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. The average burst assistance. We also observed adult animals velocities for adult marine iguanas are less feeding on macrophytic algae exposed at than 10% of the peak burst velocities of low tide; indeed, during the lowest tides fish of similar body length, including pred­ they did so almost to the exclusion of atory species (Walters and Fierstine, 1964; entering the water. Marine iguanas swim Webb, 1975; Wardle, 1975). Amblyrhyn­ with inflated lungs and their buoyancy chus are not uncommonly found in the eliminates any risk of drowning (Bartholo­ stomachs of sharks around the Galapagos mew et aI., 1976). Individuals may occa­ (Heller, 1903). These lizards with their sionally be carried from one island to 894 W. R. DAWSON ET AL. another in the Galapagos Archipelago by in a diving posture at the surface, making the swift currents prevailing there. How­ futile undulatory movements. ever, their relatively weak swimming ca­ Diving mammals and birds show a suite pacities would make any directed long of physiological specializations that pro­ distance movements between islands im­ long the time they can remain submerged probable. The variation in color apparent and facilitate recovery after diving. These among the populations inhabiting the dif­ adaptations include a high aerobic scope, ferent islands suggests a low level of gen­ large hematocrit and blood oxygen capac­ etic interchange among insular groups of ity, and high myoglobin concentrations in Amblyrhynchus. skeletal muscle. None of these factors in By mammalian or avian standards, the Amblyrhynchus departs significantly from capacities of marine iguanas for tolerating levels found in other iguanid lizards. Aer­ submergence are quite impressive. Natural obic scope is low (Fig. 2); hematocrit dives generally last 5-10 min and are rela­ values average 31.5% (±4.5 s.d.), a fig­ tively shallow (1.5-5 m) (Bartholomew ure characteristic of that reported for igua­ et al., 1976; G. Wellington, pers. comm.), nid lizards as a group (Dessauer, 1970; but these lizards sometimes descend to Bennett, 1973); and skeletal muscle tissue depths as great as 12 m and remain sub­ appears as white as fish hypaxial muscle, merged for as long as 30 min (Hobson, indicating very low myoglobin content. 1965, 1969). Darwin (1883) reported Even the bradycardia reported for Ambly­ that an animal tied underwater for an hour rhynchus during a dive (Bartholomew and was still alert when released. These ob­ Lasiewski, 1965) appears to be a response servations naturally led to the conclusion generally evident in terrestrial vertebrates that marine iguanas have unusual capac­ during submergence rather than a spe­ ities for remaining submerged. However, cialized adaptation. recent investigations have established that Evolution of Amblyrhynchus.-Our study lizards as a group are very tolerant of indicates that the mode of life of the anoxia: terrestrial iguanid lizards survive marine iguana has entailed surprisingly lit­ in an atmosphere of pure nitrogen for over tle departure from capacities for activity an hour (Belkin, 1963). This tolerance and locomotion characterizing terrestrial results from a combination of low meta­ iguanids. Aerobic scope and its thermal de­ bolic rates and high tolerance of lactic acid. pendence, reliance on anaerobiosis, and re­ Moreover the common iguana, Iguana stricted stamina evident in Amblyrhynchus iguana, which occasionally dives into are consistent with data obtained for other streams as an escape response, will volun­ iguanid lizards. Other functional charac­ tarily tolerate submergence for up to 4 teristics of marine iguanas previously hr (Moberly, 1968b). Evidently the div­ thought to be unique are now known to ing abilities of Amblyrhynchus do not sur­ resemble qualitatively those of terrestrial pass those of other iguanids. In fact, our iguanids, e.g., circulatory responses to div­ observations on marine iguanas indicate ing (Bartholomew and Lasiewski, 1965), that enforced dives of one hour are suf­ tolerance of submergence, nasal salt secret­ ficiently stressful to produce a pronounced ing glands (Schmidt-Nielsen and Fiinge, loss of locomotor coordination. We ob­ 1958; Dunson, 1969). We do not wish to served increases in concentrations of blood minimize the impressive osmoregulatory lactate averaging 137 mg% following such capacity manifested in the nasal gland of dives. Diving by marine iguanas requires Amblyrhynchus: it has the highest mass­ vigorous effort. Individuals approaching specific secretory rate established for rep­ exhaustion in our tests after 1-2 min of tilian salt glands (Dunson, 1969). How­ burst swimming could not develop the ever, this is a quantitative improvement thrust necessary to submerge and remained rather than a unique development among SPECIALIZATIONS OF MARINE IGUANA 895 iguanid lizards. It is the sole physiological prey in large sedentary concentrations in specialization thus far observed in this spe­ relatively exposed positions. cies. The partially webbed feet and lat­ Within the geographic range occupied by erally compressed tail specified as adapta­ members of the family Iguanidae, the com­ tions of