acta ethol (2002) 4:91–95 DOI 10.1007/s102110100049
O R I G I N A L A RT I C L E
Emilio Civantos
Testosterone supplementation in juvenile Psammodromus algirus lizards: consequences for aggressiveness and body growth
Received: 2 November 2000 / Received in revised form: 15 June 2001 / Accepted: 17 June 2001 / Published online: 27 July 2001 © Springer-Verlag and ISPA 2001
Abstract In some species, more aggressive individuals are more successful in resource competition. High testosterone level is associated with increased activity and aggressive behavior, and this may have a direct effect on metabolic rate and cause an increase in energy expenditure. Here, I examined the influence of exogenously administered testosterone on aggressiveness and body growth in juvenile Psammodromus algirus male lizards. Juvenile males were given testosterone-filled (experimental) or empty (control) implants. Testosterone produced an increase in aggressiveness and activity in the experimental males. However, despite being more aggressive, experimental males did not acquire larger home ranges than control males. Experimental males also experienced a significant reduction in growth rate over the 2-month period following implantation. Experimental males also were in poorer condition at the completion of the experiment, compared to control males. These results suggest that although an elevated testosterone level may have positive effects on aggressiveness and activity, it also may have negative effects manifested as reduced growth rate and body condition. Keywords Testosterone · Aggressiveness · Body growth · Juvenile · Psammodromus algirus
Introduction One of the most common assumptions about territorial animals is that individuals acquire space by winning contests (Maynard Smith and Parker 1976; Krebs 1982; Maynard Smith 1982; review in Stamps 1994; Stamps and Krishnan 1994). That is, individuals are assumed to Communicated by T. Czeschlik E. Civantos (✉) School of Biosciences and Process Technology, Section of Biology, Vaxjo University, 35195 Vaxjo, Sweden e-mail:
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gain possession of areas where they win fights or chases, whereas animals that lose agonistic interactions leave areas in which they were defeated. Thus, the more dominant individual secures the territory, often excluding subordinates from optimal habitats (Krebs 1971; King 1973). This assumption forms the basis for concluding that the degree of individual aggressiveness or relative dominance may determine the size or quality of a territory that an individual can secure. In some species, more aggressive individuals are more successful in resource competition. A previous study on juvenile Psammodromus algirus lizards showed that more aggressive individuals had larger home ranges than did less aggressive individuals. Moreover, home range size and quality influenced probability of survival: survivors had larger home ranges with a greater degree of vegetative cover, compared to nonsurvivors (Civantos 2000). However, benefits resulting from an increase in aggression may be balanced by long-term costs such as increased risk of injury, increased exposure to predators, or increased energy expenditure, which may result in lower lifetime fitness of more aggressive males (Marler and Moore 1988, 1989, 1991). One way to test the trade-off between these potential costs and benefits is by using hormones. The importance of testosterone as a primary modulator of aggression has been documented in many animals (Wingfield 1985; Wingfield et al. 1987), including lizards (Fox 1983; Moore 1988; Salvador et al. 1996, 1997). For instance, Marler and Moore (1988) showed that testosteroneimplanted males were more aggressive than controls, suggesting a greater degree of success in male–male competition. In several species, more aggressive males with artificially increased testosterone levels are more successful in reproductive competition (Wittenberger 1981). For example, side-blotched lizards (Uta stansburiana) increased the size of their territories, obtained higher quality home ranges, and increased their status in a dominance hierarchy (Fox 1983). However, increased testosterone levels also may detrimentally affect growth rate. This may be of particular
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importance to juvenile individuals that need to reach quickly a size that allow them to compete for resources with other individuals. Abell (1998) showed that testosterone-treated females experienced a significant reduction in growth rate in body mass and body length over a 6-month period following implantation. Testosterone also inhibited growth in the garter snake Thamnophis sirtalis parietalis (Crews et al. 1985). High testosterone level is associated with increased activity and aggression or territorial behavior in lizards (DeNardo and Sinervo 1994; Marler and Moore 1989; Salvador et al. 1996). This has a direct effect on metabolic rate (oxygen consumption) and causes an increased energy expenditure (Marler et al. 1995). In the present work, I investigate the effect of testosterone treatment on aggressiveness, activity, home range size, and growth rate in juvenile male P. algirus lizards. I hypothesize that the benefits that are associated with an increase in aggressiveness may be balanced by costs manifested as reduced body growth.
