample years of population size of G. galloti galloti on a

6 Marine Ecology 29 (Suppl. 1) (2008) 2–11 ª 2008 The Authors. Journal compilation ª 2008 Blackwell Publishing Ltd
de los Santos & de Nicolás Environmental niche of the smut lizard population

Discussion
Space and time axes of the lizard population niche around a
sandy beach

Pitfall trapping is widely used for capturing animals


found on the ground surface. Critical studies (see reviews
in Southwood 1978) on the efficiency of pitfall trapping
concluded that ‘pitfall traps are of little value for the
direct estimation of populations or for the comparison of
assemblages’ largely because, capture success is highly
influenced by changes in the animals at risk on account
of variables such as weather, substrate, behavior, etc.
However, this is still the primary means of assessing den-
sity of ground-dwelling animals (de los Santos et al.
2002a).
The spatial variation in population size of G. galloti
galloti in the Malpaı́s of Güı́mar can be related to the
sand content in the volcanic laundry, superficially or into
the rock fissures. The maximum values of population size
were registered for the sandy beach (sandy lava plot) and
the lava plot. The individuals rest in the cracks of the
rocks, where they are relatively active, while forage over
the sandy areas, looking for fleshy fruits as well as insects
(Valido et al. 2003). Food resources partitioning between
juveniles and adults, insectivores, frugivores, respectively,
provides a more suitable niche for lizard growth and cre-
ates a stable population in this sand–rock ecosystem.
Juveniles prefer the sandy niche and adults the rocky lava
niche, next to sandy fringe. The development of an
assemblage of psammophilous insect species in the sand
fringe (de los Santos et al. 2002b, 2006) contributes to
the increase in lizard population size. This is an example
of interaction (sensu Tracy & Christian 1986) between the
physical and the biotic axes of the animal niche, suggest-
ing that animals also exploit its physical environment.
The vagility of the population seems to be important
Fig. 3. Seasonal changes in monthly average population size per among the most critical factors in the interpretation of
hectare (95% CI) of Gallotia galloti galloti in the Malpaı́s of Güı́mar: the pitfall captures (Briggs 1961). The behavior of the
(a) 1984, (b) 1993 and (c) 2004 ⁄ 5. individuals, particularly in relation to the vagility or
home range movement, would affect the capture success.
Hence, trap density and capture probability can be related
to behavioral studies of animal movement (Skalski &
per ha basis on two sampling plots. The temporal distri- Robson 1992).When animals have low net displacement
bution of the population monthly means differed over during the activity period, the population at risk of trap-
the study period. The estimates of the population sizes ping is confined to the trap area (Crist & Wiens 1995).
among years fluctuated between characteristic intervals These situations occur when individuals are relatively sed-
for spring, summer and autumn. From 1984 to 2005, a entary and occupy territories or a well-defined home
remarkable decrease in the population sizes has been range. When individuals are transient to the trap area
shown: 1500–2000 individuals ha)1 (1984), 700 individu- and populations have an open spatial structure, other trap
als ha)1 (1993) and 250–500 individuals ha)1 (2004– arrangements may be more efficient (Mandelbrot 1983)
2005). The above observations were most likely related to because the transect has low probability of recapture and
the habitat use and distribution patterns of lizard around therefore does not permit the use of mark recapture esti-
the sandy beach. mators. However, in cases of high population densities

Marine Ecology 29 (Suppl. 1) (2008) 2–11 ª 2008 The Authors. Journal compilation ª 2008 Blackwell Publishing Ltd 7
Environmental niche of the smut lizard population de los Santos & de Nicolás

