A REAPPRAISAL OF THE AQUATIC SPECIALIZATIONS OF THE GALAPAGOS MARINE IGUANA (AMBLYRHYNCHUS CRISTATUS) Wn.LIAM R. DAWSON, GEORGE A. BARTHOLOMEW, AND ALBERT F. BENNETT Division of Biological Sciences, The University of Michigan, Ann Arbor, Michigan 48109, Department of Biology, University of California, Los Angeles, California 90024, and School of Biological Sciences, University of California, Irvine, California 92717 Received May 21, 1976. Revised January 4, 1977 It is tautological to say that an organism from general iguanid physiological patterns is adapted to its environment. It is even in following its unique mode of life. The tautological to say that an organism is amount of work required to harvest its physiologically adapted to its environment. algal food is of particular interest. These However, just as in the case of many lizards must swim through the surf zone, morphological characters, it is unwarranted dive beneath the surface (lungs remain to conclude that all aspects of the physi­ inflated during diving so that the animals ology of an organism have evolved in must initially overcome their own buoy­ reference to a specific milieu. It is equally ancy), hold their breath during submerg­ gratuitous to assume that an organism will ence, surface, and then swim back to shore inevitably show physiological specializa­ through the surf (Bartholomew et al., tions in its adaptation to a particular set 1976). The exertion associated with this of conditions. All that can be concluded underwater grazing must surpass the for­ is that the functional capacities of an aging of any other large iguanid, all of organism are sufficient to have allowed which are primarily herbivorous (Pough, persistence within its environment. On 1973). The coolwater temperatures around one hand, the history of an evolutionary the Galapagos Archipelago (15-25 C) po­ line may place serious constraints upon tentially hinder development of the in­ the types of further physiological changes tensity of activity required during feeding. that are readily feasible. Some changes All large iguanids so far investigated, in­ might require excessive restructuring of cluding Amblyrhynchus, bask in the sun the genome or might involve maladaptive and reach body temperatures in the vicin­ changes in related functions. On the other ity of 35 C. Activity in terrestrial iguanids hand, a taxon which is successful in occu­ characteristically occurs at these higher pying a variety of environments may be body temperatures, and the Van't Hoff less impressive in individual physiological effect would predict greatly depressed rates capacities than one with a far more limited of functional processes at these lower distribution. temperatures. A case in point concerns the functional Since physiological investigations have capacities of the Galapagos marine iguana revealed that iguanids possess very little (Amblyrhynchus cristatus) , representing stamina, the locomotor performance re­ the large and diverse family Iguanidae quired during activity is of particular in­ that is easily the major saurian group in terest. Other iguanids that have been in­ the Western Hemisphere. Amblyrhynchus, vestigated can sustain vigorous activity however, is unique not only among the for only a minute or two and this activity iguanids but among all lizards in feeding is accomplished almost exclusively through exclusively on intertidal and subtidal ma­ anaerobic metabolism involving the pro­ rine products, predominantly soft-bodied duction of lactic acid, rather than through macrophytic algae. It is of interest to ask greatly augmented aerobic metabolism how far the marine iguana has departed (Moberly, 1968a; Bennett, 1972; Bennett EVOLUTION 31:891-897. December 1977 891 892 W. R. DAWSON ET AL. first two minutes of stimulation, nearly AO V02 2- Smin· _ - - - - - - --J O.8 half of the total response occurring within the first half-minute (Fig. 1). Below 35 C, maximal rates of oxygen consumption do 30 Amblyrhynchus 0.6_ J: not develop until after activity has been +Activity C. ?: completed. The aerobic work capacity of O.A "M{l an animal is generally represented by its i 2°F----l--_+V02 0-2min a ... .;> aerobic scope (Fry, 1947), the difference at any single body temperature between 10 0.2 standard and maximal rates of oxygen consumption. The maximal aerobic scope 2 3 A for Amblyrhynchus (Fig. 2), 0.71 cc O2 / min (g X h), resembles values reported for FIG. 1. Time course of activity (left hand other iguanid lizards (Bennett and Daw­ ordinate), as indicated by movements of the son, 1976). left hind leg, and oxygen consumption (right Anaerobic metabolism overshadows aero­ hand ordinate) of marine iguanas during a 5-min bic metabolism during activity by marine period of electrical stimulation. The results are iguanas. Average values of blood lactate averaged for 6 animals (mean body mass, 489 g) a~ 30 C. The levels of oxygen consumption after activity range between 105 and 140 (V02) indicated by the horizontal bars represent mg%. This range is identical