losos_ch08.qxd 4/14/09 2:11 PM Page 156 FIGURE 8.11 Anole exclusion from trees in the Luquillo Mountains, Puerto Rico. By climbing trees and capturing lizards, Dial and Roughgarden (1995) were able to remove lizards from trees isolated by Hurricane Hugo to monitor the effect to lizards on the ecosystem. Plastic collars on the trunks prevented lizard recolonization. Photo © Roman Dial. (e.g., Wolcott, 1923; Reagan, 1996). In some cases, these seeds may have been ingested incidentally, but in other instances, seeds, which are digested more slowly than pulp, may be the last remaining trace of a fruity meal in the digestive tract of an anole.205 Nectarivory has been reported in a number of West Indian trunk-crown anoles (Liner, 1996; Perry and Lazell, 1997; Campbell and Bleazy, 2000; Echternacht and Gerber, 2000; Okochi et al., 2006; Valido, 2006), a grass-bush anole (Perry and Lazell, 2006), and two Lesser Antillean species (Timmermann et al., 2008). The greater occurrence of frugivory and nectarivory among island species compared to those on the mainland agrees with a trend seen for lizards in general (Olesen and Valido, 2003). Andrews (1979), in a review of anole diet studies, argues that West Indian species generally eat small prey, whereas mainland species take much larger prey. Moreover, mainland anoles generally have more food in their stomach than do West Indian lizards, indicative of a higher rate of food intake. Work by Vitt and colleagues (e.g., Vitt and Zani, 1996a, 1998a,b 2005; Vitt et al., 2001, 2002, 2003a,b) indicates that extensive variation exists among mainland species in prey size and in the extent to which lizards have full stomachs; unfortunately, quantitative comparisons among published studies by various researchers are not possible. 205. Indeed, intact seeds some times make their way out the other end. When anoles are captured alive, they often defecate in the container into which they are placed, and seeds are not infrequently found in the poop. 156 • ANOLE LIFE HISTORY AND POPULATION BIOLOGY losos_ch08.qxd 4/11/09 9:06 AM Page 157 (a) (b) 150 4.0 3.5 125 3.0 100 2.5 75 2.0 FIGURE 8.12 1.5 50 Food web effects of anoles. The 1.0 numbers of spiders and damage Leaf damage (percent) Number of web spiders 25 0.5 to leaves both increase when A. sagrei is removed from experi- 0 0 mental enclosures. Based on data Control enclosures with lizards from Spiller and Schoener (1996) Lizard-removal enclosures kindly provided by David Spiller. PLACE IN THE ECOSYSTEM Anoles thus eat and are eaten (as well as parasitized) by many other species. Conse- quently, given their great abundance in the West Indies, anoles probably play an impor- tant role in the functioning of ecosystems, both as major predators on insects and as food for predators on higher trophic levels. A number of experimental studies have con- firmed this expectation. These experiments have been impressive in scope and some- times adventurous in execution. In the Bahamas, A. sagrei has been introduced to small islands lacking them (Schoener and Spiller, 1999), using other lizard-less islands as controls. In Puerto Rico, Dial and Roughgarden (1995) took advantage of the aftermath of Hurricane Hugo, which fragmented the canopy into discrete tree crowns isolated from each other. Dial climbed 14 trees, removing most or all anoles from seven of them, a Herculean task given that the trees were 20–30 m tall. By placing polypropylene plastic collars around the trunks of the trees to prevent re-colonization, they were able to use each tree as an experimental unit (Fig. 8.11). Finally, on St. Eustatius, Pacala and Roughgarden (1984) created six 12 ϫ 12 m fenced enclosures in the middle of the rainforest. Isolating these enclosures from the outside involved removing all overhang- ing vegetation so that lizards could not walk in and out of the enclosures through the canopy. Once the enclosures were completed, all lizards were removed from all of them, and then subsequently reintroduced into three of the enclosures to initiate the experiment. Similar experiments in approximately 9 ϫ 9 m enclosures were conducted in the Bahamas by Spiller and Schoener (1988, 1990). The results of these experiments have been very similar. The abundance of web spi- ders is generally much higher in the absence of anoles compared to in their presence (Fig. 8.12). Arthropod density is also often affected, although effects are not entirely consistent among studies and vary by type of arthropod: many types increase in the absence of anoles, presumably a result of release from predation, but others decrease in ANOLE LIFE HISTORY AND POPULATION BIOLOGY • 157 losos_ch08.qxd 4/11/09 9:06 AM Page 158 abundance, presumably due to predation from the more abundant spiders, an example of an indirect effect. Another indirect effect is an increase in plant damage in the absence of anoles, which results