algal food preferences and seasonal foraging strategy of the marine iguana, amblyrhynchus cristatus,...

BULLETIN OF MARINE SCIENCE, 77(1): 51–72, 2005

51Bulletin of Marine Science© 2005 Rosenstiel School of Marine and Atmospheric Science of the University of Miami

ALGAL FOOD PREFERENCES AND SEASONAL FORAGING STRATEGY OF THE MARINE IGUANA, AMBLYRHYNCHUS

CRISTATUS, ON SANTA CRUZ, GALÁPAGOS

Scoresby A. Shepherd and Michael W. Hawkes

ABSTRACTThe 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. For-aging 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 tempera-ture. 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 sub-merged 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 in-crease sea temperatures 2–5 oC, and reduce algal abundance in the inter- and 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, 200552

on the components of iguana foraging behavior under changing environmental con-ditions to reveal the key constraints to feeding.

PHYSICAL SETTING AND NATURAL HISTORYThe Galápagos Islands lie on the equator near the northern limit of the subtropi-

cal 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 upwell-ings 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 mid- to low tide, depend-ing 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 var-ies according to season (Walsh, 1993), swell and local wave action, the extent of up-welling, 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 inter-tidally 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 dura-tion 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 IGUANASPast studies, carried out on different islands, and in different seasons and con-

ditions, 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 (Car-penter, 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 obser-vations 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 ABUNDANCEAlgal 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 sur-faces. 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 mid- and 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.

FORAGING BEHAVIORThe foraging and feeding behavior of iguanas was monitored at 1–2-wk intervals over an 8-

mo period from 1 to 3 hrs before the predicted time of low water, until all iguanas had left the feeding ground. Iguana foraging was monitored for 33 d at Site 1, and for 24 d at Site 2.

Daily foraging duration (FD) was defined as the difference between the mean time of ar-rival of iguanas at the intertidal and the mean time of their departure. As the feeding grounds at each site (a promontory and an outcrop respectively) had narrow points of access and a maximum of 10–15 foraging iguanas, we recorded the time of arrival and departure of every individual to and from the feeding ground. Interruptions to feeding by temporarily returning to resting sites away from the feeding ground were rare, and when they occurred, the period of resting time was deducted from the total foraging time.

Iguanas normally grazed and paused intermittently, with feeding bouts usually lasting for periods of ca. 60 sec. After allowing some minutes for acceptance time, the observer stationed himself unobtrusively near the focal individual and counted the number of feeding bites per 30 sec. period of continuous feeding and the dominant alga grazed on. Because bite rate is size-dependent and slows during the period of foraging as the iguana cools (Wikelski and Trillmich, 1994), data were recorded for three size classes of iguana: 150–200 mm snout-vent


length (SVL), 200–300 mm SVL, and >300 mm SVL throughout the period of foraging. Data on bite rates were recorded for 2–6 individuals in each size class and a daily mean for the three size classes calculated. Where replicate bite rate data were obtained for the same indi-vidual, a mean value was used to avoid pseudoreplication.

Data on algal food eaten (number of feeding bites per algal species) were pooled for all individuals observed during each day’s observations. Visual algal recognition was facilitated by the presence of monospecific patches of the major species (for provisos see below), identi-fiable with experience based on form and color, and confirmed if in doubt by sampling, and later examination. We did not record feeding of the few juvenile iguanas (< 150 mm), which fed at higher levels of the shore, and recorded arrival and departure only of large males when they fed on distant, exposed, or partly submerged rocks (see below). Lengths of iguanas were estimated with a graduated 1 m-ruler fixed at the end of a stick, and placed against the iguana until the observer gained experience and judged length by eye.

Wikelski and Trillmich (1994) distinguished three types of foraging behavior —running, feeding, and resting. We omitted “running” as a component because at our sites iguanas fed on algal patches in the splash zone, and instead of running from surging water, clung to the rock in situ. To determine the proportion of time spent feeding, we estimated the proportion (Pi) of all individuals (usually 5–10) visible to the observer and engaged in feeding at any one time at 3–5 min intervals throughout the foraging period while at least four individuals were on the feeding grounds. The mean of all values of Pi on a given day provided an estimate of the average proportion of the total time on the feeding ground engaged in feeding. The mean number of daily feeding bites (DFB) for the subpopulation observed is given by the equation:

DFB P FD BR= ∗ ∗

where FD is the mean foraging duration, and BR is the mean bite rate for large, medium and small iguanas on a given day.

To test statistically the algal preferences of iguanas we used Ivlev’s (1961) electivity coef-ficient, E, which measures the degree of selection of a particular prey species relative to its abundance in the habitat. The relationship is defined as:

E r p r pi i i i= − +

where ri is the relative abundance of prey item i consumed (as a proportion of the total amount eaten), and pi is the relative availability of the same species in the habitat. The index ranges from –1 to +1; negative values mean that the item is avoided (i.e., it is eaten less often than if taken at random); values around zero indicate random feeding; and positive values indicate active selection. The index has been widely used in marine studies, and is relatively unbiased for large (> 300) sample sizes (Strauss, 1979).

