El Nino and the Evolution of Flightlessness in the Galapagos Flightless Cormorant

The Galapagos islands provide many stunning examples of evolution due to their unique environment and their isolation from the mainland. A particularly interesting illustration of this peculiar island biology is the Galapagos Flightless Cormorant (C. Harrisi). This endemic coastal sea bird, while 1.8-2.2 times bigger than its close relative, C. Neglectus, has smaller wings, rendering this bird flightless (Livezey, 158). The evolution of flightlessness in the Galapagos Flightless Cormorant has been well explored; the usefulness of the adaptation of flightlessness is evident as is the genetic mechanism responsible for its morphological differences. However, the importance of El Nino – a long-occurring, and population-devastating event – has often been overlooked in explanations for C. Harrisi's morphological differences from other cormorants. First, this paper will give an overview of the useful adaptations and the genetic evolutionary mechanisms for these adaptations in the flightless cormorant; second, the effects and time-span of El Nino on the Galapagos Islands and the Flightless Cormorants will be discussed; and third, it will be shown that long term analysis of evolution in the flightless cormorant should include the effects of El Nino.

Flightless Cormants inhabit a small section of the Galapagos Islands on adjacent shores of Isabella and Fernandina. Throughout the Galapagos archipelago, and especially in this region, cold, arctic ocean currents converge with equatorial currents, causing an upwelling of nutrient rich waters. The bottom dwelling vertebrates and small octopi which form the basis of C. Harrisi's diet feed on the plankton and algae supported by these nutrients (Snow, 266). Because the Flightless Cormorant feeds on the ocean floor, a task different than that of plunge-diving or surface-skimming, it has adapted very differently from the flighted birds around it. The most important adaptations of the flightless cormorant are directly related to this food source and the environment present in the Galapagos.

The isolation of the Galapagos from a large landmass is key in the development of a flightless species of bird. Flight is a key instrument in avoidance of predation; in a setting where terrestrial predators abound, the better a bird can fly, the greater its chances of survival. For this reason, the existence of predatory mammals often precludes the evolution of flightlessness (McNab, 630). For the cormorant family, which is comprised of large, relatively slow-walking individuals, flight is the only means of escape and locomotion in continental areas. However, because the only routes of colonization of the islands are closed to most terrestrial and all large predatory mammals, selection pressures for flight are no longer so severe. The rocky, flat, easily accessible shorelines that the cormorants inhabit also make flight an unnecessary ability; a region with less accessible nesting sites might also preclude a species of flightless cormorants. With selection pressures for flight relaxed, more subtle advantages can be selected for. With an obviated need for flight, wings become too energy intensive to produce and maintain, and too awkward to carry while foraging underwater.

Flighted birds must develop and maintain large wings and strong muscles to be capable of flight. These processes both in youth and in adulthood require hard-earned calories that could go to a number of other uses. In Rails and in Steamer ducks, the mass of the pectorals, the principle flight muscle, is heavily correlated to the bird's metabolic rate. In general, less pectoral muscle mass means a lower metabolism than a large muscle mass in these two species (McNab, 636). In a resource poor environment, as often occurs in El Nino years, this slower metabolism often leads to a greater survival rate, as a bird can survive on fewer fish per day (McNab, 638-639). Cormorants have notoriously high metabolisms for sea birds, and they cannot fast for more than two or three days (Valle, 613). In this case, any slight metabolic advantage would be hugely advantageous for this sea bird. Flightless cormorants have a very low pectoral muscle mass, roughly 1.2% of their body weight, compared to their flighted relatives, which have muscle masses in the 11.3-11.5% range. This could indicate a lower basal metabolic rate in C. Harrisi (McNab, 637), and as a result, a better survival rate in the environment of the Galapagos. The adaptation of flightlessness could also have advantages for developing cormorants as well. Wing and bone structures are significantly different in the Flightless Cormorant than in close relatives (Livezey 200). These adaptations as well as less muscular development and different bone mass may lead to more productive energy expenditures in the juvenile Flightless Cormorant (Feduccia 258). In addition to the removal of an unnecessary appendage, the evolution of flightlessness also has had some positive, direct effects on the flightless cormorant's ability to hunt.