from an increased abundance of herbivorous insects (this effect was not observed in the St. Eustatius study [Pacala and Roughgarden, 1984]). These three-level trophic cascades were taken a step further in the experiments involving the introduction of the predatory curly-tailed lizard discussed earlier in the chapter (Schoener et al., 2002). The presence of the predatory lizard reversed the effect of A. sagrei on spider density and diversity, but didn’t alter any of the other effects of A. sagrei, perhaps because the larger predatory lizard also eats ground arthropods (Schoener et al., 2002). The presence of anoles on Bahamian islands also decreases spider species richness, both experimentally (Spiller and Schoener, 1988, 1998; Schoener and Spiller, 1996) and among natural populations (Toft and Schoener, 1983). Given their abundance, one might expect that anoles in the West Indies play an important role in determining the flow of energy and nutrient cycling; indeed, Reagan (1996) estimated that the three most common anoles in the Luquillo Mountains consume approximately 450,000 insects per hectare per day. However, despite the increase in ecosystem level analysis in the last 10–15 years, few studies have focused on the West Indies, and thus the role of anoles in ecosystem functioning has been little studied. The most comprehensive food web for a West Indian locality was established for St. Martin; in that web, the two anole species link to a very large number of other species, either as predators or prey (Goldwasser and Roughgarden, 1993); a food web for anoles in the Luquillo Mountains in Puerto Rico shows a similarly large number of connections (Reagan et al., 1996). In the post-hurricane study in Puerto Rico, densities of A. evermanni and A. stratulus were strongly positively related to insect abundance, which varied among trees. Aerial insect abundance was greater in tree gaps than within the canopy: as a result, trees downwind from forest gaps supported more lizards because they had the greatest arthro- pod abundance, apparently as a result of insects being blown into the canopy from the tree gaps (Dial and Roughgarden, 2004). Arthropod groups that were commonly caught in sticky traps suspended across tree gaps at 12–15 m height, and thus were likely being blown into the canopy from the ground, exhibited similar abundance changes through time in trees with and without lizards. Dial and Roughgarden (2004) suggested from this observation that although anoles may reduce the abundance of these insects in the canopy, the underlying population dynamics of the insects are determined by what hap- pens in the tree gaps where they are born. In contrast, for those arthropod groups which spend their entire life cycle in the canopy and thus are rarely caught in tree gaps, popu- lation abundances fluctuated out of synchrony between trees with and without lizards. Dial and Roughgarden (2004) suggested that the presence of anoles fundamentally changes the population dynamics of these insects. 158 • ANOLE LIFE HISTORY AND POPULATION BIOLOGY losos_ch08.qxd 4/11/09 9:06 AM Page 159 Similar studies have not been conducted on mainland anoles. However, the lower density of mainland anoles may indicate that their ecosystems effects are generally much less than those of West Indian lizards (Rand and Humphreys, 1968). MAINLAND—ISLAND COMPARISON Andrews (1979), synthesizing many of the types of data reviewed in this chapter, argued that the life history and population biology of mainland and West Indian anoles are fun- damentally different. She argued that West Indian anole populations are generally food limited, whereas mainland anole populations are generally limited by predation. In sup- port of this argument, she made the following points: . Mainland anole survivorship is lower . Mainland anole densities are lower . Mainland anole food intake is greater . Mainland anole average prey size is larger, presumably reflecting the ability of mainland anoles to be more selective in what they eat . Mainland anole growth rate is higher . Mainland anoles spend less time foraging, which Andrews attributed both to higher average prey size and greater risk of predation of mainland anoles From these points, Andrews (1979) concluded that, as a generality, West Indian anole life history evolution has been shaped by intraspecific competition, whereas mainland anole evolution has been determined primarily by predation. As the literature summarized in this chapter indicates, most work in the last three decades has continued to support the dichotomies Andrews recognized. However, it is notable that work on anole population biology has diminished in the last 10–15 years; little work of this sort is currently being conducted, so to some extent Andrews’ hypoth- esis may not have been falsified partly because few relevant data have been collected in recent years.