As the amount eaten could not be measured, we used data on the number of feeding bites recorded on each alga as a measure of consumption. The availability of algae varied according to the extent of intertidal habitat exposed, which depended in turn on swell height and on the height of the tide when feeding occurred (see below). We stratified intertidal habitat into two types, Ulva-dominated mid-tidal surfaces, Mu , and the steeper surfaces with red algae in the mid- to low intertidal, Lra , and, by gridding the habitat (see below), estimated the propor-tional availability of each habitat type according to tidal height from the linear relations:

M L M a Tu ra u h+ = = +1 and

where Th is the tidal height, and 0 < Th < 0.8 at the mean time of feeding (average of mean arrival and departure times) on a given day. The constant “a” was estimated to be 0.2 at both sites; i.e., at a zero tide the area of Lra available for grazing was four times that of Mu , declining


linearly to zero when the tidal height was 0.8. Total available algal biomass (AAB) was calcu-lated from algal biomass in each habitat from the same relations.

The overall availability, Ai , of the ith algal species was then estimated from the equation:

A B C M B C Li iu iu u ir ir ra= ∗ ∗ + ∗ ∗

where Biu and Bir are the respective biomasses (g 100 cm−2) of the ith species within algal patch-es in the two habitats, Mu and Lra , and Ciu and Cir are their respective cover values.

The spatial extent of intertidal grazed areas was estimated for each site by gridding the intertidal, assuming regular 3-dimensional shapes of rocks in each grid where necessary, and measuring the dimensions with a 50 m tape. From length-frequency data obtained for the res-ident iguana populations and the length-weight relation given by Bartholomew et al. (1976), we calculated the biomass of iguanas m−2 of intertidal habitat. The estimate is approximate because iguana condition varies with environmental conditions (Wikelski et al., 1997).

Data on average swell height arriving at each site are presented in three categories: low (< 0.5 m), moderate (0.5–1.5 m), and high (> 1.5 m), but estimated heights were used in the multiple regressions. Tidal information for Santa Cruz was extracted from naval tide tables of Ecuador’s Instituto Oceanográfico de la Armada (INOCAR), and sea and air temperature data were obtained from the CDRS dock records in Academy Bay taken daily at 3-hr inter-vals. Tides are semi-diurnal, with a maximum spring range of 2 m and a neap range of 1 m. Multiple regression analyses for the variables FD, DFB, and DFB vs various environmental parameters were performed with the SAS statistical package. In these analyses feeding tidal height (Th ) was the tidal height at the mean time of feeding as defined above.

OIL SPILLOn 18 January 2001 an oil spill occurred when the oil tanker JESSICA was wrecked on San

Cristóbal Island (Wikelski et al., 2001a; 2002). Rocky substratum at Site 2 was lightly oiled by diesel and bunker oil on 20–21 January 2001, and this presumably affected the feeding of iguanas until 26 January. The behavior of the iguanas was monitored over 3 d during this period, and also on 27–28 January 2001, when feeding returned to normal.

CHOICE EXPERIMENTSFeeding choice experiments were carried out on basking iguanas at the CDRS dock. Igua-

nas were offered a choice of 5–10 g of each of two species of freshly collected algae juxtaposed on the rock before an iguana, and the outcome observed from a distance.

RESULTS

ALGAL ABUNDANCEAlgal biomass at Site 1 was less than half that at Site 2 during the study period. At

both sites biomass and cover of algae declined with increasing temperature from the cool to the hot season (Figs. 1–3). Mean intertidal algal biomass was inversely cor-related with air temperature (Site 1, r = −0.92, P < 0.001; Site 2, r = −0.56, P = 0.01).

At Site 1 U. lobata, dominant in September, declined in biomass and cover over the next 3 mo, disappeared in January, and then reappeared in May (Fig. 2A). On vertical surfaces at the mid- to low tide mark, algal cover and biomass declined during the hot season (Fig. 2B,C), with biomass lagging cover during the May recovery. Hypnea pannosa J. Agardh, Hypnea spinella (C. Agardh) Kützing, Gelidium pusillum var. pacificum Taylor, and Polysiphonia decussata Hollenberg were variously dominant or sub-dominant during the period (Fig. 2B).


At Site 2 Ulva declined similarly during the hot season, except on elevated rocks in the splash zone where it persisted throughout the year (Fig. 3A). On vertical surfaces, algal cover declined during the hot season as patches became more fragmented, and “bare” areas of crustose algae increased in cover. Hypnea pannosa, H. spinella, P. decussata, and G. pusillum var. pacificum were variously abundant from September to May (Fig. 3B). Algal biomass declined during the entire period (Fig. 3C). Minor species in the genera Padina, Galaxaura, Chaetomorpha, Spatoglossum, Codium, Prionitis and Grateloupia persisted near low water mark.

In general, blade lengths at Site 1 were less than half the length of those at Site 2 (Figs. 4A, B), and mean blade length of avoided species (e.g., H. pannosa, Ulva) was generally greater than that of preferred species (H. spinella, G. pusillum) (see below). But trends in blade length during the study period varied with species. Hypnea spi-nella declined at both sites to ca 4 mm length, which is too short to be further grazed (cf Wikelski et al., 1997). Gelidium pusillum declined at Site 1, but persisted at ca 8 mm length at Site 2 despite grazing. Hypnea pannosa declined in length during and after the hot season at Site 1, but increased during the same period at Site 2. Ptero-cladiella capillacea (S.G. Gmelin) Santelices & Hommersand, although preferred, increased in length at Site 2 until the end of the hot season.