The flightless cormorant feeds primarily on the ocean floor, where it searches under rocks and in crevices for food (Snow 266). Evolution away from flight has allowed the reduction of wing size as well as changes in bone, muscle density and feather structure. These structural changes cause a decrease in buoyancy allowing for more time at the sea floor searching and catching prey. The hollow, air-filled wings, oil-coated, non-wetting feathers and the different muscular structures of flighted birds lead to a high buoyancy making it difficult for these birds to remain submerged for lengthy periods. The wings of the flightless cormorant are much smaller than those of related birds, greatly decreasing their buoyancy. C. Harrisi also has a unique feather structure; easily soaked outer feathers allow for decreased buoyancy, and close, hair-like, water-proof down helps maintain body heat in cold waters (Snow 267-8). (Fig A) Contractions in the enlarged abdominal muscles of the flightless cormorant also reduce buoyancy while diving (Fig B) (Livezey, 202). While flightlessness has had some specific morphological benefits on the hunting abilities of the cormorants, the simply larger body mass which is possible in flightless birds is also beneficial.

Body mass in the Flightless Cormorant has been positively correlated to longer and deeper dives which leads to a greater chance of finding and catching prey. Large males can remain submerged longer, and can also dive in deeper waters than females of smaller size (Livezey 206). The benefits of a larger body include an increased resistance to cold as well as a greater overall density. Larger Flightless Cormorants have an increased ratio of volume to surface area. Because a smaller percentage of their mass is on the surface of their bodies, and a larger mass contains more thermal energy than a smaller one, larger birds have an increased tolerance to cold (Livezey 208). This cold tolerance allows the birds to spend more time in the water moving and hunting. A greater overall body density also helps birds dive more deeply and stay submerged for longer periods of time. Because they can remain underwater for longer periods of time they have more time to search for and chase prey. While larger body size makes for better hunting, it also requires more calories to maintain, making the body sizes of the Flightless Cormorant closely tied to the food availability in the Galapagos. These adaptations are beneficial to C. Harrisi, and the process which produced them can be explained by genetic mechanisms of change.

Neoteny, the preservation of juvenile characteristics in adults, is a simple genetic mechanism that can explain these adaptations. The small wing size to body mass ratio, the undeveloped flight feathers (fig. A), as well as weak fusion and undifferentiation of tendons are all characteristics of young birds, and are present in C. Harrisi (Livezey, 206). Neoteny is also apparent in the comparison of wing to body size ratio through development. This size ratio is identical among flighted cormorants and the Flightless Cormorant in their earliest stages of development. Only later do the two ratios depart; juveniles in other cormorant species continue to increase their proportionate wing length, while Flightless Cormorants level off at the juvenile ratio (Livezey, 169). Gigantism, the increase in growth time and ultimately adult size, is another genetic mechanism that plays a role in the morphology of C. Harrisi, resulting in the Flightless Cormorant's large size (Livezey, 206). Both of these genetic mechanisms are simple processes, affecting only growth times and rates. This fits with the relatively short amount of time, roughly 3.5 million years, C. Harrisi has been evolving to the environment of the Galapagos. While these traits and adaptations seem to make sense in the standard environment of the Galapagos, the periodic and strong effects of El Nino need to be considered to give a full account of the evolution of flightlessness.

