The
Stressful Life of the Galápagos Marine Iguana:
Natural and
Anthropogenic Pressures
Although not as
physically impressive as the giant tortoise, as intriguing as the blue-footed
booby, or as famous as the Darwin’s Finches, one of the Galápagos’ most unique
endemic species may well be the marine iguana, Amblyrhynchus cristatus.
Marine iguanas can be found on almost every island in the Galápagos,
including many tiny islets and rocky outcroppings, and are most abundant in
areas with shallow reefs and large intertidal zones (Boersma and Bowman 1983,
Jackson 1993). Uniquely suited to a
partially terrestrial, partly marine lifestyle, marine iguanas have the most efficient
salt excreting glands of any reptile, allowing them to feed on macrophytic
green and red algae, then get rid of the salt by “sneezing” (Wikelski 1990,
Jackson 1993). Though they most
commonly feed on algae covered rocks in the intertidal zone during low tide,
marine iguanas are famous for their ability to dive in the waves to forage for
food. Dives are usually shallow
(1.5-5m) and only last for a few minutes, but marine iguanas are capable of
diving deeper than 12 meters and remaining submerged for up to an hour
(Wikelski 1990, Jackson 1993).
Marine iguanas
rarely take full advantage of such developed diving abilities, however, because
of the challenge presented by thermoregulation. Unlike other grazing animals, poikilothermic marine iguanas can
only forage as long as they can maintain their body temperature. They usually feed until their body
temperature is just above the water temperature—often up to 10ºC lower than
their ideal body temperature of 35.5ºC—and their heart rate has dropped from
100 to 30, then return to land. To warm
up, they flatten their bodies against rocks to absorb as much heat as possible,
switching to a basking position with the torso raised to avoid overheating
after they reach optimum body temperature.
If they get too hot, they can pant to cool off (Jackson 1993). Marine iguanas are highly social (densities
can exceed 3000 iguanas/kilometer of coastline) and often spend the night in
crevices in piles of up to 50 iguanas, primarily for the purpose of heat
conservation (Wikelski 1990).
Marine iguanas
are also limited in their foraging by the time of day during which their food
is available. Since they feed in
intertidal areas, iguanas must forage during low tide and therefore usually eat
once a day, or sometimes less frequently.
Careful observation has suggested that they synchronize their feeding
with the tides through the interaction of a circadian and circatidal rhythm,
making them the only terrestrial organisms to use a combination of the two
biorhythms (Wikelski and Hua 1995).
Breeding season
for marine iguanas can vary between populations and within the same population
from year to year, but mating generally begins in January. Males abandon their usual social groups and
begin to defend territory, displaying their red, green, and orange mating
colors (Wikelski 1990). Males challenge
each other with head-bobbing displays and fights sometimes ensue, making
reproduction a very costly part of a male iguana’s life, to the point that some
males take a year off from mating to recover (Wikelski 1990)!
Reproduction is
not very easy for females either; mating involves being held by the neck and
dragged around, sometimes for up to 25 minutes (Wikelski 1990)! After copulation occurs, the female looks
for a place in a sandy area to dig a nest (fights can break out in areas where
good nesting sites are scarce, such as on Española), then lays 2-4 eggs, about
the size of chicken eggs, which she watches carefully for about 95 days. Juvenile mortality can be high (up to 60%) during
the first year, since snakes, lava gulls, Galápagos hawks, and, on inhabited
islands, feral cats and dogs, prey on young (Wikelski 1990).
Although no
other lizards in the world share marine iguanas’ dependence on both a
terrestrial and marine ecosystem and their unique adaptations for this
lifestyle, genetic studies have suggested that the ancestors to marine iguanas
had already diverged from the ancestors of the Galápagos’ endemic land iguanas
when both arrived from the mainland.
The marine iguanas’ ancestors probably already possessed their nasal
salt glands and diving ability, so they needed only to evolve in response to
available food sources and form social groups (Wikelski 1990). In an ecosystem with few predators and no
interspecific competition, marine iguanas quickly adapted to feed on
macrophytic green and red algae, a food source they share only with crabs. Today, spatial and temporal food
availability continues to play a key role in shaping the populations and
distributions of marine iguanas in the Galapagos, particularly when it comes to
the iguanas’ size. And in marine
iguanas, size matters. Marine iguanas
are sexually dimorphic, but both males and females gain advantages from larger
body size. Larger males attract more
mates, and larger females have greater fertility (Wikelski, Carrillo, and
Trillmich 1997). Additionally, only
larger iguanas (greater than 2kg) are capable of subtidal foraging in areas
with high wave action, and larger iguanas can feed more independently of the
tide cycle, taking advantage of warmer water and more sun by foraging at noon
everyday (Wikelski 1990).
