by Dr. Susan M. Kain
Many animals living in the gypsum dunes at White Sands National Monument match the white sands on which they live. Animals reported to be lighter-colored in the dunes than in non-dune populations include insects, spiders, scorpions, lizards, mammals, and even toads (see Table 1). These white animals raise several questions. Why, for example, did white animals evolve in the dune field? Why are some dune-field animals white and others not? How do the animals become white? Much research is still necessary to fully answer these questions, but our current understanding of these issues is summarized below.
Why did light coloration evolve?
Animals become better adapted to their environment by a process called natural selection, in which traits that increase an individual’s reproductive success by improving its fit to the environment will tend to spread in the population. Light coloration could evolve through natural selection in dune field animals if individuals with light-coloration genes reproduced more than individuals with dark-coloration genes. Consider the case of a brownish female lizard moving from the brownish desert into the white dunes. If she has babies, those babies are likely to have slightly different skin colors, just like human siblings have slightly different skin and hair colors. The lighter-colored babies would blend in better with the white sand and therefore be less likely to end up as lunch for a roadrunner or another predator. Because the light-colored individuals would be more likely to survive to reproduce, more light-coloration and fewer dark-coloration genes would be passed on to the next generation. After many generations of selection for lighter individuals, the population could eventually become white.
The scenario presented above suggests one reason why lighter-colored individuals may be more likely to survive and reproduce than darker-colored individuals: they may be better camouflaged (Benson, 1933). Alternatively, lighter-colored individuals that are active during the day may be better able to regulate body temperature because they reflect more of the intense desert sunlight (Benson, 1933). No one has tested these hypotheses for the white animals at White Sands. However, three lines of circumstantial evidence do
suggest that lighter coloration usually functions as camouflage rather than functioning in temperature regulation. First, many of the white animals are nocturnal, so regulating absorption of the sun's rays would not be an important selective factor.
Second, several of the species that are lighter than usual at White Sands are darker than usual (or have closely related species that are darker than usual) at the Valley of Fires lava flow at the north end of the Tularosa Basin (Table 1). You would expect to find dark animals on the black malpais and light animals on the white sands if the color serves as camouflage. In contrast, given that the climate and amount of sunlight are similar throughout the Basin, you would not expect to find light coloration in one area of the Tularosa Basin and dark coloration in another if the coloration served only in regulating temperature (Benson, 1933).
Finally, evidence from species in other habitats suggests that, in general, "background color-matching of animals seems clearly to be developed through natural selection influenced by predator pressure" (Norris and Lowe, 1964, p. 569). Many researchers have shown that camouflaged animals are less likely than animals that are not camouflaged to be taken by predators. Even nocturnal animals can benefit from matching their habitat, presumably because nocturnal predators use vision to find prey illuminated by moonlight or starlight (Dice and Blossom, 1937 cited in Norris and Lowe, 1964). Experimental tests will be necessary to confirm that lighter coloration provides camouflage for species at White Sands, and to determine whether it also influences temperature regulation.
Given the presence of so many species that are white in the dune field but not in the surrounding desert, it seems clear that conditions in the dunes select for different adaptations than do conditions in surrounding habitats. The dune field can be considered a sand island in a sea of desert. Just as oceanic islands often have unusual species that are not found elsewhere, islands of habitat like the White Sands dune field can also have species not found elsewhere. Species that are restricted geographically to one or a few localities are called endemic species (Anonymous, 1996; Hale and Margham, 1991; Hine, 1999). Endemic species evolve when populations living in islands of habitat are reproductively isolated from other populations of the same species for a sufficiently long period of time. No species, but six subspecies (Table 1), are restricted to the dune field and therefore could be considered endemic. The number of endemic subspecies or species depends, of course, on how species and subspecies are defined. Because most of the taxonomic work on dune-field animals was done many years ago, application of modern taxonomic techniques, including DNA or protein analysis, could help to clarify the status of endemic species and subspecies at White Sands.
Why are most dune-field animals not white?
