BULLETIN OF MARINE SCIENCE, 77(1): 51–72, 2005
ALGAL FOOD PREFERENCES AND SEASONAL FORAGING
STRATEGY OF THE MARINE IGUANA, AMBLYRHYNCHUS
CRISTATUS, ON SANTA CRUZ, GALÁPAGOS
Scoresby A. Shepherd and Michael W. Hawkes
ABSTRACT
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 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
© 2005 Rosenstiel School of Marine and Atmospheric Science
of the University of Miami
51
52
BULLETIN OF MARINE SCIENCE, VOL. 77, NO. 1, 2005
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 mid- to 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 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 BEHAVIOR
The foraging and feeding behavior of iguanas was monitored at 1–2-wk intervals over an 8mo 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 arrival 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
54
BULLETIN OF MARINE SCIENCE, VOL. 77, NO. 1, 2005
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 individual, 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), identifiable 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 coefficient, 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 = ri − pi ri + pi
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 proportional availability of each habitat type according to tidal height from the linear relations:
M u + Lra = 1 and M u = a + Th
where T h is the tidal height, and 0 < T h < 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
SHEPHERD AND HAWKES: ALGAL FOOD PREFERENCES AND FORAGING OF GALÁPAGOS MARINE IGUANA
55
linearly to zero when the tidal height was 0.8. Total available algal biomass (AAB) was calculated 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:
Ai = Biu ∗ Ciu ∗ M u + Bir ∗ Cir ∗ Lra
where Biu and Bir are the respective biomasses (g 100 cm−2) of the ith species within algal patches 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 resident 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 intervals. 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 (T h ) was the tidal height at the mean time of feeding as defined above.
OIL SPILL
On 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 EXPERIMENTS
Feeding choice experiments were carried out on basking iguanas at the CDRS dock. Iguanas 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 ABUNDANCE
Algal 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 correlated 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).
56
BULLETIN OF MARINE SCIENCE, VOL. 77, NO. 1, 2005
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.
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 spinella 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. Pterocladiella capillacea (S.G. Gmelin) Santelices & Hommersand, although preferred,
increased in length at Site 2 until the end of the hot season.
IGUANA GRAZING
Site 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 preferred, and with varying choices during the year. Values for E over 8 mo (Fig. 5A)
SHEPHERD AND HAWKES: ALGAL FOOD PREFERENCES AND FORAGING OF GALÁPAGOS MARINE IGUANA
57
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.
58
BULLETIN OF MARINE SCIENCE, VOL. 77, NO. 1, 2005
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-intertidal. 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.
SHEPHERD AND HAWKES: ALGAL FOOD PREFERENCES AND FORAGING OF GALÁPAGOS MARINE IGUANA
59
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.
show that Ulva was mostly avoided, but eaten during high low tides when other species 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 (November), G. pusillum (December–May), and H. pannosa briefly in late May (Fig. 4A).
Thus, algal preferences changed with algal species’ availability. During the cool season (October–December) the preference hierarchy was:
H. spinella > P. decussata ≥ Ulva > H. pannosa, G. pusillum
60
BULLETIN OF MARINE SCIENCE, VOL. 77, NO. 1, 2005
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 significantly 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 negative 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.
SHEPHERD AND HAWKES: ALGAL FOOD PREFERENCES AND FORAGING OF GALÁPAGOS MARINE IGUANA
61
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.
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 EXPERIMENTS
The outcome of the choice experiments (Table 1) varied with season. During September–October the iguanas largely ignored all algal food offered, with a choice exercised 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
62
BULLETIN OF MARINE SCIENCE, VOL. 77, NO. 1, 2005
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
34 (8)
29 (9)
37 (5)
26 (5)
31 (5)
Choice of species offered
H. spinella vs Ulva
H. spinella vs G. howei (?)
G. howei (?) vs H. pannosa
G. pusillum vs H. spinella
G. pusillum vs Ulva
Result (number of times chosen)
H. spinella (8)
H. spinella (8), G. howei (?) (1)
Grateloupia sp. (4), H. pannosa (1)
G. pusillum (4), H. spinella (1)
G. pusillum (5)
P
0.004
0.020
0.188
0.188
0.031
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 ECOLOGY
Delay/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
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.
SHEPHERD AND HAWKES: ALGAL FOOD PREFERENCES AND FORAGING OF GALÁPAGOS MARINE IGUANA
63
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.