El Nino is an oceanic and atmospheric phenomena, that greatly affects water and air temperatures in the Galapagos and throughout the Pacific every 3-7 years (Ortlieb 183). El Nino causes a general warming of the waters in the Galapagos, reducing the nutrient-rich upwelling that the marine ecosystem depends upon. Algal growth is minimal, and fish populations are reduced as a result, limiting the food supply for predators, including the Flightless Cormorant (Ortlieb 181). El Nino is a periodic event that varies in strength each occurrence, and over periods of centuries and millennia. Evidence for large El Nino swings over the past 1000 years has been found in coral records (Fig C) (Cobb). Flood deposits, beach ridge sequences, and glacial core samples have also been utilized to map more ancient El Nino events (Ortlieb 181). These records indicate that very strong El Nino events have occurred roughly once every 400 years, for the past 4500 years. Modern thermal gradients have existed in the Pacific Ocean for the past 3.5 million years, suggesting that El Nino events could have been occurring as the Galapagos Islands were first being formed (Ortlieb 194). Given that El Nino has played a long-occurring, and ecosystem-affecting role in the Galapagos it is necessary to consider its effect on the flightless cormorant population and the implications of these effects in terms of the evolution of flightlessness.

While most El Nino events have little effect on the adult population of Flightless Cormorants, during major El Nino events there is a severe decrease in population size. In the 1983 El Nino the cormorant population dropped from 850 to 400 individuals (Valle 610), all chicks and juveniles were abandoned, and only a small, core population of adults survived . Because of the mating strategies of the Flightless Cormorant, the population rebounded back to its original number in less than a year, but the population base consisted of the small group of surviving individuals (Valle, 613). While no studies have been published detailing the morphological effects on the Flightless Cormorant population after this El Nino, the significance of this event is huge.

In such a small population of breeding individuals, especially when periodically reduced by El Nino, genetic drift and founders effect could play a significant role in the evolution of the species. These two evolutionary possibilities suggest that chance events can eliminate even the fittest animals in a population, and if that population is small, the traits of the weaker animals could be passed on through the generations. El Nino events severely reduce the population size of C. Harrisi, magnifying the effects of genetic drift, and they are also cyclical, creating a large time span for these effects to accumulate. Periodic population-decimating events have a large positive effect on a population's proclivity to genetic drift by reducing the amount of genetic diversity in that population (Franklin 138). However, it is difficult to prove that genetic drift has occurred and affected evolution as we can only see the end result. It is impossible to know how a more stable, larger population may have evolved. Also, the breeding population of 650 individuals during normal years is theoretically just larger than the threshold necessary to sustain a species with little genetic drift (Valle 612, Franklin 139). C. Harrisi's ancestors may have had more difficulty surviving El Nino years than current populations. If this is the case, ancient El Nino events would cause even greater drops in population size, leading to a greater chance of genetic drift. Also, if El Nino events occurred with great frequency in the past, this evolutionary process may again have been magnified. More research on El Nino needs to be done to see if this is a factor worth considering. A more direct contribution of El Nino to the evolution of flightlessness might be harsher selection pressures during event years.

The strength of selection pressures during El Nino years is terrific. During a strong El Nino year, nearly half the population dies off with the reduction of food supply. Those individuals with any metabolic, hunting or mass-related advantage will be just a little more likely to survive. The progeny of those surviving individuals, with their minute advantages, will replace the half that perished the year before. If there is strong selection for a particular trait during an El Nino year, when the population rebounds, the frequency of that trait in the population will greatly increase. It is even possible that this increase might set back adaptations making individuals more fit in normal years. From the previous discussion of El Nino's effects and adaptations of C. Harrisi, it can readily be seen that flightless individuals with slower metabolisms and denser, heavier mass bodies will better survive an El Nino than those that do not. There is one caveat to this line of reasoning: all of these adaptations help in non-El Nino years.

It is quite possible to conceive of flightlessness evolving in the normal environment of the Galapagos. The population would survive on a fixed amount of food, and those individuals better able to hunt would be stronger and more successful in rearing their progeny. Birds with the ability to reproduce more quickly could take advantage of minute fluctuations in population size, thereby explaining the rapid rebound of the cormorant populations after El Nino events. None of the adaptations present in the Flightless Cormorant population seem to require genetic drift to achieve; all could be reached through natural selection. It seems that all of the adaptations of the Flightless Cormorant could be explained in the context of a stable environment or could be discounted as byproducts of a neotenous evolution.