Although some dune-field animals are lighter colored than individuals in other populations of the same species, most animals that live in the dunes are not unusually colored. Among insects, for example, Stroud (1950) notes that "the absence of adaptation to the soil color is more striking than its presence." He collected 343 insect species at eight different collecting sites within the dunes, and only four of those species were lighter colored than expected (Table 1). Similarly, Blair (1943) trapped twenty-three different species of mammals in the dunes, and only three were lighter colored than expected (Table 1). The absence of light coloration in most species raises the question of why light coloration has not evolved more often. There are many hypotheses to explain these differences. More research is necessary to determine the relative importance of these factors in influencing the evolution of light coloration in dune-field animals.
The first hypothesis to explain why light coloration is relatively rare in the dunes is that in species without light coloration there was simply no genetic variation for color upon which natural selection could act. Natural selection can only produce a better fit between an organism and its environment if a beneficial trait is genetically transmitted to offspring. For example, if animals became camouflaged to the dunes by rolling in the sand and having sand grains adhere to their fur or skin, the offspring of lighter-colored individuals would not necessarily also be lighter-colored, so
It is also possible that lighter color may not evolve even when there is genetic variation for color (Norris, 1964). This general hypothesis could apply in a number of different contexts. First, lighter color would be slower to evolve in species where the benefit of being light-colored is relatively low (i.e., the intensity of selection is low). For example, large nocturnal predators like badgers and kit fox may benefit less from being camouflaged to the white sands than would a small mouse or lizard, because the larger predators have few visually-hunting predators of their own. Note, though, that it is possible that predators would be better able to sneak up on unwary prey if they, too, blended in with the habitat. Consider, for example, the well-camouflaged the polar bear.
Second, lighter color may be slower to evolve in species in which light coloration yields some benefits and dark coloration yields others (i.e., there are opposing selective pressures). For example, darker "cold-blooded" animals like lizards and insects can absorb heat more quickly than lighter-colored animals and therefore reach their activity temperature more quickly. Selection for being dark may therefore oppose selection for light camouflage coloration in the dunes.
Some lizards in the dunes can change color with the temperature. Bleached earless lizards (Bundy, 1955) and Cowles prairie lizards (Lowe and Norris, 1956) are darker-colored when they are cold, presumably because dark sun absorbs heat more quickly, and then gradually get lighter as their temperature increases. However, dune field lizards never get as dark as more normally-colored lizards from outside of the dunes (Bundy, 1955), so camouflage coloration still probably reduces possible temperature-regulation benefits from darker coloration. Thus, camouflage coloration may not have evolved in some reptiles, insects, and other cold-blooded animals if the benefits of dark coloration facilitating temperature regulation outweigh the benefits of camouflage.
Third, lighter color may be slower to evolve in species that spend less time moving around on the open sands and therefore benefit less from being camouflaged to the sands. For example, the bleached earless lizard (H. m. ruthveni) forages in the open on the sand, while the Cowles prairie lizard (Sceloporus undulatus cowlesi) forages primarily in darker vegetation. Because of these differences in foraging ecology, the Cowles prairie lizard probably benefits less from being camouflaged to the white sands of the open dunes. This may help explain why the bleached earless lizard is much lighter-colored than is the Cowles prairie lizard (Dixon, 1967).
Fourth, light coloration may not have evolved in some species because they have other means of defending against predators and do not need camouflage. For example, the black darkling beetle makes itself obvious as it marches across the white sands in the middle of the day, so it seems surprising that it has not adopted white camouflage coloration. However, its common name, the stinkbug, hints at why it does not need to be camouflaged. If they are threatened, these beetles stand on their heads and, if the threat continues, spray smelly chemicals that make them an unappealing meal for predators. Some other species that do not have camouflage coloration may also have other kinds of defenses that protect them against predators and make camouflage unnecessary.
Finally, even in species where light coloration is beneficial, it will be less likely to evolve in species where individuals regularly disperse between different habitats (i.e., there is gene flow between populations). When there is dispersal between populations under different selective pressures, genes favored in one habitat (e.g., light coloration genes in the dune field) will be selected against in the other habitat (e.g., in the desert surrounding the dunes). Such gene flow reduces the chance that individuals in either population become adapted to their environment.
