Algal Food Preferences and Seasonal Foraging Strategy of the Marine Iguana, Amblyrhynchus Cristatus, on Santa Cruz, Galápagos

The abundance of intertidal algae, algal food preferences, and foraging behavior of the marine iguana, Amblyrhynchus cristatus Bell, were studied at two sites on Santa Cruz Island, Galápagos, over a tropical cool and hot season. At both sites iguanas had a consistent, seasonally changing hierarchy of preferred algal species, selected according to their availability. During high low tides, Ulva lobata (Kützing) Harvey, usually avoided, was eaten more often because preferred red algae were submerged and unavailable. At other times, one or other of the 4–5 red algal species, seasonally abundant at the sites, were preferred. Feeding preferences changed from the cool to hot season, as algal biomass and cover declined. Foraging behavior also changed between seasons. Only in the cool season did iguanas delay their arrival when low tide was early in the morning, but they anticipated late afternoon low tides. Foraging efficiency increased with temperature and increasing algal biomass. At the site of high algal abundance, bite rates increased and feeding duration decreased, with increasing ambient temperature. At the site where algae were scarce in the hot season, both bite rates and foraging duration increased with increasing temperature. The proportion of time that iguanas on the feeding ground were engaged in feeding also varied seasonally, and increased during high swell and high low tides, which compensated for less grazing time. The total number of feeding bites per day declined with temperature at the site of high algal abundance, but increased with temperature at the site of algal scarcity. Thus, feeding behavior optimized the intake of preferred species at the highest rate of re-warming within constraints imposed by tide and swell. Large males maximized food intake and feeding efficiency by submerged feeding in rock pools. We present a variable “sawtooth” model to explain differences in foraging duration according to seasonally varying algal abundance and temperature. The Galápagos Islands are a dynamic environment. Periodic El Niño events increase sea temperatures 2–5 oC, and reduce algal abundance in the interand shallow subtidal. The marine iguana, Amblyrhynchus cristatus Bell, unique among reptiles in feeding almost exclusively on marine macroalgae (Darwin, 1845), is variously stressed by El Niño events, when only algae of poor food quality persists (Laurie, 1989), and by expanding anemone barrens that smother grazing habitats (Okey et al., 2003). Hence, it is important to understand the algal diet of iguanas, and the variability in algal abundance. Previous studies have rarely considered the botanical aspects of iguana foraging. Here we briefly summarize earlier studies on iguana diet, provide information on algal abundance and seasonality at two feeding sites on Santa Cruz, Galápagos, and describe the food, feeding preferences, and foraging behavior of the iguana over 8 mo spanning a cool and a hot season. At these sites iguanas have low densities of < 1000 per km of shore, skewed toward older age classes, because of high predation on hatchlings by feral dogs and cats (Laurie, 1983). We undertook this study of the seasonally changing availability of algae and the iguanas’ responses in order to reveal algal preferences and other factors influencing diet. We collected quantitative data BULLETIN OF MARINE SCIENCE, VOL. 77, NO. 1, 2005 52 on the components of iguana foraging behavior under changing environmental conditions to reveal the key constraints to feeding. PHYSICAL SETTING AND NATURAL HISTORY The Galápagos Islands lie on the equator near the northern limit of the subtropical convergence. In the cool “garua” season (June–November) the Humboldt current brings cool waters of 20–22 oC to the central and eastern islands of the archipelago, and in the hot season (December–May) the convergence moves south and increases water temperatures to 24–26 oC, except during El Niño events when temperatures increase by 2–5 oC. (Houvenaghel, 1978; Feldmann, 1986). Nutrient-rich upwellings periodically bathe the coasts of the western, southern, and central islands, and stimulate the growth of macro-algae, which provides food for populations of marine iguanas (Wellington, 1975). In southern Santa Cruz, rocky substrata are dominated in the cool season by Ulva lobata (Kützing) Harvey at mid-tide levels, and by red algae in the genera, Gelidium, Hypnea, Polysiphonia, Pterocladiella, and Grateloupia, at midto low tide, depending on the extent of splash. In the hot season, algae persist only in low abundance at low tide level (Cinelli and Colantoni, 1974; Houvenaghel and Houvenaghel, 1974; Walsh, 1993). Iguanas graze mainly in the intertidal, except for large males, which may graze subtidally. Populations thus depend on the