such as our study, a large study area could increase the


Comparison with other lizard populations from several
absolute number of marked individuals available for
geographical areas
recaptures, when a high number of captured animals are
marked and released after the ith sample. This is equiva- We compared our estimates of population size for
lent to an increase in the sampling intensity (Blower et al. G. galloti galloti with those of lizards in other mainland
1981). and island environments. After standardizing the esti-
Seasonal variation in thermoregulatory behavior, body- mates of population sizes with respect to hectare area, we
air temperature and population size patterns remain to be observed appreciable differences among populations at
described for the lizard fauna of any region. In some the same and different sites. Although a single lizard spe-
studies (Heatwole 1970; Case 1976; Huey & Pianka 1977; cies exists in the study area, we should consider the com-
Huey et al. 2003), seasonal models of body temperature, petition with other co-occurring insectivorous predators,
time of activity, basking incidence, microhabitat utiliza- if we have in mind the density compensation hypothesis
tion, and the adult-juvenile activity cycles have been dis- on islands (MacArthur et al. 1972): the gecko Tarentola
cussed for some lizard species. As in many lizard faunas delalandii Duméril & Bibron 1836 (Sauria, Gekkonidae),
(Huey & Slakin 1976; Huey & Pianka 1977), only juve- the west canary skink Chalcides viridianus Gravenhorst
niles of G. galloti galloti are active during the winter 1851 (Sauria, Scincidae) and the Etruscan pygmy shrew
months. The activity of juvenile lizards during the winter Suncus etruscus Savi 1822 (Mammalia, Insectivora,
is generally thought to reflect surface-to-volume consider- Soricidae).
ations (Cowles 1941; Fitch 1956) or relatively low fat Although this assemblage of species configures a frame
reserves of juveniles necessitating greater activity in winter of interspecific competition, the comparison of the pres-
(Huey & Pianka 1977). Low ‘optimal’ body temperatures ent study with other studies shows that unispecific popu-
may be correlated with the ability of adults to be active lation density on the island of Tenerife may be higher
year round (Huey & Pianka 1977), suggesting that G. than mainland levels of summed population densities
galloti galloti has high optimal body temperature because (Turner et al. 1970; Andrews 1976; Martı́n et al. 1995;
adults brumate. Shenbrot & Krasnov 1997; Beauchamps et al.1998; Young
Ground-dwelling lizards of Tenerife may have slightly & Young 2000; Rogovin et al. 2000; Kwiatkowski & Sulli-
higher summer mean Tb values than other species because van 2002; Sabo & Power 2002; James 2003; Wiederhecker
they respond to small rises in temperature during the et al. 2003; Germano & Williams 2005). In relation to
winter with short periods of activity. It is also necessary other islands, population densities may be higher than,
to keep in mind the benign character of the climate in similar to or lower than the one found for G. galloti gall-
the coast of Tenerife. Consequently, we should expect oti, depending upon the particular island, habitat, and
large fluctuations in the lizard population sizes, if we con- group of animals studied (Ruibal & Philibosian 1974;
sider that the night minimum temperature does not usu- Schoener & Schoener 1980; Reagan 1992; Stamps et al.
ally fall below 13 C and the thermal environment is 1997, see review; Rodda et al. 2001; Towns et al. 2002,
conditioned by the Trade winds, ‘calima’ and other inter- see review; Mcnair 2003, see review). The high density of
ferences that can introduce changes during short periods G. galloti galloti in Tenerife is only surpassed by the den-
of time. sity of some species in tropical island habitats. A partial
Beginning with Pianka (1966), many authors have explanation for the large difference is that the average live
recognized two basic modes of foraging in lizard, com- weight of this saurian species is approximately 10 times
monly called ‘sit and wait’ (SW) and ‘widely foraging’ less than that of G. galloti galloti, half the size, with a
(WF). Sit-and-wait predators are traditionally considered maximum snout-vent length (SVL) of 145 mm in mature
sedentary, waiting for prey to enter their field of vision males and a maximum weight of 60 g (Martı́n 1985).
and then attacking it. Widely foraging species, on the
other hand, typically spend much of their time moving,
Are lizard population sizes unusually constant
actively searching for prey (Huey & Pianka 1981; Perry &
through time?
Pianka 1997; Perry 1999). The dispersion of the indivi-
duals (in ⁄ output population) and the behavioral changes Strictly speaking, low values of population-size variability
(activity ⁄ inactivity) most notably can increase the esti- through time imply that lizard populations are constant
mates of population size as well as their variability. (Schoener 1985). An approximate model of stable struc-
Hence, we should also look at the insect-juvenile lizard ture of the smut lizard niche would consider that adults
assemblage niche-relationships in search of the co-occur- are sedentary, and once they have established a territory
rence with certain pre-imago stages of the insect life on a specific area, rarely move from that site. Coloniza-
cycles (de los Santos et al. 2006). tion of new areas would be done primarily by juveniles

8 Marine Ecology 29 (Suppl. 1) (2008) 2–11 ª 2008 The Authors. Journal compilation ª 2008 Blackwell Publishing Ltd
de los Santos & de Nicolás Environmental niche of the smut lizard population

and egg and ⁄ or juvenile mortality may regulate the popu- Barquı́n E., Wildpret W. (1975) Diseminación de plantas cana-
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