Still, Wikelski
has found that marine iguanas do not reach the maximum size that could be
predicted based only on possible food intake, and instead are limited by
environmental factors distinct to each island and population (Wikelski and
Wrege 2000). Variation in the size of
iguanas is huge: the largest males on Fernandina can weigh more than five
kilograms (the largest recorded weighed 12kg), while males on Genovesa may only
reach two kilograms (Wikelski 1990). In
general, the largest iguanas are found on the southwest islands where the cold
Cromwell Current brings nutrients that increase productivity, providing more
algae growth (Wikelski 1990).
Even within
populations, the seemingly simple idea that “bigger is better” is not
necessarily true. Wikelski, Carrillo,
and Trillmich (1997) found that the largest iguanas in two different
populations on Santa Fe and Genovesa were less efficient feeders than somewhat
smaller iguanas in their respective groups, though the threshold size at which
larger individuals reached a negative energy was very different in each
population. In addition to having lower
bite rates than smaller individuals, larger iguanas were often forced to feed
in less-preferred areas, a phenomenon that occurs in other grazing species and
is known as “grazing succession” (Wikelski, Carrillo, and Trillmich 1997). Because of their less efficient feeding,
larger iguanas are the most likely to be affected by food shortages such as
those that occur during El Niño years (Wikelski, Carrillo, and Trillmich
1997).
Response to Environmental Stress:
Marine Iguanas and El Niño
At
first glance, it seems hard to believe that iguanas feeding in the intertidal
zone, where they share green and red algae with a variety of crabs, can find
enough food. The key lies in the fact
that algae is quick to reproduce, so the biomass is much larger than is
obviously apparent (Jackson 1993).
Thirty-seven grams of algae per day is plenty to feed a one-kilogram
iguana, and algae usually grows fast enough to support large populations with
high densities (Wikelski 1990).
However, when algae production declines, as is the case during years
when El Niño affects the Galápagos, marine iguana populations suffer
greatly. During El Niño events, the sea
temperature, usually between 18 and 23ºC, can exceed 30ºC for months at a
time. Algae production nosedives
because the nutrients that come with colder water are unavailable (Romero and
Wikelski 2001).
Scientists
first began examining the affects of El Niño on marine iguanas after the very
severe 1982-83 El Niño. Cooper and
Laurie (1987) found that mortality was about 67% during the El Niño, and they
concluded that deaths were caused by starvation due to the iguanas’ inability
to digest brown algae, which they ate when green and red algae was
unavailable. Researchers got the chance
to look deeper into El Niño’s effects during the 1997-98 El Niño, one of the
longest and severest in history, causing up to 90% mortality in some
populations (Romero and Wikelski 2001).
Romero and
Wikelski (2001) carefully studied marine iguana populations on six different
islands, examining stress hormones to determine the iguanas’ response to the environmental
stress created by El Niño. Despite
little competition and predation, marine iguanas, like all animals, need coping
mechanisms to help them survive adverse conditions, and in vertebrates, part of
the stress response includes the release of glucocorticoid steroid
hormones. Over short term periods,
increased levels of corticosterone, the specific hormone found in reptiles, can
be beneficial, but chronic high levels can lead to problems including reproductive
failure and neural damage (Romero and Wikelski 2002).
In
their El Niño study, Romero and Wikelski took blood samples within two to three
minutes after capturing iguanas (the corticosteroid response does not begin
until at least three minutes after initial exposure to the stressful stimulus)
then again after 15 and 30 minutes of restraint stress in a cloth bag. Some iguanas from Santa Fe were held for
another sample after 60 minutes as well.
The researchers also used a body condition index, (mass/snout-vent
length3) x 106, as a measure of how well the iguanas were
coping and to allow for an inter-island comparison (Romero and Wikelski
2001). Their results were very
consistent: the maximum body condition index was approximately 60, and animals
with an index less than 25 were the most likely to die. The range of indexes was different among
islands, with the lowest indices on Fernandina and North Seymour and the
highest on Santa Cruz. Different
islands also had different baseline and stress-induced levels, which where
higher than non-El Niño levels on all islands but Santa Cruz, and on all
islands iguanas with a body condition index less than 35 had higher
corticosterone levels that were highly correlated with body condition (Romero
and Wikelski 2001).