abundance of intertidal algae, which varies according to season (Walsh, 1993), swell and local wave action, the extent of upwelling, and the abundance of competing herbivores. Marine iguanas are morphologically adapted for intertidal foraging in strong swell by having long claws, tough skin, blunt heads, flattened tails, and well-developed salt glands (Dawson et al., 1977; Wikelski and Trillmich, 1994). Most iguanas feed intertidally around low tide to maximize body temperature for digestion and assimilation of algae (White, 1973; Buttemer and Dawson, 1993), and thermoregulate by warming in the sun after foraging bouts. Foraging time is constrained by cold water, the duration and height of the low tide, and the height of the swell, which effectively elevates low tide, cools the iguana, and impedes feeding. ALGAL FOOD OF IGUANAS Past studies, carried out on different islands, and in different seasons and conditions, give no coherent picture of iguana diet. Some (Darwin, 1845; Wellington, 1975; Bartholomew, 1978; Nagy and Shoemaker, 1984; Wikelski et al., 1997) have found that Ulva tends to predominate in the gut of iguanas, whereas others (Carpenter, 1966; Estes et al., 1982; Laurie, 1985; Trillmich and Trillmich, 1986; Cooper and Laurie, 1987; Wikelski et al., 1993) have found numerous species of green, red, and brown algae, and even regurgitates, feces, and sea lion afterbirth (Wikelski and Wrege, 2000) in the gut. Such differences in diet may be due to location (northerly islands have relatively more Ulva), proximity to upwellings, and aspect (exposed, steeply sloping rock faces have relatively more red algae; see Frost and Frost, 1983). MATERIAL AND METHODS Two sites on the south coast of Santa Cruz, with different exposures to swell, were chosen for study. Site 1 was a small, exposed promontory of pahoehoe lava, ca 1 m above high water SHEPHERD AND HAWKES: ALGAL FOOD PREFERENCES AND FORAGING OF GALÁPAGOS MARINE IGUANA 53 mark, jutting 20 m seaward, ca 350 m east of Charles Darwin Research Station (CDRS) in Academy Bay (0o45ʹ S; 90o17ʹ W). In moderate swell, breaking waves and white water surge over the rocks providing good conditions for intertidal algal growth and iguana grazing. About 25 iguanas were monitored in this narrow splash zone of ca 120 m2. Ulva abundance was monitored from 9 October to 31 December 2000 and again from 7 April to 23 May 2001 on a horizontal mid-tidal platform, and red algal abundance on an adjacent vertical face, ca 4 m long by 1 m high facing south and west. Algae on the mid-tidal platform were grazed down by mid-November 2000, and the iguanas began to graze farther out on the promontory. From 12 November 2000 to 24 May 2001 we monitored a second wall in the low intertidal, where iguana grazing was then concentrated. Site 2 was on the exposed south coast, about 250 m east of Tortuga Bay (0o45ʹ S; 90o17ʹ W), where ca 45 iguanas resided and grazed along 75 m of shoreline with ca. 290 m2 of intertidal algae. We monitored iguana feeding and behavior on a small elevated outcrop of pahoehoe lava 3 m high, jutting about 8 m into the sea, and sprayed by breaking waves. Ulva abundance at a mid-tidal level was monitored from 23 September until December 2000 when Ulva disappeared. In the low intertidal, red algal abundance was monitored from 23 September 2000 to 26 May 2001 on vertical faces of the outcrop over 5 m2, representative of the area grazed. At both sites, non-destructive algal monitoring was done in a discrete area of abundant algal growth, favored by grazing iguanas, and where in situ observations of grazing were carried out. At both sites, the observer recorded observations from 1 to 2 m distance of a focal individual, without disturbing it. ALGAL ABUNDANCE Algal cover and biomass were measured at both feeding sites at ca 2-wk intervals until 23/26 May 2001. To estimate cover, a 1 m tape measure was laid haphazardly over the rock surface, and the length of tape lying over each species’ group of erect algae was noted. There were two replicate measures for each mid-tidal location, and 8–10 for each low-tide location. Algal patches, usually dominated by one species, together formed a mosaic pattern on rocky surfaces. Biomass was obtained by removing with a chisel 2–4 replicate 100 cm2 samples of algae within patches on a nearby, similarly grazed vertical surface (i.e., with similar blade length) to avoid destructively sampling the monitoring site. Results are expressed as mean values in grams fresh weight (gfw) for the midand low intertidal, respectively. Mean blade length was measured in the laboratory from biomass samples. Algae were blotted and weighed fresh, and voucher material preserved and mounted on herbarium sheets which were deposited in the CDRS (officially CDS) herbarium. Shallow subtidal algal cover and biomass were visually checked and measured periodically at both sites by snorkeling.