IGUANA GRAZINGSite 1.—Here, ca 25 iguanas, excluding hatchlings, were resident, and the mean

daily number observed grazing during the study was 12.4 (SE 0.8), indicating that iguanas on average grazed on alternate days, assuming high site fidelity as found by Wikelski and Trillmich (1994). The area of exposed grazeable rock at low water was ca 150 m2 including rock pools. Mean iguana density was ca 0.17 m−2, total estimated iguana biomass was 14.6 kg, and mean biomass 48.7 g m−2 d−1, taking into account the alternate-day feeding schedule.

Iguanas grazed near the base of the promontory during the cool season and toward its extremity in the hot season, as swell declined, and algal blade-length decreased through grazing (Fig. 4A). When red algal beds were accessible, red algae were pre-ferred, and with varying choices during the year. Values for E over 8 mo (Fig. 5A)

Figure 1. Air temperatures (°C) at time of low tide, and sea temperatures at flood tide taken at CDRS dock, eastern Academy Bay from October 2000–May 2001.


Figure 2. Algal cover and fresh weight biomass at Site 1, Academy Bay, from October 2000–May 2001. Biomass units are g fresh weight 100 cm−2; samples were taken within algal patches at (A) Mid-intertidal. Proportional cover and biomass of Ulva and red algae. (B) Low intertidal. Proportional cover of Ulva, Hypnea spinella, H. pannosa, Gelidium pusillum and Polysiphonia decussata. (C) Low intertidal. Total algal biomass. Bars are standard errors.


Figure 3. Algal cover and fresh weight biomass (g fresh weight 100 cm−2) at Site 2, Tortuga Bay, from October 2000–May 2001. Biomass values are taken within algal patches at (A) Mid-inter-tidal. Proportional cover and biomass of Ulva. (B) Low intertidal. Proportional cover of Ulva, Hypnea spinella, H. pannosa, Gelidium pusillum, Polysiphonia decussata, and Pterocladiella capillacea. (C) Low intertidal. Total algal biomass. Bars are standard errors.


show that Ulva was mostly avoided, but eaten during high low tides when other spe-cies were unavailable.

Thus, from 9 October to 2 December the proportional number of feeding bites per day on Ulva was correlated with low tide height above datum (N=8; r = 0.705; P = 0.05). Preferred species were H. spinella (October–December), P. decussata (No-vember), G. pusillum (December–May), and H. pannosa briefly in late May (Fig. 4A). Thus, algal preferences changed with algal species’ availability. During the cool sea-son (October–December) the preference hierarchy was:

H. spinella > P. decussata ≥ Ulva > H. pannosa, G. pusillum

Figure 4. Mean blade length (mm) of dominant species of algae grazed by iguanas from October 2000–May 2001 at (A) Site 1, Academy Bay, and (B) Site 2, Tortuga Bay.


and during the hot season (late December–May):

G. pusillum > H. spinella ≥ H. pannosa > Ulva.

Here, the sign (>) indicates a significant preference in >75% of comparisons, the sign (≥) a preference in > 50% of comparisons, and where a preference occurred in < 50% of comparisons, the species are ordered in descending order of weak preference.

During the hot season G. pusillum was significantly preferred to H. pannosa on only 64% of sampling days, possibly because as the hot season progressed the short blade length of G. pusillum made grazing it unprofitable (Fig. 4A). Otherwise there was no evidence that blade length influenced choice. Within species, there was no correlation between E and blade length, and across species there was a highly significant inverse correlation between positive values of E and blade length (r = −0.61; P < 0.001); i.e., iguanas tended to graze species with shorter blades. The preferences described above are broad and do not imply other species were not taken incidentally. While the Ulva mat was virtually monospecific, the H. pannosa and H. spinella mats contained a little Ulva, Chaetomorpha antennina (Bory) Kützing and Jania sp., the G. pusillum mat a little Hypnea spp., and the P. decussata mat a little Centroceras sp.

Site 2.—Here, ca 45 iguanas were resident along ca 75 m of coastline, with a total area of grazing substratum of ca 290 m2, giving a mean density of 0.16 m−2 of available grazing substratum. Estimated total iguana biomass was 27.5 kg and mean iguana biomass was 47.4 g m−2 d−1, assuming the same alternate-day feeding schedule as at Site 1. The outcrop monitored had a surface area of ca 40 m2, and the mean daily number (N = 25) of iguanas grazing there was 10.0 (SE 0.8), suggesting a higher density there of 0.25 m−2. No trend in the daily number of iguanas observed grazing occurred, except during the breeding season in January 2001 (see Trillmich, 1983; Wikelski et al., 2001b for details of breeding season).

Iguanas grazed on the same outcrop on all low tides, except in April 2001 when they grazed on nearby boulders during high low tides or strong swell. Values for E (Fig. 5B) show the shift in algal preferences over time. Ulva was grazed during high low tides, and, like Site 1, the proportional number of feeding bites on Ulva was sig-nificantly correlated with low tide height (N = 8; r = 0.77; P = 0.03). Hypnea spinella was preferred during the cool season, P. capillacea briefly in December during low tides, and G. pusillum in the hot season. Polysiphonia decussata, always with nega-tive E values, was present throughout the year, but rarely eaten. Grateloupia howei (?) Setchell & Gardner, grazed mostly by large submerged males, was preferred once during a zero tide.