marine iguanas for swimming and bination of physical and biological circum­ diving (Darwin, 1883) do not differ stances evident in the Galapagos appears greatly from those of Iguana iguana. These unique. Continental islands or mainland morphological features were not distinctive coasts are likely to have mammalian pred­ enough to merit special comment in the ators. Other tropical islands are likely to original description of Amblyrhynchus offer fewer food resources because coralline cristatus (Bell, 1825), which was made algae rather than softer-bodied forms uti­ without information on the behavior and lized by Amblyrhynchus predominate in the ecology of this species. warmer waters surrounding them (Car­ If the physiological grade represented by penter, 1966; W. R. Taylor, pers. comm.). the family Iguanidae is in a sense preadap­ Islands located at higher latitudes may of­ tive for the mode of existence followed by fer the food resources, but have cool tem­ Amblyrhynchus cristatus, why are there no peratures and few sunny days. In addition other marine iguanids? Any examination to these considerations, the Galapagos of this question requires definition of the Archipelago lies astride the equatorial cur­ major features of the particular environ­ rent. This location facilitates rafting from ment occupied by marine iguanas. As in tropical America, where the family Iguan­ the areas in which most large iguanids live, idae has its greatest radiation. Moreover, the terrestrial environment of Ambly­ most of the islands in this archipelago are rhynchus is relatively warm and equable. large enough to support a reasonably di­ The equatorial location of the Galapagos verse biota that would have made them Archipelago also ensures that strong inso­ hospitable to large iguanid immigrants. lation occurs throughout the year on the Immunological evidence (Higgins and leeward sides of the islands and at least Rand, 1974, 1975; Higgins et al., 1974), seasonally on the windward sides, impor­ suggests that the Galapagos marine iguana tant considerations for heliothermic lizards. and the Galapagos land iguana (Cono­ The cool waters surrounding the Galapagos tophus spp.) are more closely related to Islands, the upwelling occurring at many one another than either is to any mainland points off them, and the extensive rocky or iguana. These two insular forms probably lava substrates allow an abundant and di­ differentiated within the Archipelago from verse flora of soft-bodied macrophytic a common ancestor, presumably a terres­ algae of the types utilized by Ambly­ trial herbivore. This differentiation must rhynchus (Carpenter, 1966; Silva, 1966). have occurred in substantially less than the We should note here that the upwelling is several million to 10 million years regarded quite localized even within the Galapagos as the maximum age of the Archipelago Archipelago, with a corresponding concen­ (Cox, 1971), for the ancestral form could tration of marine iguanas on adjacent not have survived before the establishment shores. It is of interest that the social of a flora offering suitable food resources. organization of this lizard parallels that of In the case of Amblyrhynchus, the evolu­ sea lions and other otariids, which assemble tionary events leading from the ancestral in dense concentrations on shore. Until the form have resulted in a number of habits introduction of dogs, cats, pigs, and rats that have been interpreted as indicating a by man, the Galapagos Islands have been high degree of specialization for marine free of terrestrial mammalian predators, situations. However, aside from osmoreg­ which might abort any evolutionary experi­ ulation and, possibly, processing of food, ment involving the grouping of potential the major portion of these adaptations is 896 W. R. DAWSON ET AL. behavioral. These reflect the fact that the tative of a terrestrial line that was behavioral repertoire of marine iguanas preadapted for exploiting a unique com­ has evolved in a manner permitting recog­ bination of circumstances. nition and procurement of macrophytic algae as food and the establishment of a ACKNOWLEDGMENTS social order permitting the concentration We thank the Darwin Foundation for of large numbers of these lizards on shore permission to use the facilities of the Dar­ at points adjacent to locally abundant food win Biological Research Station and grate­ resources. That foraging by marine iguanas fully acknowledge the assistance and co­ is accomplished under conditions in which operation of the Director of the Station, temperature regulation is not feasible indi­ Dr. Craig McFarland, and the Manager, cates a further behavioral distinction be­ Mr. Rolf Sievers. Supported in part by tween these animals and other heliothermic NSF grants GB-25022, GB-32947X, and lizards. The acquisition of a semi-aquatic BMS-75-10100. Contribution number 214 habit has involved relatively little reor­ from the Darwin Biological Research ganization of conventional patterns of igua­ Station. nid physiology. With regard to metabolism and capacities for swimming and diving, LITERATURE CITED we feel justified in regarding the marine BARTHOLOMEW, G. A., AND R. C. LASIEWSKI. iguana as a member of a terrestrial line 1965. Heating and cooling rates, heart rate that was preadapted for exploiting a and simulated diving in the Galapagos marine iguana. Compo Biochem. Physiol. 