Because
there was such a pronounced correlation between body condition and
corticosterone level, the researchers used both factors to predict survival and
found that a combination of the two was a better predictor than just body
condition alone. Because none of the
animals in the study were able to eat as much as they could in a non-El Niño
year, the scientists realized that fasting alone is not sufficient to raise
corticosterone levels; instead, marine iguanas may use other strategies to keep
a body condition index greater than 35 for as long as possible, with high
levels of corticosterone indicating a last-ditch effort to survive. Corticosterone release then may be crucial
in natural selection, lending support to the idea that El Niño has been and continues
to be an important selective force in marine iguana populations (Wikelski and
Romero 2001).
Among
the strategies marine iguanas may use to survive adverse conditions during El
Niño years is to shrink in body size.
During El Niño periods between 1990 and1999, when the phenomenon was unusually
frequent, scientists observed iguanas that shrunk in length up to 20% (Wikelski
and Thom 2000). That drastic a change
cannot fully be explained by shrinkage in connective tissue and cartilage,
which only account for 10% of body length, suggesting that marine iguanas may
be the only adult vertebrates that can shrink and regrow, yet another of the
species’ unique adaptations. Because
larger iguanas have lower foraging efficiency and require more food, the ability
to shrink and regrow can mean the difference between dying during an El Niño or
surviving to the maximum life span of 28 years (during which time an iguana may
experience several El Niños) (Wikelski and Thom 2000).
One
survival strategy marine iguanas do not usually adopt during times of food
shortage is to expand their dietary niche to include food sources that would
usually be treated as inferior. While
some species feed as specialists until resource limitations force them to
become generalists, many others, including marine iguanas, do not. The only consistent exception in marine
iguanas has been found in the population on Seymour Norte, where larger iguanas
are known to supplement their diets by eating a succulent plant, Batis maritima (Wikelski and Wrege
2000). Batis is not known to have significant nutritional value, and the
fact that only the larger iguanas eat the plant suggests that it simply helps
them to maintain their body size and the associated reproductive benefits. Because marine iguanas are so site-faithful
and because their digestive systems are specialized to digest algae, Batis eating behavior seems unlikely to
spread to other populations (Wikelski and Wrege 2000).
Response to Anthropogenic Stress:
Oil Spills, Tourism, and Invasive Species
In his 1990
article for the South American Explorer’s Club newsletter, Martin Wikelski
called introduced species the iguanas’ biggest threat. In what now seems like ironic foreshadowing,
he also stated, “The future of the marine iguana is unclear. Galápagos coastal waters are now part of a
national park and protected. (Hopefully
there will be no oil spills!)” (Wikelski 1990). Since Wikelski wrote his article almost 15 years ago, marine
iguanas have faced continuing anthropogenic pressures from introduced species,
the Jessica oil spill in 2001, and
the uncertain effects of tourism and a growing human presence on the
islands. Additionally, although we have
treated El Niño as a natural phenomenon, it is important to consider that
humans may increasingly be affecting the natural cycles of El Niño events by
contributing to global climate change, and therefore the “natural” pressures of
El Niño may be partially anthropogenic.
When
the oil tanker Jessica ran aground on
17 January 2001, the accident presented an unfortunate, but unique, opportunity
for scientists to study the effects of small-scale contamination on a species
whose stress-response had already been thoroughly documented before the
accident (Wikelski, et al. 2002).
Scientists collected blood samples from marine iguanas on Santa Fe, 32km
west of the spill, seven days after the incident. At the time, 70% of 170 individuals examined had oil residue on
their skin, and oil was still visible in tide pools. The blood samples showed elevated levels of corticosterone
similar to amounts found in individuals that died within 2-4 weeks of food
shortage during the 1994 El Nino, meaning that the iguanas were probably very
sensitive to the contamination (Wikelski, Romero, and Snell 2001).
Sure
enough, a census of the iguana populations on Santa Fe and Genovesa the year
after the Jessica accident showed a
62% mortality rate on Santa Fe, while the Genovesa population, untouched by the
oil, remained stable. The results of
the study clearly suggest that the spill had drastic effects, even though it
was small by comparison to others and produced only low-level contamination
(one liter of oil/meter of beach and only 44ppm of oil in the water) (Wikelski,
et al. 2002). Most likely, the
microsymbiont bacteria that live in the iguanas’ hindgut to aid in digestion
were poisoned by the oil, preventing digestion of food and causing the iguanas
to die of starvation (Wikelski, et al. 2002).