During the cool season (September–November) the preference hierarchy of the iguanas at Site 2, using the same criteria as for Site 1, was:

H. spinella > Ulva ≥ G. howei (?) > H. pannosa, P. decussata

and during the December transition:

P. capillacea > G. pusillum, H. spinella > H. pannosa, P. decussata,

and in the hot season (January–May):

G. pusillum > H. spinella, P. capillacea, H. pannosa, G. howei (?), Ulva.


Blade lengths were double those at Site 1, and the only example of a possible effect of blade length was in May when an avoided species, H. pannosa, was preferred to G. pusillum, whose mean blade length was then 6 mm (Figs 4B, 5A). Otherwise, both within and across species, there were no correlations between E and blade length.

CHOICE EXPERIMENTSThe outcome of the choice experiments (Table 1) varied with season. During Sep-

tember–October the iguanas largely ignored all algal food offered, with a choice ex-ercised only once. During November–December the iguanas chose to eat one alga offered in about half the experiments and rejected all algae in the remainder. From

Figure 5. Changes in Ivlev’s electivity coefficient (E) for different species of algae from October 2000–May 2001 at (A) Site 1, Academy Bay, and (B) Site 2, Tortuga Bay.


January to May they variously consumed all algae offered, ate one species only, or rejected both. The trials gave this provisional preference hierarchy:

G. pusillum > H. spinella > Ulva, G. howei (?) > H. pannosa.

Algal preferences at the two sites and in the choice experiments were consistent with each other.

FORAGING ECOLOGYDelay/Anticipation.—The mean time of arrival of iguanas at the feeding sites varied

between seasons and with the timing of low tide. In the cool season iguanas delayed their arrival after early morning low tides (Site 1 only), and anticipated late afternoon low tides by arriving early (both sites). Plots of delay-anticipation in the cool season vs time of low tide for each site (Fig. 6A,B) gave approximately linear relations (Table 2) when regression slopes did not differ significantly (t = 1.3; P = 0.2). Thus, at Site 1 the mean delay in arrival after early morning low tides (before 0730 hrs) was 118 min in the cool season compared with 13 min in the hot season. Conversely, for low tides after 1300 hrs, the mean anticipation was significantly more in the cool season (124 min) than in the hot season (39 min) (Mann-Whitney U test; P = 0.03). In the hot season the mean time of arrival before low tide (12 min at Site 1, and 8 min at Site 2) did not differ significantly from zero at either site (Site 1: r = 0.382, P = 0.18, and Site

Table 1. Result of choice experiments in which two species of algae were offered to iguanas. N = total number of trials, with number of times a choice was made in brackets. Probability, P, is calculated from the binomial test.

N Choice of species offered Result (number of times chosen) P34 (8) H. spinella vs Ulva H. spinella (8) 0.00429 (9) H. spinella vs G. howei (?) H. spinella (8), G. howei (?) (1) 0.02037 (5) G. howei (?) vs H. pannosa Grateloupia sp. (4), H. pannosa (1) 0.18826 (5) G. pusillum vs H. spinella G. pusillum (4), H. spinella (1) 0.18831 (5) G. pusillum vs Ulva G. pusillum (5) 0.031

Figure 6. Delay or anticipation of the daily low tide at the mean time of arrival by iguanas at (A) Site 1, Academy Bay, and (B) Site 2, Tortuga Bay. Negative values on vertical axis are number of minutes of delay in feeding after time of low tide, and positive values are number of minutes in anticipation of the time of low tide. Hot season values (January–May) are open circles and cool season values closed circles.


2: r = 0.516, P = 0.12; see Fig. 6). We excluded two post-oil spill data points at Site 2 when the mean arrival was 56.5 min after time of low water.

Bite Rate, Proportion of Time Feeding and Foraging Duration.—The mean number of foraging excursions per iguana per day was 1.03 at Site 1 and 1.02 at Site 2. How-ever, at the latter site large males made two feeding excursions per low tide on 44% of monitoring days.

The mean bite rate (BR) of iguanas at both sites varied with season and was signifi-cantly correlated with air temperature (Fig. 7A,B; Table 2). BR was also correlated with available algal biomass (AAB; for Site 1, r = −0.42, P = 0.02; for Site 2, r = −0.43, P = 0.04), but this is expected given the effect of grazing on algal biomass and the inverse correlation between temperature and AAB (see above).

Foraging duration (FD) varied between sites and seasonally. At Site 1, FD over the whole period was influenced significantly by swell and temperature but not by tide height or AAB. Swell explained 17% of the variation in the regression and tem-perature 18% (Table 2). However, a clearer picture results when FD is plotted against AAB for the two periods, October–March and April–May, when maximum algal biomass was < 5 g 100 cm−2 (termed the algal threshold; Fig. 8A). FD varied little with algal biomass above the threshold, but increased sharply below it (but for three anomalous data points see caption to Fig. 8A). In the former period mean FD was 32.4 min (SE 1.0) and showed no significant trend with time (N = 20; r = −0.133; P = 0.5), temperature (r = 0.03; P > 0.5), AAB (r = 0.22; P = 0.26) or swell (r = −0.27; P = 0.22). From April to May 2001 FD varied significantly from 50 to 121 min according to swell height (Fig. 8A, Table 2). At Site 2, FD decreased linearly with increasing temperature and swell (Fig. 8B, Table 2), the former accounting for 25% and the latter 16% of the variation.