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. However, 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 significantly 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 temperature 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 (T h ) 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,
Total number of daily
feeding bites (DFB)
Proportion of time on
feeding ground spent
feeding (P)
Mean daily bite rate
(BR)
Foraging duration
(FD)
Dependent variable
Delay/anticipation
21 P = 0.263 + 0.058 SW − 0.056 AT
29 DFB = −2,188 + 114.3 AT
For AAB > 5 g 100cm−2
17 DFB = 575.64 − 10.74 AAB
For AAB < 5 g 100cm−2
10 DFB = 1,426.2 − 273.8 SW
21 DFB = 932.6 − 42.9 SW − 22.2 AT
2
1
2
31 P = −1.646 + 0.477 SW − 0.062 SW2 + 0.666 Th + 0.009 AT +
0.007AAB − 0.0005 AAB2
N Equation
16 Winter data only
D/A = −209.1 + 19.63 H
10 D/A = −133.6 + 14.32 H
30 BR = −0.18 + 0.91 AT
23 BR = −0.76 + 0.94 AT
31 FD = −16,086 − 4,551 SW + 1,220 AT
For AAB < 5 g 100 cm−2
10 FD = 109.2 − 32.3 SW
21 FD = 16,734 − 1,090.4 SW − 391.3 AT
1
2
2
1
2
1
Site
1
r2 = 0.535
r2 = 0.630
r2 = 0.323
r2 = 0.431
χ2 = 359
χ2 = 1,271
r2 = 0.775
r2 = 0.757
r2 = 0.865
r2 = 0.651
r2 = 0.612
r2 = 0.814
r2 = 0.513
Goodness of fit
P < 0.05
SW P = 0.053
AT P < 0.001
P < 0.05
P < 0.001
P < 0.001
P < 0.001
P < 0.001
SW P < 0.03
AT P < 0.0002
P < 0.001
SW P < 0.005
AT P < 0.001
SW P < 0.0001
SW2 P < 0.001
Th P < 0.0001
AAB P < 0.005
AAB2 P < 0.0001
AT P < 0.0005
SW P < 0.005
AT P < 0.001
P < 0.0001
P
Table 2. Regression equations relating various parameters of foraging behavior with environmental parameters. Site 1 is in Academy Bay, Site 2 at Tortuga Bay.
D/A is delay/anticipation (min); BR is the mean bite rate (bites 30 s−1); FD is mean foraging duration (min); P is the mean proportion of time on feeding ground
spent feeding; DFB is the mean total number of bites per day; H is time of low water (number of hours from midnight); AT is air temperature at time of low tide;
AAB is available algal biomass (g 100 cm−2); SW is swell height (m), and Th is tidal height (m) at mean time of feeding.
64
BULLETIN OF MARINE SCIENCE, VOL. 77, NO. 1, 2005
SHEPHERD AND HAWKES: ALGAL FOOD PREFERENCES AND FORAGING OF GALÁPAGOS MARINE IGUANA
65
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 symbols. (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.
BR, FD, and P. Because iguanas may adjust these variables according to environmental 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 increasing 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 increasing temperature and swell, the former accounting for 33% and the latter 9% of
the variation (Fig. 10B, Table 2).
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.
66
BULLETIN OF MARINE SCIENCE, VOL. 77, NO. 1, 2005
Figure 10. Number of iguana feeding bites per day vs (A) available algal biomass at Site 1, Academy 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.
Grazing by Large Males.—Large males (> 30 cm SVL) grazed in more exposed places 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’ foraging 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 CHOICE
The 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
SHEPHERD AND HAWKES: ALGAL FOOD PREFERENCES AND FORAGING OF GALÁPAGOS MARINE IGUANA
67
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 sawtooth 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.
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). However, 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. pusillum 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 (Wikelski and Wrege, 2000).
Herbivore food choice is influenced by plant nutritional qualities, morphology,
toughness, chemical deterrents and attractants, digestibility, and abundance (reviewed 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;
68
BULLETIN OF MARINE SCIENCE, VOL. 77, NO. 1, 2005
Laurie, 1989, 1990; Fleming, 1995; Rubenstein and Wikelski, 2003). Hence iguanas 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 BEHAVIOR
Delay 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 always 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 additively 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 feeding 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 excursion 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
SHEPHERD AND HAWKES: ALGAL FOOD PREFERENCES AND FORAGING OF GALÁPAGOS MARINE IGUANA
69
(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 adverse conditions, the iguanas compensated for the reduced grazing time available by
feeding more efficiently; i.e., pausing for less time between feeding bouts. The relations 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 presumably cooled less and fed more leisurely. Thus, increasing temperature seemed to have
opposite effects at the two sites; pausing between feeding bouts reduced grazing efficiency 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 between 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 regression.
In an inter-island comparison, DFB broadly correlates inversely with algal biomass, 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 abundance. The model does not consider the effect of shoreline topography or degree of
70
BULLETIN OF MARINE SCIENCE, VOL. 77, NO. 1, 2005
exposure to swell either on algal abundance or on rate of iguana cooling. Flat expanses 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 MALES
According to Trillmich (1983) and Wikelski and Trillmich (1997), large males forage 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 intertidal feeding.
