Saturday, November 28, 2009

The Incredible Size Variation of the Marine Iguana

No marine iguana (Amblyrhynchus cristatus) article would be complete without Charles Darwin's famous defamations against the reptiles, calling them "hideous", "disgusting clumsy Lizards", "imps of darkness"*, "stupid", and so forth (see his Journal of Researches). Despite these harsh sentiments, Darwin did not disown the reptiles during his visit, but made lasting observations on their biology. The laterally flattened tail and webbed feet are adaptations for a semi-aquatic habitat, one specimen demonstrated that the iguanas could survive being submerged for at least an hour; the strong claws of equal length are "admirably adapted" for grasping on to rocks**; instead of consuming fish (as some suspected earlier), the enlarged intestines and stomach contents suggested a diet wholly composed of marine algae; Darwin also suspected that they lacked land predators*** by repeatedly throwing an individual into a pool, only for it to continuously return to land! In The Voyage of the Beagle he observed that the iguana population at Albemarle Island was significantly larger than those on other islands; this remarkable variation is occasionally mentioned in marine iguana publications, but its significance is rarely discussed - hence this post.

* For some reason, the quote is rendered "I call them 'imps of darkness'..." or "someone calls..." in different publications.
** Darwin observed this function on the coast, but he apparently did not consider its function in marine browsing. It also seems unusual that he did not observe specimens consuming algae exposed by a low tide.
*** Galapagos Hawks have been known to hunt iguanas in groups and can take adult females (on Santa Fe the iguanas have compensated by using mockingbirds as sentinels); Great Blue Herons are major predators of hatchlings (Romero and Wikelski 2009). However, some island populations of marine iguanas are virtually not subjected to predation (see below). These days feral cats and dogs are causing trouble since marine iguanas have no way of recognizing these terrestrial predators as a threat (Romero and Wikelski 2009). 

"Hideous?" I'd think "ruggedly handsome" would be a more apt description. Darwin described the iguanas as being "dirty black" (being dark aids in their thermoregulation), but as seen in this and other specimens, their coloration is actually highly variable. Also, what's with so many 19th century naturalists talking about reptiles in such disparaging terms?
Photo taken (and modified) from the Wikipedia Commons.

Before we get to the issue of size, some more background on the marine iguana is in order. Darwin considered the Galapagos land iguanas to be a second species within Amblyrhynchus; the land iguanas are now considered to be three species within Conolophus but molecular evidence has confirmed that they form the sister clade to the marine iguana (Gentile et al. 2009, Wiens and Hollingsworth 2000). Interestingly, the Galapagos iguanas appear to have diverged less than 10 million years ago, before the origin of the modern islands and implying that they inhabited other, now-submerged, islands in the vicinity (Rassmann et al. 1997). The (Amblyrhynchus + Conolophus) clade was formerly assumed to be related to chuckwallas (possibly due to long branch attraction and convergence), but now it is thought that they form a clade with spinytail iguanas - all of these clades occur around the central part of the Americas. (Wiens and Hollingsworth 2000). The MarineBio website has a fine summary of marine iguana biology - although their size figure could stand to use some revision.

A marine iguana goes for a swim - they locomote with their tails and hold their appendages flat against their body. Taken and modified from the Wikipedia Commons.

Wikipedia correctly mentions that the smallest iguanas are from Genovesa and the largest are from Fernandina and Isabela, although bizarrely the next paragraph simply states that males are 1.3 m long, females are 0.6 m in length, and the males weigh up to 1.5 kg (~3.3 lbs). Darwin's Journal of Researches mentions that specimens can reach 4 feet (1.2 m) in length and he gives a weight of 20 pounds (9 kg) for one large specimen. Romero and Wikelski (2009) comment that the Genovesa males are typically only 0.5 kg (~1 pound - about 0.9 kg/2 lbs max) in weight while the largest on Isabela can be over 10 kg. A photograph published by the authors (which I probably can't reproduce) shows an enormous 12 kg (26 pound) male with a very light coloration and huge amounts of tissue associated with the dorsal crest. I'm baffled as to how most popular sources have a maximum mass which is off by a factor of 8 - fortunately peer-reviewed sources do not make this mistake!

Size is a fundamental characteristic for organisms as it influences their morphology, physiology, behavior, and life history (Wikelski 2005). However, there are numerous and often interrelated factors which influence body size, so it is difficult to determine how the trait evolved - fortunately for me, Wikelski (2005) is a review paper on this subject for marine iguanas. The evolution of body size appears to have occurred rapidly in different marine iguana populations; Rassmann et al. (1997) determined through mitochondrial DNA that the iguanas on Fernandina and Genovesa form a "northern clade" (i.e., in the northern islands of the archipelago) despite their body sizes at the opposite end of the spectrum. Selective pressure through predation can be a very strong force, but since some marine iguana populations have virtually no predation and males are subjected to negligible predation on every island, this factor can effectively be ruled out (Wikelski 2005). Like the case for most organisms, there is a correlation between the size of the landmass and that of the organism (the larger Galapagos islands are also subjected to increased upwelling), however body size has historically increased on every island, apparently due to increasing temperatures (Wikelski 2005). While large males would seem to have a lot going for them - they have thermal inertia (useful for diving deeper than competitors), an increased ability to cling to rocks, and sexual preference from females (due to their ability to establish display areas) - during El Nino years the upwelling stops and while the iguanas can shrink (in body length, not just mass) to ameliorate the famine conditions, females have a 70-80% survival rate and large males have a survival rate of a mere 20-50% (Wikelski 2005).