The proportion of time iguanas were engaged in feeding while at the feeding site (P) varied seasonally and between sites. At Site 1, P increased linearly with increasing tidal height (Th ) and temperature (T), and non-linearly with increasing swell (SW) and AAB (Fig. 9A), and at Site 2, P increased with increasing swell but decreased with increasing temperature (Table 2). Other variables had no significant effect (Fig. 9B).

The mean total number of daily feeding bites (DFB) is the product of the variables,

Figure 7. Mean iguana bite rates (bites 30 sec−1) vs air temperature at (A) Site 1, Academy Bay, and (B) Site 2, Tortuga Bay.


Tabl

e 2.

Reg

ress

ion

equa

tions

rel

atin

g va

riou

s pa

ram

eter

s of

for

agin

g be

havi

or w

ith e

nvir

onm

enta

l par

amet

ers.

Site

1 is

in A

cade

my

Bay

, Site

2 a

t Tor

tuga

Bay

. D

/A is

del

ay/a

ntic

ipat

ion

(min

); B

R is

the

mea

n bi

te r

ate

(bite

s 30

s−1

); F

D is

mea

n fo

ragi

ng d

urat

ion

(min

); P

is th

e m

ean

prop

ortio

n of

tim

e on

fee

ding

gro

und

spen

t fee

ding

; DF

B is

the

mea

n to

tal n

umbe

r of

bite

s pe

r da

y; H

is ti

me

of lo

w w

ater

(nu

mbe

r of

hou

rs f

rom

mid

nigh

t); A

T is

air

tem

pera

ture

at t

ime

of lo

w ti

de;

AA

B is

ava

ilabl

e al

gal b

iom

ass

(g 1

00 c

m−2

); S

W is

sw

ell h

eigh

t (m

), a

nd T

h is

tidal

hei

ght (

m)

at m

ean

time

of f

eedi

ng.

Dep

ende

nt v

aria

ble

Site

NE

quat

ion

Goo

dnes

s of

fit

PD

elay

/ant

icip

atio

n1

16W

inte

r da

ta o

nly

D/A

= −

209.

1 +

19.

63 H

r2 =

0.8

65P

< 0

.001

210

D/A

= −

133.

6 +

14.

32 H

r2 =

0.6

51P

< 0

.001

Mea

n da

ily b

ite r

ate

130

BR

= −

0.18

+ 0

.91

AT

r2

= 0

.612

P <

0.0

01(B

R)

223

BR

= −

0.76

+ 0

.94

AT

r2 =

0.8

14P

< 0

.001

Fora

ging

dur

atio

n (F

D)

1 2

31 10 21

FD

= −

16,0

86 −

4,5

51 S

W +

1,2

20 A

TFo

r A

AB

< 5

g 1

00 c

m−

2

FD

= 1

09.2

− 3

2.3

SWF

D =

16,

734

− 1

,090

.4 S

W −

391

.3 A

T

r2 =

0.5

13

r2 =

0.7

75r2

= 0

.757

SW P

< 0

.03

AT

P <

0.0

002

P <

0.0

01SW

P <

0.0

05A

T P

< 0

.001

Prop

ortio

n of

tim

e on

fe

edin

g gr

ound

spe

nt

feed

ing

(P)

131

P =

−1.

646

+ 0

.477

SW

− 0

.062

SW

2 + 0

.666

Th +

0.0

09 A

T +

0.

007A

AB

− 0

.000

5 A

AB

2χ2

= 1

,271

SW P

< 0

.000

1SW

2 P <

0.0

01T

h P

< 0

.000

1A

AB

P <

0.0

05A

AB

2 P <

0.0

001

AT

P <

0.0

005

221

P =

0.2

63 +

0.0

58 S

W −

0.0

56 A

Tχ2

= 3

59SW

P <

0.0

05A

T P

< 0

.001

Tota

l num

ber

of d

aily

fe

edin

g bi

tes

(DF

B)

129 17 10

DF

B =

−2,

188

+ 1

14.3

AT

For

AA

B >

5 g

100

cm−

2

DF

B =

575

.64

− 1

0.74

AA

BFo

r A

AB

< 5

g 1

00cm

−2

DF

B =

1,4

26.2

− 2

73.8

SW

r2 =

0.4

31

r2 =

0.3

23

r2 =

0.5

35

P <

0.0

001

P <

0.0

5

P <

0.0

52

21D

FB

= 9

32.6

− 4

2.9

SW −

22.

2 A

Tr2

= 0

.630

SW P

= 0

.053

AT

P <

0.0

01


BR, FD, and P. Because iguanas may adjust these variables according to environmen-tal conditions in order to maximize intake, we analyzed DFB directly in relation to the same variables to determine their net effect. At Site 1, DFB declined with in-creasing temperature, and no other variable was significant. However, when the data were analyzed separately for the two successive periods, as described above for FD, a different picture emerged. During the former period, DFB increased linearly with decreasing AAB, and during the latter period DFB was much higher, and increased with decreasing swell (Fig. 10A, Table 2). At Site 2, DFB declined linearly with in-creasing temperature and swell, the former accounting for 33% and the latter 9% of the variation (Fig. 10B, Table 2).