Though
many researchers have suggested that introduced species are the biggest threat
to marine iguanas, surprisingly few studies have focused on their effects. In the 1980s, Boersma (1983) noted that
there were few iguanas near the towns on Santa Cruz and San Cristobal, and
Laurie (1983) suggested that iguana populations on Santa Cruz and San Cristobal
were extremely unbalanced, largely due to introduced predators including dogs,
cats, rats, and pigs. He concluded that
“iguanas might only survive on offshore islets such as Crossmans, Brattle,
Plazas, and Coamaño (in Academy Bay), which at present have much healthier,
more balanced populations than on the adjacent mainland.”
Though
Laurie’s predictions have not come true—yet—the national park does acknowledge
that introduced predators are a big problem.
Juan Chavez, the national park director on Isabela, said that stray dogs
and cats on the island have clearly affected iguana populations close to town
by preying on eggs and juvenile iguanas, and even some adults. He added that the population of iguanas on
Tintorera, a small rocky islet just a short swim from Puerto Villamil, is much
more stable than the population on Isabela since there are no introduced
predators (Chavez, personal communication).
Surprisingly, given the obvious impact that introduced species have had
on iguana populations, we found few articles about their effects, suggesting
one area where future research could be helpful.
While
human-induced changes to the environment such as oil spills and the
introduction of species that prey on iguanas and their eggs clearly have a
negative impact on the health of marine iguana populations around the
Galapagos, the effects of human
presence where it has little direct impact—particularly on uninhabited islands
visited by tourists—is not as well understood.
Several of the same scientists who studied the iguanas’ reactions to the
Jessica spill used similar
techniques—analysis of glucocorticoid hormone levels—to examine iguanas’
responses to tourism. Human activities
have been shown to increase glucocorticoid levels to unhealthy levels in
studies of the effects of deforestation on spotted owls, heavy metal
contamination on trout, coal waste contamination on toads, (and, needless to
say, oil contamination on marine iguanas), but in the case of tourism, some
animals such as Magellanic penguins seem to become habituated to human presence
and don’t show the negative consequences of higher hormone levels (Romero and
Wikelski 2002). Because of the
importance of ecotourism to the Galapagos economy, it is important to establish
the effects of tourism not just on marine iguanas, but on all species.
Romero
and Wikelski’s 2002 study focused on two populations of iguanas on Fernandina
island, one living very close to the trail at Punto Espinoza and the other
living about two kilometers away. Since
iguanas are very site-faithful, any mixing of the populations was
unlikely. The researchers took blood
samples within three minutes of capturing iguanas at each site, then took a
second set of samples after 30 minutes of restraint-stress in an opaque cloth
bag. Initial levels of corticosterone
were similar between the two populations, and neither showed any sign of
chronic stress, based on a comparison with iguanas studied during the 1998 El
Niño (initial levels for iguanas in the 2002 study were half those from the 1998
study). Surprisingly though, the
iguanas from the tourist site showed lower
levels of corticosterone after 30 minutes of restraint than the iguanas from
the site far from tourist activity (significant to P < .05) (Romero and
Wikelski 2002).
Though
these results show that tourism is not causing chronic stress in the marine
iguanas, it is affecting corticosterone levels, which may or may not be
beneficial in the long run. The iguanas
seem to have become habituated to human presence (though the researchers are as
yet unsure about the mechanism), which seems to be a helpful adaptation since
high levels of corticosterone have been shown to cause a host of problems
leading to death. Still, occasional
short-term increases in corticosterone may be necessary for iguanas to survive
adverse conditions, and habituated iguanas may lose the ability to respond when
necessary (Romero and Wikelski 2002).
Additionally, tourism may cause a different kind of corticosterone
response than El Niño events or oil spills (studies in one species of baboon
suggests that more than one type of response is possible), and it could be that
the hormonal response to tourism in iguanas may be smaller but more prolonged,
meaning the overall amount of hormones released could actually still be greater
in iguanas exposed to tourism than in iguanas living further from tourist
sites. Since corticosterone levels were
only measured after 30 minutes in this study, more research is necessary to see
if this is the case (Romero and Wikelski 2002). Until then, it seems that we can be cautiously optimistic that
human presence alone does not have a negative impact on marine iguanas. Therefore, if we can prevent oil spills and
habitat destruction and if we can protect iguanas from introduced species (admittedly
two big “ifs”), it seems that people and iguanas can live in harmony in the
Galápagos.
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