Wikelski (2005) concluded that the most important influences on male marine iguana body size are sexual selection for larger size from females and natural selection. The natural selection is not limited to the famine conditions caused by the El Nino phenomenon, but also temperature variation and the amount of biomass. While large iguanas have more thermal inertia, they heat up more slowly which limits their ability to dive and digest; the amount of algae biomass does indeed appear to be influenced by the size of islands (Wikelski 2005). Wikelski (2005) theorized that the reason for large size, not just in iguanas but possibly many animals, is due to sexual selection which is of course countered by natural pressures mostly relating to the supply (and for some animals, physical size) of the food source. As for why sexual dimorphism occurs, this may be related to the resources females need to allocate towards reproducing - quantitative tests of this idea, however, have yet to be carried out (Wikelski 2005).

In the four years since Wikelski (2005), it does not appear that anyone has further elaborated upon the mechanisms controlling marine iguana body size. For those writing or revising articles on the species, please cease from implying that marine iguanas are homogeneous in size and at least mention the incredible variation!

A pretty good video from the BBC. As Wikelski (2005) speculates, when the iguanas first arrived on the Galapagos there would have been very limited food on land, forcing them to forage for intertidal algae. The North Seymour population supplements their diet with land plants, so presumably the land iguana species is derived from a marine population which specialized even further.


Gentile, Gabriele, et al. (2009). An overlooked pink species of land iguana in the Galápagos. PNAS 106, 507-511. Available.

Rassmann, K., et al. (1997). The microevolution of the Galápagos marine iguana Amblyrhynchus cristatus assessed by nuclear and mitochondrial genetic analyses. Mol. Ecol. 6, 437–452.

Romero, L. Michael and Wikelski, Martin. Marine Iguanas, Life on the Edge. IN: Galápagos, Preserving Darwin's Legacy. Edited by Roy, Tui De. Firefly Books, 2009.

Wiens, John J., and Hollingsworth, Bradford D. 2000. War of the Iguanas: Conflicting Molecular and Morphological Phylogenies and Long-Branch Attraction in Iguanid Lizards. Syst. Biol. 49, 143–159. Available.

Wikelski, Martin. 2005. Evolution of body size in Galapagos marine iguanas. Proc. R. Soc. B. 272, 1985-1993. Available.

Thursday, November 19, 2009

The Benefits Of Having Stuff Grow All Over You

One would think that epibiotic growth, that is, commensal organisms attached to a living surface, would be neutral at best and a hindrance to locomotion at worst* for the basibiont, the substrate organism. 'Fouling' by epibiotic growth is a virtually omnipresent pressure in aquatic environments, so basibionts variably avoid, defend against, or tolerate epibiotic growth (Wahl 1989). Since there are potential examples beyond count, given the tendencies of this blog I'll focus on some recently described examples of tolerance from big vertebrates.

* Potential disadvantages for the basibionts includes increase in weight, decrease in flexibility, increase in friction, damage from anchoring, damage due to grazers preying on epibionts, and so forth (Wahl 1989 - citing various).

The loricariid catfish Pterygoplichthys (possibly P. disjunctivus and hybrids) was accidentally introduced to Florida and has been observed interacting with manatees while both species were present near springs during the winter, avoiding unsuitably low temperatures (Nico et al. 2009). The interaction is that the catfish graze upon the grazers:

A mother and calf with 16 loricariids. Note that manatees are typically covered in epibiotic growth. The authors recorded another instance of over 40 catfish on one individual, almost obscuring it from view. Photograph by James P. Reid, taken from Nico et al. (2009).

The heavy covering of epibionts on manatees indicates tolerance and implies either a neutral impact or a beneficial one. Nico et al. (2009) speculate that while the epibiont layer probably does not provide notable protection against UV radiation (as manatee skin is very thick), it could play a role in heat absorption. Manatee behavior towards the armored catfish is contradictory; while some individuals ignore them (Fig. 1) even if as many as 40 catfish are involved, others apparently avoid congregations of catfish and others still are irritated by the fish and attempt to dislodge them (Nico et al. 2009). Since the interaction is so recent, perhaps it is possible that manatees have not learned or evolved a standardized response. Manatees generally ignore other fish including remora species that feed on their fecal matter and bluegills that apparently feed on epibionts (Williams et al. 2003, Powell 1984); however they are not tolerant of a porgy species which occasionally nips at them (Nico et al. 2009 - citing pers. com.). The grazing on manatees could be beneficial for the removal of parasites and removal of diseased and damaged tissue, although it also carries the risk of disease transmission (Nico et al. 2009). This is a surprisingly complicated situation and clearly the role of epibionts needs to be further investigated, as do the risks and benefits of allowing fish to graze. Nico et al. (2009) speculate that manatees that avoid loricariids may move to colder water, where they expend more energy than normal attempting to maintain body heat.