Figure 8. (A) Iguana foraging duration (min) vs available algal biomass (g fresh weight 100 cm−2) at Site 1, Academy Bay in different swell conditions. The vertical dashed line at 5 g is the algal biomass threshold (see text). The three data points in closed triangles below the algal biomass threshold were data obtained during a high low tide when available algal biomass was low. Data obtained in October-March are closed symbols, and data obtained in April–May are open sym-bols. (B) Iguana foraging duration (min.) vs air temperature at Site 2, Tortuga Bay. Post-oil spill data are in open symbols. At both sites, data obtained on days of low swell are shown with circles, data on days of moderate swell with triangles, and data on days of high swell with squares.

Figure 9. Proportion of time iguanas on the feeding grounds spent feeding vs (A) height of the tide at Site 1, Academy Bay. Height of the tide was calculated at the mean time of foraging duration (thus taking into account delay or anticipation in relation to low tide), and (B) air temperature at Site 2, Tortuga Bay. At both sites, data obtained on days of low swell are shown with circles, data on days of moderate swell with triangles, and data on days of high swell with squares.


Grazing by Large Males.—Large males (> 30 cm SVL) grazed in more exposed plac-es than other iguanas, and sometimes submerged in rock pools. Submerged grazing by large males was observed on 45% of the days of observations at Site 1 and 6% of days at Site 2. The mean submergence time (both sites combined) was 2.9 min (N = 24; SE 0.3 min) and maximum submergence time was 6.3 min. The mean bite rate while submerged (N = 8) was 14.2 30 s−1 (SE 0.9), significantly less than the mean bite rates in air (19.2 30 s−1; SE 1.0) of the largest size class on the same days (t = 2.72; P = 0.04). However, mean P while submerged was 0.71 (N = 6, SE 0.08), significantly more than mean P of 0.29 (SE 0.02) for the intertidally feeding population on the same days (t = 2.9; P = 0.02).

Mean FD by large males (N = 8) at Site 1 was 14.2 min (SE 2.3); i.e., 48% of, and significantly less (t = 3.41; P < 0.004) than that of intertidal foragers on the same days, but at Site 2 (N = 9), mean FD was 26.2 min (SE 3.8); i.e., 91% of, and not significantly less than, that of intertidal foragers on the same days (t = 0.56; P > 0.5). The difference in FD of large males between sites was significant (t = 2.38; P = 0.03).

Effect of Oil Spill.—After the January oil spill every measure of the iguanas’ forag-ing behavior declined at Site 2 for 5 d. The mean daily number of grazing iguanas fell significantly from 10.0 to 3.7 (SE 1.1; t = 2.54; P = 0.02); mean FD fell significantly from 30.1 (SE 1.6) to 13.3 min (SE 0.7; t = 3.1; P = 0.005); and mean P fell significantly from 0.26 (SE 0.01) to 0.12 (SE 0.01; t = 4.02; P < 0.001). As a result, mean DFB fell significantly from 343 (SE 18) to 76 (SE 11; t = 3.64; P = 0.002; Fig. 10B). In addition iguanas drank seawater on four occasions, a behavior not previously observed (M. Wikelski, Princeton University; pers. comm.).

DISCUSSION

FOOD CHOICEThe shores of southern Santa Cruz have mixed tropical and temperate elements.

Many calcified algae and an intense grazing regime are tropical features (Wellington, 1975; Lubchenco et al., 1984), while foliose and turfing intertidal algae washed by

Figure 10. Number of iguana feeding bites per day vs (A) available algal biomass at Site 1, Acad-emy Bay, and (B) air temperature at Site 2, Tortuga Bay. At both sites, data obtained on days of low swell are shown with circles, data on days of moderate swell with triangles, and data on days of high swell with squares. At Site 1, cool season data are open symbols, and hot season data are closed symbols.


cool upwelling waters are temperate features (Hatcher, 1983; Hawkins and Hartnoll, 1983; Walsh, 1993). The tropical iguana exploits this temperate algal food resource when conditions of cool temperatures, tide, and wave action favor algal growth, but severely constrain the grazer (Trillmich and Trillmich, 1986; Wikelski et al., 1993; Wikelski and Trillmich, 1994).

Recent studies of the iguana diet at Genovesa and Santa Fé (Wikelski et al., 1997) were conducted at sites where high densities of iguanas (114–382 g m−2 d−1) competed for a limited algal resource (e.g., algal biomass values 0.35–1.1 gfw 100 cm−2). How-ever, on Santa Cruz iguana biomasses were 10%–50% of those studied by Wikelski and colleagues (Kruuk and Snell, 1981; Laurie, 1983), and algal biomasses were up to 10 times higher. These conditions on Santa Cruz gave an opportunity to examine food choice and feeding behavior where food was rarely limiting.

The consistently strong preferences for H. spinella in the cool season and G. pusil-lum in the hot season imply that other influences, such as physical constraints on feeding and relative abundance, had minor influence on diet choice. Tidal height determined the availability, and hence choice, of species such as Ulva and G. howei (?). However, blade length had little effect, except when preferred species were grazed down to 3–5 mm length (Wikelski et al., 1997), and iguanas then switched to other species. The strong inverse correlation between E and blade length at Site 1 implies that grazing on preferred algae persisted until they became too short to graze. The choice experiments were consistent with field observations, but must be accepted with caution due to the iguanas’ irregular participation, except when hungry (Wikel-ski and Wrege, 2000).