OIL SPILL
Although 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 feeding 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.
LITERATURE CITED
Anon. 2002. Biological impacts of the Jessica oil spill on the Galápagos environment. Charles
Darwin Foundation for the Galápagos Islands, Puerto Ayora, Santa Cruz. 137 p.
Bartholomew, G. A. 1978. Post cruise report of the RV ALPHA HELIX expedition for the study
of physiological and behavioral adaptations of the Galapagos iguanas. Unpub. rep. Charles
Darwin Research Station. Santa Cruz. 11 p.
________________, A. F. Bennett, and W. R. Dawson. 1976. Swimming, diving and lactate production of the marine iguana Amblyrhynchus cristatus. Copeia 709–720.
Buttemer, W. A. and W. R. Dawson. 1993. Temporal pattern of foraging and microhabitat use
by Galápagos marine iguanas, Amblyrhynchus cristatus. Oecologia 96: 56–64.
Carpenter, C. C. 1966. The marine iguana of the Galapagos Islands, its behaviour and ecology.
Proc. Calif. Acad. Sci. 34: 329–376.
Choat, J. H. and K. D. Clements. 1998. Vertebrate herbivores in marine and terrestrial environments: a nutritional ecology perspective. Annu. Rev. Ecol. Syst. 29: 375–403.
SHEPHERD AND HAWKES: ALGAL FOOD PREFERENCES AND FORAGING OF GALÁPAGOS MARINE IGUANA
71
Cinelli, F. and P. Colantoni. 1974. Alcune osservacioni sulla zonacione del benthos marino sulle
coste rocciose delle isole Galápagos (Oceano Pacifico). Museo zoologico dell’Universita di
Firenze. 22 p.
Cooper, J. E. and W. A. Laurie. 1987. Investigation of deaths in marine iguanas, (Amblyrhynchus cristatus) on the Galapagos. J. Comp. Path. 97: 129–135.
Darwin, C. 1845. Journal of researches into the natural history and geology of the countries
visited during the voyage of HMS Beagle around the world under the command of Capt.
Fitzroy R.N. 2nd Revised Ed. John Murray, London. 520 p.
Dawson, W. R., G. A. Bartholomew, and A. F. Bennett. 1977. A reappraisal of the aquatic specialisations of the Galapagos marine iguana (Amblyrhynchus cristatus). Evolution 31: 891–
897.
Duffy, J. E. and M. E. Hay. 1990. Seaweed adaptations to herbivory. Bioscience 40: 1286–1298.
Estes G., M. Jackson, and B. Meatyard. 1982. Feeding ecology of marine iguanas (Amblyrhynchus cristatus) at Punta Nuñez, Santa Cruz. Informe anual 1982. Estación Científica Charles
Darwin 319–320.
Feldmann, G. C. 1986. Patterns of phytoplankton production around the Galapagos Islands.
Pages 77–106 in J. Bowman, M. Yentsch, and W.T. Peterson, eds, Lecture notes on coastal
and estuarine studies, Vol. 17. Springer-Verlag, Berlin.
Fleming, A. E. 1995. Growth, intake, feed conversion efficiency and chemosensory preference
of the Australian abalone, Haliotis rubra. Aquaculture 132: 297–311.
Frost, I. and M. B. Frost. 1983. Limitations to algal growth in the Galapagos islands: its consequences on the breeding strategy of the marine iguana Amblyrhynchus cristatus. Noticias
de Galapagos 37: 23–4.
Hatcher, B. G. 1983. Grazing in coral reef ecosystems. Pages 164–179 in D.J. Barnes, ed. Perspectives on coral reefs. Clouston, Canberra.
Hawkins, S. J. and R. G. Hartnoll. 1983. Grazing on intertidal algae by marine invertebrates.
Oceanogr. Mar. Biol. Ann. Rev. 21: 195–282.
Houvenaghel, G. T. 1978. Oceanographic conditions in the Galápagos archipelago and their
relationships with life on the islands. Pages 181–200 in R. Boje and P. Tomczak, eds, Upwelling systems. Springer, Berlin.
__________ and N. Houvenaghel. 1974. Aspects écologiques de la zonation intertidale sur les
côtes rocheuses des îles de Galapagos. Mar. Biol. 26: 135–152.
Ivlev, V. S. 1961. Experimental ecology of the feeding of fishes. Yale University Press, New
Haven. 354 p.
Kruuk, H. and H. Snell. 1981. Prey selection by feral dogs from a population of marine iguanas
Amblyrhynchus cristatus. J. Appl. Ecol. 18: 197–204.
Laurie, A. W. 1983. Marine iguanas in Galapagos. Oryx 17: 18–25.
___________. 1985. Population dynamics and social organization of marine iguanas in the
Galapagos. Progress Report No. 5. Charles Darwin Research Station, Santa Cruz. 27 p.