The interaction between cetaceans and their epibionts seems to be less obscure than the manatee situation. In dealing with Orcinus orca predation, mysticetes have adopted fight or flight countermeasures; the Balaenoptera species are fliers while the right whales (Eubalaena spp.), bowhead whale (Balaena mysticetus), humpback whale (Megaptera novaeangliae) and grey whale (Eschrichtius robustus) are fighters (Ford and Reeves 2008). Although the number of documented cases of orcas killing mysticetes are few, the rate of scarring suggests that predation attempts are significant, likely for juveniles (Ford and Reeves 2008). The ability to sprint at considerable speeds in the Balaenoptera species seems to be a direct evolutionary response to predation, but the fight species may have evolved to be slow and maneuverable primarily because of their ecological niches (Ford and Reeves 2008). Possibly mirroring the evolution of horns in some bovids, the offensive structures in right whales and humpback whales are used both for intraspecific male combat and interspecific defense and it is not clear for what purpose they originally evolved (Ford and Reeves 2008). Although right whales and humpback whale will swing or lunge with their heads, flippers and flukes are the primary means of defense for these species; gray whales roll on their backs to protect their vulnerable ventrum (Ford and Reeves 2008).

Right whales have hardened patches of skin known as callosities on the dorsal, lateral, and ventral surfaces of the head. These callosities host thousands of amphipods, epibionts with no obvious beneficial function for the whales - apparently the cornified epidermal tissue provides their ideal habitat and harboring the arthropod is a side effect for possessing the morphology. Southern right whales, however, possess barnacles which probably do have a function in making the callosities more formidable.

The Southern Right Whale has callosities with both amphipods and barnacles. From here. Has anyone every suggested that right whales may be responsible for sightings of 'marine saurians'?

Humpback whales lack callosities, but they have analogous barnacles which fulfill the same function - and provide an unambiguous example of a positive epibiotic interaction. Humpbacks can have up to 450 kg of large barnacles ( up to a 5 cm diameter) concentrated on the head, leading edge of their flippers, tips of the tail flukes, throat pleats, and near the genital slit (Ford and Reeves 2008 - citing Clark 1966, Slijper 1962). While intraspecific purposes are also likely, it is probably no coincidence that humpback whales defend against orcas using their head, flippers, and flukes (Ford and Reeves 2008). It seems like the throat and genital regions would be particularly susceptible to either biting or ramming attacks, further suggesting the defensive function of the barnacles.

Grey whales have often continuous encrustations of barnacles on the dorsal portions of their rostrum, anterior portion of their backs as well as their flippers, fluke, and elsewhere (Ford and Reeves citing Rice and Wolman 1971). Considering the defensive behavior of the whales, once again it appears that the barnacle placement is no coincidence. Exactly how these whales attract barnacles to particular portions of their body certainly is a good question; how do the callosities of some right whales have barnacles and others don't?

Epibiosis certainly doesn't end with heat balance (maybe) and creating weapons, Wahl (1989) notes that other potential benefits for the basibiont include a supply of vitamins and/or nitrogen compounds, water retention during low tide, camouflage, mask chemical cues, and drag reduction (!) - thanks to hydrophobic bacteria on skin. There are of course many, many potential disadvantages as well.


Ford, John K. B.; Reeves, Randall R. 2008. Fight or flight: antipredator strategies of baleen whales. Mammal Rev. 38(1), 50–86.

Nico, Leo G; Loftus, William F.; Reid, James P. 2009. Interactions between non-native armored suckermouth catfish (Loricariidae: Pterygoplichthys) and native Florida manatee (Trichechus manatus latirostris) in artesian springs. Aquatic Invasions 4(3), 511-519. Available.

Powell, J. A. 1984. Observations of cleaning behavior in the bluegill (Lepomis macrochirus), a centrarchid. Copeia 1984, 996-998.

Wahl, Martin. 1989. Marine epibiosis. I. Fouling and antifouling: some basic aspects. Mar. Ecol. Prog. Ser. 58, 175-189. Available.

Williams, E. H. Jr.; Mignucci-Giannoni, A. A.; Bunkley-Williams, L.; Bonde, R. K.; Self-Sullivan, C.; Preen, A.; Cockcroft, V. G. 2003. Echeneid-sirenian associations, withinformation on sharksucker diet. Journal of Fish Biology 63(5), 1176-1183. Available.