Methods Psammodromus algirus is a medium-sized terrestrial, diurnal, oviparous lizard inhabiting the Iberian Peninsula, southern France, and northwestern Africa (Böhme 1981). P. algirus enter hibernation in late October and emerge in early March. During the mating period, beginning shortly after emergence, males defend territories and fight with other males for access to females (Salvador et al. 1995). Also juvenile individuals of this species actively defend their territory against intruding conspecific juveniles (Civantos 2000). Females produce one clutch per season and carry the eggs for approximately 6–8 weeks before ovipositing in July. The eggs hatch between late August and early October, with variation among years depending on weather conditions. Snout–vent length (SVL) of hatchlings is 24–29 mm. Individuals become sexually mature in their second spring when SVL is 65–70 mm (Civantos and Forsman 2000). The study was conducted in a deciduous oak forest near Navacerrada (40°44′N, 4°00′W), central Spain, during April–June 1999. Vegetation included small deciduous trees and well-developed low sapling scrub oaks (Quercus pyrenaica) and less abundant and dispersed perennial evergreen bushes (Cistus laurifolius). Some isolated patches of large rocks are present in the forest. In February 1999, I delimited a 0.5-ha plot that was divided into a grid with markers every 10 m. I visited the plot 5 days a week between 4 and 20 April 1999 and searched for juvenile male lizards (born the previous autumn) by walking over the plot between 0930 and 1330 hours and between 1600 and 1700 hours. The sex of individuals was determined from the number of femoral pores, number of ventral scales, and number of spots on the right side (Civantos et al. 1999). Individuals were captured by hand and marked by toe clipping for permanent identification. The position where individuals were first sighted was recorded. All individuals were carried to “El Ventorrillo” field station where they were weighed to the nearest 0.01 g with an electronic balance and measured for SVL to the nearest 0.5 mm with a ruler. Only juvenile males with a SVL above 35 mm were selected for the experiment. The individuals used in the experiment hatched during fall 1998 and mature in their second spring at an SVL of about 65 mm. Each captured male was arbitrarily assigned to either the experimental (n=10) or the control group (n=7). Both control and experimental males received a subcutaneous implant of a 4-mm-long Silastic tube (Down Corning; 1.95 mm o.d., 1.47 mm i.d.). Both ends of the tube were plugged with a wooden cap and sealed with Silastic adhesive. Males were cold anesthetized and implanted through a
small lateral-dorsal incision that was closed with a suture. Experimental males received an implant that contained 1 mm of packed crystalline testosterone-propionate (Sigma Chemicals). Hormone dose and the implant size were adjusted to the size and weight of the animals following the previously published works on this and other lizards (Marler and Moore 1991; Hews et al. 1994; Hews and Moore 1995; Salvador et al. 1996, 1997; Abell 1998). Control males received an empty implant. Although I did not measure the testosterone levels in the blood, I did not observe any toxic effects of the hormone on the individuals (no abnormal behaviors or immediate death). After hormone manipulation, individuals were painted with two or three color spots on the back for individual identification in the field and released during the same day at the point of capture. One week after males were given an implant, I conducted observations of the individuals in the field. All of the observations were made in two consecutive weeks. Focal observations of marked lizards were made during periods of 15 min with binoculars from a distance of 3–4 m. Observations were made on sunny days between 1000 and 1330 hours and between 1600 and 1700 hours. Activity patterns (movement, no movement) were recorded every 30 s (one zero-sampled, Altmann 1974) and are presented in the Results section as proportion of focal observation points during which the male was moving. I tallied movement when a lizard moved for more than 2 s and walked more than 3 cm. The experimental treatment of each male was unknown to the observer during field observations. To estimate home range, I performed several censuses per day over the study plot and mapped the position of each individual sighted with respect to the grid markers. I attempted to randomize the time of day and direction of these censuses. Home range for each lizard was defined by the convex polygon surrounding all observation points (Rose 1982). To minimize dependency between repeated observations of single individuals, I recorded the location of each individual only once each day. I estimated that eight points per individual were enough to encompass the home range (Rose 1982). The number of points per individual ranged between 8 and 12. Thus, home ranges were obtained by consecutive resightings of individuals, and not points of defense. I therefore refer to these areas as home ranges, rather than territories. To estimate the degree of intraspecific aggressiveness, I used tethered intruders presented to marked individuals following Stamps (1977, 1978; see also Civantos 2000). The intruder individual was tethered around the abdomen with a dark 2-m nylon thread (0.1 mm thick) attached to a stick, positioned 20 cm from a resident, and the stick was fixed to restrict intruder movement. The experimenter moved back 3 m and observed the focal individual for 5 min through binoculars, recording its first response. I used individuals of the same age class captured at least 200 m away from the study plot as intruders. I introduced an intruder matched in size to the marked individual (