to that re­ the average values for the 0-to-2- and 2-to-5-min ported for the iguanid lizards Iguana intervals of the stimulation period, respectively. iguana (Moberly, 1968a) and Sauromalus hispidus (Bennett, 1973) and is character­ istic of physically exhausted reptiles (Ben­ and Dawson, 1972; Bennett and Licht, nett and Dawson, 1976). Anaerobic me­ 1972). We decided that it was worthwhile tabolism provides 70-90% of the total ATP determining whether the marine iguana has gen~rati?n during a burst of activity in the evolved special physiological capacities to manne Iguana and accounts for over 97% deal with its demanding activity regime. of the carbohydrate utilization (Bennett In this investigation we have addressed et al., 1975). This metabolic situation and several questions. Does Amblyrhynchus the magnitude of oxygen consumption and possess greater aerobic and/or anaerobic lactate buildup in Amblyrhynchus are in­ capacities than other lizards? Are marine distinguishable from those characterizing iguanas particularly good swimmers or terrestrial iguanids. Neither aerobic nor divers? Do these animals show physio­ anaerobic capacities have been expanded logical specializations permitting them to in the adaptation to the marine habitat. cope with the low body temperatures that Maximization of aerobic scope near pre­ appear to be incurred during feeding? Our ferred body temperature is a common fea­ observations, some of which are reported ture of saurian metabolism (Wilson, 1974), elsewhere (Bennett etaI., 1975; Bartholo­ but one that seems inappropriate for Am­ mew et al., 1976), allow us to deal with blyrh!n~hus. Nevertheless, aerobic scope the above questions in an evolutionary of this lizard peaks at basking body tem­ context. perature (ca. 35 C) rather than at some­ Activity metabolism.-Resting Ambly­ what lower temperatures (Fig. 2), at which rhynchus were stimulated to maximal ex­ most of the strenuous work of the animal ercise for five minutes and oxygen con­ sumption, lactate production, and gross is probably conducted as it forages in cool activity output were determined (see Ben­ water. Vascular mechanisms serving to nett et al., 1975, for detailed procedures). delay cooling have been found in several Marine iguanas fatigue rapidly; virtually terrestrial lizards and are particularly well all escape behavior takes place during the developed in marine iguanas (Bartholomew SPECIALIZATIONS OF MARINE IGUANA 893 and Lasiewski, 1965). However, the time spent in the water by Amblyrhynchus ap­ 0.8 pears to guarantee substantial cooling dur­ -.::­ ing foraging. It is thus important that .s: this animal can achieve vigorous activity Ol at body temperatures well below 35 C ",0.6 (aerobic scope is maximal at 35 C), as a o M byproduct of primary reliance on anaero­ E biosis. The anaerobic component of activ­ u ity metabolism is not only large but is also & 0.4 o nearly temperature independent (Ql0 = u 1.2). Low thermal dependence of anaero­ V) .~ bic function is characteristic of iguanids ~ 0.2 Amblyrhynchus generally (Moberly, 1968a; Bennett and Licht, 1972) and appears preadaptive for ~ operation of marine iguanas at the lower body temperatures developing in the aquatic portion of their habitat. o 25 40 Swimming and diving ability.-Darwin (1883) observed that marine iguanas show "perfect ease and quickness of swimming," FIG. 2. The relation of aerobic scope of ma­ but our observations (Bartholomew et al. rine iguanas (mean body mass, 489 g) to body temperature (Ts). Values for aerobic scope are 1976) indicate that they swim rathe: calculated from Bennett et al. (1975) and this slowly and have little stamina. When reference should be consulted for details of pro­ released in the water, they attempted to cedure. escape from us by bursts of swimming lasting less than 2 min. The fastest adult weak swimming abilities would appear to marine iguana we observed (snout-vent be easy prey for such predators. length, 55 cm; total length, 106.5 em) Only the larger marine iguanas are suf­ s,,:,am at 0.85 m/sec (47.9 body lengths/ ficiently powerful to swim through break­ mm), and the mean velocity for burst ing waves. Even the largest animals may swimming by five adults (mean snout-vent have difficulty returning to shore through length, 43.2 cm; mean total length, 97.0 heavy surf. The hatchlings forage exclu­ c~) was 0.74 m/sec (46 body lengths/ sively on the rocks exposed at low tide mm). Following the brief period of burst not entermg. the water voluntarily. Hatch-' swimming, adult marine iguanas cruised at lings that we placed in the water beyond velocities averaging only 0.45 m/sec (28 the surf invariably swam immediately to­ body lengths/min). Thus peak burst ve­ ward shore and often became exhausted locities are only about twice cruise veloci­ in the surf. They reached shore only by ties, a situation equivalent to a terrestrial floating in on a favorable wave, their own herbivore being able to run only twice as locomotion being insufficient without such fast as it can walk.