__________. 1989. Effects of the 1982-83 El Niño sea warming on marine iguanas (Amblyrhynchus cristatus Bell 1825) populations on Galápagos. Pages 121–143 in P. Glynn ed., Global
consequences of the 1982–83 El Niño–Southern Oscillation. Elsevier, New York.
__________. 1990. Population biology of marine iguanas (Amblyrhynchus cristatus) I. Changes
in fecundity related to a population crash. J. Anim. Ecol. 59: 515–528.
Lubchenko, J. and S. D. Gaines. 1981. A unified approach to marine plant-herbivore interactions. I. Populations and communities. Annu. Rev. Ecol. Syst. 12: 405–437.
__________, B. A. Menge, S. D. Garrity, P. J. Lubchenco, L. R. Ashkenas, S. D. Gaines, R. Emlet,
J. Lucas, and S. Strauss. 1984. Structure, persistence, and role of consumers in a tropical
rocky intertidal community (Taboguilla Island, Bay of Panama). J. Exp. Mar. Biol. Ecol. 78:
23–73.
Nagy, K. A. and V. H. Shoemaker. 1984. Field energetics and food consumption of the Galapagos marine iguana, Amblyrhynchus cristatus. Physiol. Zool. 57: 281–290.
72
BULLETIN OF MARINE SCIENCE, VOL. 77, NO. 1, 2005
Okey, T. A., S. A. Shepherd, and P. Martinez. 2003. A new record of anemone barrens in the
Galapagos. Noticias de Galápagos 62: 17–20.
Rubenstein, D. R. and M. Wikelski. 2003. Seasonal changes in food quality: a proximate cue for
reproductive timing in marine iguanas. Ecology 84: 3013–3023.
Stephens, D. W. and J. R. Krebs. 1986. Foraging theory. Princeton University Press, Princeton.
247 p.
Strauss, R. E. 1979. Reliability estimates for Ivlev’s electivity index, the forage ratio, and a proposed linear index of food selection. Trans. Am. Fish. Soc. 108: 344–352.
Trillmich, K. G. K. 1983. The mating system of the marine iguana (Amblyrhynchus cristatus).
Zeitschrift fur Tierpsycologie 63: 141–172.
________________ and F. Trillmich. 1986. Foraging strategies of the marine iguana, Amblyrhynchus cristatus. Behav. Ecol. Sociobiol. 18: 259–266.
Walsh, F. 1993. Biological monitoring of Academy Bay seashores 1988–1991. Unpubl. rep.,
Charles Darwin Research Station, Santa Cruz. 46 p.
Wellington, G. 1975. The Galapagos marine environment. Report to Department of Parks and
Wildlife, Quito. Charles Darwin Research Station, Santa Cruz. 357 p.
White, F. N. 1973. Temperature and the Galapagos marine iguana: insights into reptilian regulation. Comp. Biochem. Physiol. 45: 503–513.
Wikelski, M. and M. Hau. 1995. Is there an endogenous tidal foraging rhythm in marine iguanas? J. Biol. Rhythms 10: 335–349.
___________ and F. Trillmich. 1994. Foraging strategies of the Galápagos marine iguana (Amblyrhynchus cristatus): adapting behavioral rules to ontogenetic size change. Behaviour
128: 255–279.
__________ and __________. 1997. Body size and sexual size dimorphism in marine iguanas
fluctuate as a result of opposing natural and sexual selection: an island comparison. Evolution 51: 922–936.
__________ and P. H. Wrege. 2000. Niche expansion, body size, and survival in Galápagos marine iguanas. Oecologia 124: 107–115.
__________, V. Carillo, and F. Trillmich. 1997. Energy limits to body size in a grazing reptile, the
Galapagos marine iguana. Ecology 78: 2204–2217.
__________, M. B. Gall, and F. Trillmich 1993. Ontogenetic changes in food intake and digestion rate of the herbivorous marine iguana (Amblyrhynchus cristatus Bell) Oecologia 94:
373–379.
__________, L. M. Romero, and H. L. Snell. 2001a. Marine iguanas oiled in the Galápagos. Science 292: 437–438.
__________, C. Carbone, P. A. Bednekoff, S. Choudhury, and S. Tebbich. 2001b. Why is female
choice not unanimous? Insights from costly mate sampling in marine iguanas. Ethology
107: 623–638.
__________, V. Wong, B. Chevalier, N. Rattenborg, and H. L. Snell. 2002. Marine iguanas die
from trace oil pollution. Nature 417: 607–608.
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: <shepherd.scoresby@saugov.
sa.gov.au>. (M.W.H.) Dept of Botany, University of British Columbia, No. 3529-6270 University Blvd., Vancouver, B.C. Canada V6T 1Z4. E-mail: <[email protected]>.