Herbivore food choice is influenced by plant nutritional qualities, morphology, toughness, chemical deterrents and attractants, digestibility, and abundance (re-viewed by Lubchenko and Gaines, 1981; Duffy and Hay, 1990; Choat and Clements 1998). While Laurie (1985) noted that some algal genera avoided by iguanas, such as Bifurcaria (= Blossevillea), Laurencia, and Ochtodes contained chemical deterrents, food quality is probably the major determinant of food choice in iguanas. Red algae are generally higher in protein and energy content, and digestibility than green algae (specifically Ulva) and brown algae (specifically Hincksia) (Cooper and Laurie, 1987;

Figure 11. Schematic variable sawtooth model of foraging behavior of iguanas at (A) Academy Bay in the cool season (this study), (B) Tortuga Bay in the hot season (this study), (C) Santa Fé in the cool season (after Wikelski and Trillmich, 1994; Wikelski et al., 1997); (D) Fernandina in the cool season (Trillmich and Trillmich, 1986), and (E) Genovesa in the hot season (after Wikelski et al., 1997). Iguana body temperature, T, falls while foraging and rises while basking, in a saw-tooth manner. Iguanas stop feeding when full or when cold, whichever happens first. Curves fall steeply in the cool season when cooling is fastest, and more slowly in the hot season when cooling is least. When algal biomass is high the iguana suffices with a single feeding excursion, but if algal biomass in the cool season is low, the iguana may require two or more feeding excursions during a low tide.


Laurie, 1989, 1990; Fleming, 1995; Rubenstein and Wikelski, 2003). Hence igua-nas are expected, in accordance with optimal foraging theory (Stephens and Krebs, 1986), to prefer red algae. This prediction was confirmed by Rubenstein and Wikelski (2003) for G. pusillum, which was the most energy-rich species available for iguanas on Santa Fé, and was preferred to other algae, including Ulva. But when preferred species are scarce or unavailable, grazers are expected to switch to more abundant, but less nutritious species (Stephens and Krebs, 1986; Wikelski and Wrege, 2000). This would explain the switch by iguanas to Ulva at high tides and the occasional switch to H. pannosa. The role of seasonally changing nutrient and carbon content of Galápagos algae (Rubenstein and Wikelski, 2003) in influencing food preferences is still poorly known.

FORAGING BEHAVIORDelay and Anticipation.—Wikelski and Hau (1995) proposed two non-exclusive

hypotheses to explain the deviations (morning delay and afternoon anticipation) in iguanas’ bi-tidal (24.8 hrs) foraging rhythm (see also Trillmich and Trillmich, 1986; Buttemer and Dawson, 1993). First, iguanas that arrived first in the intertidal gained a competitive advantage over conspecifics; and second, the temporal shift was al-ways toward midday, with higher temperatures, which favored more efficient feeding (higher bite rates, longer endurance, faster running from swell). Wikelski and Hau (1995) could not test their second hypothesis because at their sites algae were scarce. Where algae are abundant the first hypothesis is redundant because prior arrival confers no feeding advantage. The presence of pronounced delay/anticipation in this study in the cool season with abundant algae, and little or none in the hot season, when cooling is less problematic, clearly supports the second hypothesis. Wikelski and Hau’s (1995) steeper delay/anticipation curves, with up to 3 hrs anticipation for iguanas on food-limited Genovesa and Santa Fé compared with our data suggest that, when food is limiting, competition and increased feeding efficiency act addi-tively to increase anticipation of afternoon tides, but antagonistically to reduce delay after early morning tides.

Excursion Frequency.—Wikelski and Trillmich (1994) hypothesized that the rate of cooling coupled with a severely limited food intake determined the number of feed-ing excursions per day. Cooling rates were higher when the intertidal was subject to continual wave swash (e.g., Santa Fé), and were greater in the cool season than the hot season. During a single low tide at Santa Fé, rapidly cooling iguanas shuttled between feeding and basking sites from 1.2 to 2.8 times a day according to size, and spent 60% of their time feeding, and 27% of their time running from waves (Wikelski and Trillmich, 1994). At Fernandina, iguanas averaged 1.9 foraging excursions per day and spent 67% of their time feeding (Trillmich and Trillmich, 1986). At our sites, with abundant algae, and less swash, and hence a lower cooling rate, one feeding ex-cursion on a given day, with more time resting, and no time running, was sufficient, consistent with Wikelski and Trillmich’s (1994) cooling hypothesis.

Mean Daily Feeding Bites (DFB) and Its Components.—Foraging duration is the outcome of the interaction between available algal biomass (AAB), which, via blade length, determines the amount ingested per bite (Wikelski et al., 1997), and the two components of foraging, bite rate (BR), and proportion of time feeding (P). BR seems to be temperature-dependent. It slows diurnally during feeding as the iguana cools


(Wikelski and Trillmich, 1994); seasonally it increases with temperature (this study); and geographically, it is higher on the more northern islands (Wikelski et al., 1997).