16:573-582. unique combination of circumstances. BARTHOLOMEW, G. A., A. F. BENNETT, AND W. R. DAWSON. 1976. Swimming, diving, SUMMARY and lactate production of the marine iguana, Amblyrhynchus cristatus. Copeia 1976:709­ Contrary to earlier descriptions, the Ga­ 720. lapagos marine iguana is not a particularly BELKIN, D. A. 1963. Anoxia: Tolerance in fast swimmer, the mean velocity for burst reptiles. Science 139:492-493. BELL, T. 1825. On a new genus of Iguanidae swimming by large adults being only 0.85 Zool. J. 2:204-208. m/s, Moreover, this lizard depends on BENNETT, A. F. 1972. The effect of activity on physiological patterns characteristic of ter­ oxygen consumption, oxygen debt, and heart restrial iguanids in its amphibious exis­ rate in the lizards Varanus gouldii and Sou­ tence. Aerobic metabolic scope is rela­ romalus hispidus: J. comp, Physiol. 79:259­ 280. tively restricted and highly dependent --. 1973. Blood physiology and oxygen trans­ upon body temperature. This function port during activity in two lizards, Varanus reaches a maximum at 35 C, a value char­ gouldii and Sauromalus hispidus. Compo Bio­ acteristic of basking marine iguanas, but chem. Physiol. 46A:673-690. BENNETT, A. F., AND W. R. DAWSON. 1972. substantially higher than the water tem­ Aerobic and anaerobic metabolism during ac­ peratures at which the most strenuous ac­ tivity in the lizard Dipsosaurus dorsalis. J. tivities of this species occur. Its abilities comp, Physiol. 81:289-299. to forage in cool waters appear to depend --. 1976. Metabolism, p. 127-223. In C. Gans, and W. R. Dawson (eds.) , Biology of upon substantial anaerobic capacities, the Reptilia, Vol. 5 (Physiology A). Aca­ which resemble those of terrestrial iguan­ demic Press, New York. ids. As in these other lizards, anaerobic BENNETT, A. F., AND P. LICHT. 1972. Anaerobic metabolic scope appears relatively inde­ metabolism during activity in lizards. J. comp. PhysioI. 81:277-288. pendent of temperature in the marine BENNETT, A. F., W. R. DAWSON, AND G. A. iguana. Physiological results and a review BARTHOLOMEW. 1975. Effects of activity of the probable events leading to the evo­ and temperature on aerobic and anaerobic metabolism in the Galapagos marine iguana. lution of the Galagapos marine iguana sup­ J. comp, Physiol. 100:317-329. port a view of this animal as a represen- CARPENTER, C. C. 1966. The marine iguana of SPECIALIZATIONS OF MARINE IGUANA 897

the Galapagos Islands, its behavior and phys­ --. 1969. Remarks on aquatic habits of the iology. Proc. Calif. Acad. Sci. 34:329-376. Galapagos marine iguana, including submer­ Cox, A. 1971. Paleomagnetism of San Cristobal gence times, cleaning symbiosis, and the shark Island, Galapagos. Earth Planet Sci. Lett. 11: threat. Copeia 1969:401-402. 152-160. MOBERLY, W. R. 1968a. The metabolic re­ DARWIN, C. 1883. Journal of Researches. New sponses of the common iguana, Iguana iguana, Edition. Appleton, N.Y. to activity under restraint. Compo Biochem. DESSAUER, H. C. 1970. Blood chemistry of rep­ PhysioI. 27:1-20. tiles: Physiological and evolutionary aspects, --. 1968b. The metabolic responses of the p. 1-72. In C. Gans and T. S. Parsons (eds.) , common iguana, Iguana iguana, to walking Biology of tbe Reptilia, Vol. 3. Academic and diving. Compo Biochem. Physiol. 27: Press, New York. 21-32. DUNSON, W. A. 1969. Electrolyte excretion by POUGH, F. H. 1973. Lizard energetics and diet. the salt gland of the Galapagos marine iguana. Ecology 54:837-844. Am. J. Physiol. 216:995-1002. SCHMIDT-NIELSEN, K., AND R. FANGE. 1958. FRY, F. E. J. 1947. Effects of the environment Salt glands in marine reptiles. Nature 83: on animal activity. Pub. Onto Fish. Res. Lab. 783-785. No. 68. SILVA, P. C. 1966. Status of our knowledge of HELLER, E. 1903. Papers from the Hopkins the Galapagos benthic marine algal flora prior Stanford Galapagos Expedition, 1898-1899. to the Galapagos International Scientific Proj­ 14. Reptiles. Proc. Wash. Acad. Sci. 5:39-98. ect, p. 149-156. In R. 1. Bowman (ed.), The HIGGINS, P. J., AND C. S. RAND. 1974. A com­ Galapagos. University of California Press, parative immunochemical study of the serum Berkeley. proteins of several Galapagos iguanids. Compo Biochem. Physiol. 49A:347-355. WALTERS, V., AND H. L. FIERSTINE. 1964. --. 1975. Comparative immunology of Gala­ Measurements of swimming speeds of yellow­ pagos iguana hemoglobins. J. expo ZooI. 193: fin tuna and wahoo. Nature 202:208-209. 391-397. WARDLE, C. S. 1975. Limit of fish swimming HIGGINS, P. J., C. S. RAND, AND J. HAYNES. speed. Nature 255:725-727. 1974. Galapagos iguanas: Amblyrhynchus WEBB, P. W. 1975. Hydrodynamics and ener­ and Conolophus serum protein relationships. getics of fish propulsion. Bull. Fish. Res. Bd. J. expo Zool. 189:255-259. Canada 190. HOBSON, E. S. 1965. Observations on diving in WILSON, K. J. 1974. The relationship of oxygen Galapagos marine iguana, Amblyrhynchus supply for activity to body temperature in cristatus (Bell). Copeia 1965:249-250. four species of lizards. Copeia 1974:920-934.