While this argument is strictly true, there are still some very compelling reasons to look at El Nino events. El Nino events do have a large effect on the population size and the genetic variability of the Flightless Cormorant. Such a periodic massive die-off must have cumulative effects on the genetic variability of the population as well as the rate of selection and traits selected for. For example, the very swift rebound of the cormorant population could be explained as above, or it could be an adaptation to large swings in the food supply caused by El Nino. Those birds which can reproduce most quickly will fill the population vacuum the next year with their progeny, leading to a great increase in the trait of opportunistically-breeding birds. Another example is that metabolic advantages seem much more important in times of scarcity. Birds with slower metabolisms will survive and be wildly successful in reproducing after an El Nino year, while in a normal year, a slower metabolism means simply having more energy to care for offspring in an already saturated population. While El Nino simply puts a different emphasis on the origin of C. Harrisi's adaptations, this viewpoint is a valuable one.

The Flightless Cormorant is very well suited for life on the Galapagos islands. Its seemingly improbable adaptations seem to suit it perfectly for normal conditions. However, the cyclical affects of El Nino and the fluctuations in food supply and climate that result are nearly as important as the normal conditions themselves. El Nino is an ancient, cyclical event that devastates the entire ecosystem on a recurring basis. For a species with a population as small and as easily reduced as C. Harrisi, this event must have an affect on the Flightless Cormorants evolution. It remains to be seen whether that effect is most prevalent in the rate of natural selection, the adaptations selected for, or the genetic drift of the population. However, while its direct relation is unclear, El Nino should be taken into account when discussing the evolution of flightlessness in the Galapagos Flightless Cormorant.

Bibliography

Barber, Richard T. and F. P. Chavez (1983) “Biological Consequences of El Nino.” Science v. 222, no 4629, p. 1203-1210.

Cobb, Kim M. (2003). “El Nino/Southern Oscillation and tropical Pacific climate during the last millennium.” Nature v. 424: pp. 271-276.

Feduccia, Alan. (1999) The Origin and Evolution of Birds 2^nd ed. New Haven: Yale University Press pp. 231-289.

Franklin, L.R. “Evolutionary Change in Small Populations.” Soule, M. E. and B.A. Wilcox (Ed.) Conservation Biology: An Evolutionary-Ecological Perspective. Sinauer Associates Inc., Sunderland, Massachusetts: 1980.

Glynn, Peter W. (1988). “El Nino-Southern Oscillation 1982-1983: Nearshore Population, Community and Ecosystem Responses.” Annual Review of Ecology and Systematics v. 19: pp. 309-345.

Livezey, Bradley C. “Flightlessness in the Galapagos cormorant (Compsohalieus [Nannopterum] harrisi): heterochrony, giantism and specialization.” Zoological Journal of the Linnean Society (1992) 105: 155-224.

McNab, Brian K. “Energy Conservation and the evolution of flightlessness in birds.” American Naturalist 1994 v. 144 no. 4 p. 628-642.

Ortlieb, Luc and Jose Machare (1993). “Former El Nino events: records from western South America.” Global and Planetary Change 7: p. 181-202.

Snow, B.K. (1966) “Observations on the Behavior and Ecology of the Flightless Cormorant.” Ibis 108: 265-280.

Valle, C. A. “Effective Population Size and Demography of the Rare Flightless Galapagos Cormorant.” Ecological Applications; 1995; v.5, no.3, p.601-617.

Fig. A

Livezey

Top: flight feather from a flighted bird; note the asymmetry and length.

Bottom: feather from the flightless cormorant note the symmetry and stubbiness

Fig B

(Livezey)

Cross-section of C. Harrisi on right, and a flighted cormorant on the left. Notice the enlarged abdominal muscle in red and the reduced pectoral muscle in blue in C. Harrisi.

Fig. C

Cobb

Ocean temperatures from coral data over the past 1000 years, note the fluctuations in temperature over time.