Two main constraints of the foraging components, P and FD, are high low tides, which limit feeding time and foraging area, and high swell, which increases wave swash and the cost of feeding (faster cooling and more difficult adhesion). Consider P. The significance of all four variables affecting DFB at Site 1, namely swell, tidal height, temperature, and available algal biomass, imply that, with increasingly ad-verse conditions, the iguanas compensated for the reduced grazing time available by feeding more efficiently; i.e., pausing for less time between feeding bouts. The rela-tions were non-linear for the variables AAB and swell, because (a) the effect of low AAB increasing P was relatively stronger below the biomass threshold than above it, and (b) the influence of increasing swell on P plateaued. At Site 2, with high algal biomass, and a more elevated feeding site, swell was the only significant constraint to feeding. Here, as temperatures rose and bite rates increased, the iguanas presum-ably cooled less and fed more leisurely. Thus, increasing temperature seemed to have opposite effects at the two sites; pausing between feeding bouts reduced grazing ef-ficiency at Site 1 when algae were scarce, but not at the elevated Site 2 with abundant algae. Wikelski and Trillmich (1994) noted similar behavioral shifts by iguanas in response to environmental harshness at Santa Fé.

The differing patterns of FD at the two sites are explained by the interaction be-tween the various constraints to feeding. Tidal height and swell had no effect on FD when algal biomass was above the threshold (Site 1 September–March, and Site 2 all year) because foraging efficiency was high. But with low algal biomass (Site 1 March–May) adverse conditions had an exaggerated effect because iguanas could prolong FD with low loss of heat, except when constrained by swell and high low tides (see Wikelski and Trillmich (1994) for similar effects at Santa Fé). At Site 2, increasing temperature over time increased foraging efficiency by increasing BR, and so reduced FD; however, increased efficiency was constrained by swell, but not tidal height (cf. Wikelski et al., 1997).

Overall, DFB integrates the various interacting effects described above. Increasing algal biomass, above the threshold, and increasing temperature, which both increase feeding efficiency, were the major influences on DFB, as found by Wikelski et al. (1997). However, the influence of the major constraint, swell, on DFB was much less than on FD due to a compensatory increase in P at both sites (see above). At Site 1, swell became significant only below the algal biomass threshold, and at Site 2, swell accounted for only a small fraction (9%) of the variation explained by the regres-sion.

In an inter-island comparison, DFB broadly correlates inversely with algal bio-mass, emphasizing the key role of food supply underlying foraging strategies. Thus DFB was 2500–3500 bites d−1 on Genovesa, 550–750 on Santa Fé (see Wikelski et al., 1997), 200–1550 at Site 1 according to algal abundance, and 300–450 at Site 2.

We can now integrate the numerous studies of iguana foraging by extending Wikelski and Trillmich’s (1994) sawtooth model to incorporate seasonal effects and algal abundance (Fig. 11). Rates of cooling in the model are schematic and inferred from published data. Where cooling is rapid, as in the cool season, and algal biomass low, iguanas make repeated feeding excursions. With higher ambient temperature, iguanas suffice with a single feeding excursion whose length depends on algal abun-dance. The model does not consider the effect of shoreline topography or degree of


exposure to swell either on algal abundance or on rate of iguana cooling. Flat ex-panses of intertidal rock, as at Punta Espinoza, Fernandina (Nagy and Shoemaker, 1984), would likely reduce the cooling rate of grazing iguanas, whereas steep rock faces with high wave energy, as in this study, would both increase algal abundance and increase the cooling rate.

LARGE MALESAccording to Trillmich (1983) and Wikelski and Trillmich (1997), large males for-

age subtidally because they need the additional food available there for maintenance. At our sites algae were virtually absent subtidally due to intense sea urchin and fish grazing, but abundant in low intertidal rock pools where large males sometimes fed. Submerged feeding was clearly more efficient than intertidal feeding at Site 1, where FD was less than half, although DFB changed little due to a high compensatory value of P. At Site 2 preferred species were all intertidal, and this apparently favored inter-tidal feeding.

OIL SPILLAlthough hydrocarbon residues at Site 2 had dissipated within 11 d of the spill

(Anon., 2002), slight contamination was the most likely cause of the aberrant feed-ing behavior of iguanas in the 5 d following the arrival of oil. No post-spill iguana mortality was observed, in contrast to the high mortalities at Santa Fé (Wikelski et al., 2002), much closer to the source of the spill. Feeding behavior may be a sensitive indicator of slight contamination.

ACKNOWLEDGMENTS

We thank CDRS for use of research facilities and accommodation while in the Galápagos, and G. J. Edgar for his support for the study. The second author thanks University of British Columbia for sabbatical leave, the first author for the opportunity to work on the project, and A. Tye, Head of Botany at CDRS, for valued suggestions for working in the Galápagos. Y. Xiao kindly helped with the regression analyses, M. Wikelski provided much advice, and with R. Day, T. Ward, and G. Edgar and anonymous referees, helpfully criticized the manuscript.

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DATE SUBMITTED: 6 May, 2003. DATE ACCEPTED: 1 October, 2004.

ADDRESSES: (S.A.S.) Senior Research Fellow, South Australian Research and Development Institute, PO Box 120, Henley Beach 5022, Australia. E-mail: <[email protected]>. (M.W.H.) Dept of Botany, University of British Columbia, No. 3529-6270 Univer-sity Blvd., Vancouver, B.C. Canada V6T 1Z4. E-mail: <[email protected]>.

algal food preferences and seasonal foraging strategy of the marine iguana, amblyrhynchus cristatus,...

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