The extent of gene flow between dunes and non-dunes populations does seem to predict the extent of camouflage coloration in some lizards, mammals, and insects. The dunes population of the bleached earless lizard (H. maculata ruthveni) is isolated from the nearest population of H. maculata (located 29 km southeast; Dixon, 1967), whereas there are populations of Cowles prairie lizard immediately outside of the dune field. The extent of gene flow could explain why the bleached earless lizard is lighter colored than the Cowles prairie lizard. Dixon (1967) did find evidence of gene flow between dunes and non-dunes populations of Cowles prairie lizards. He found that prairie lizards collected from one to seven kilometers into the dune field showed "a progressively lighter ground color, especially within the first 3 kilometers" (p. 10).
Differences in the extent of gene flow between populations may also explain coloration patterns in dune-field mammals. Both Benson (1933) and Blair (1943) note that species that are reproductively isolated on the white sands are more likely to have evolved camouflage coloration than species that have populations in the surrounding area. The same is true of dark-colored animals living on the black lava at the Valley of Fires malpais. Of the nine small mammals trapped by Blair (1943) within the dune field, five species are probably not reproductively isolated from non-dunes populations, because there are animals living in the quartz sands surrounding the dunes. Of these five species, only one (20%), the spotted ground squirrel (Spermophilus spilosoma), has evolved lighter color. In contrast, of the four species that are reproductively isolated from non-dunes populations, two species (50%) have evolved white or lighter color, the Apache pocket mouse (Perognathus flavescens apachii) and the southern plains woodrat (Neotoma micropus leucophaea). Although sample sizes are quite small, these data do at least suggest that mammals that are reproductively isolated in the dunes are more likely to develop camouflage coloration. Note, though, that there could be a confounding ecological factor that makes it more likely for some species to be reproductively isolated and to evolve camouflage coloration.
Finally, the two camouflaged camel crickets in the dunes apparently differ in both the extent of gene flow between dunes and non-dunes populations and in the extent to which most animals within the dunes have colors that match the white sands. Ammobaenites were not collected at the eleven collecting localities immediately outside of the dunes, but Daihinoides were collected at sites outside of the dunes. As expected if these differences in gene flow affect the ability of the dunes populations to evolve camouflage coloration, all of the collected Ammobaenites were white, while the collected Daihinoides "vary in coloration from brown individuals to individuals which show considerable pigment reduction" (Stroud and Strohecker, 1949, p. 126)
How does the white coloration come about?
Possible mechanisms of color change
The final major question about white animals is how the white coloration comes about. There are three possible mechanisms. First, individuals may be able to change color during their lifetimes to match their current substrate, as chameleons and anoles are known to do. For such a mechanism to evolve, individuals with genes coding for flexible coloration must have been more likely to survive, reproduce, and pass their flexible-coloration genes on to their offspring. Second, each individual's light color may be fixed from birth. For fixed coloration to evolve, lighter-colored animals must have been more likely to survive, reproduce, and pass their light-coloration genes on to their offspring. Over many generations, the average color of the population would therefore get lighter and lighter, even though each individual’s color was fixed. Finally, it is possible that light coloration did not evolve through natural selection but is simply picked up from the environment. For example, substances from the gypsum may be taken up by plants and cause herbivorous animals to turn white when they ingest them (Benson, 1933). Benson (1933) argues that this third hypothesis is unlikely to explain the light coloration of animals at White Sands because the plants at White Sands are similar to plants present in other areas of the Tularosa Basin and probably take up substances similar to plants growing in alkaline soils elsewhere in the Basin.
It is still possible that direct accumulation of gypsum dust or sand on the skin of an animal could turn the animal white. The only species for which this appears likely is the white lycosid spider (see Table 2), which Bugbee described as "brown in basic color but its abdomen usually appeared as if covered with hoar-frost." Because "this white color was easily rubbed off when individual specimens were handled," it is possible that the white color is derived from external substances. Note, though, that it is also possible that the substance that is easily rubbed off is deposited by the spider and is internally derived.
To differentiate between the remaining two hypotheses, it is necessary to determine whether individual animals are able to change their color to match their current substrate as the chameleon hypothesis predicts, or whether individual color is fixed. These predictions have been most thoroughly tested in lizards.
Differentiating mechanisms of color change in lizards
Many species of lizards are able to quickly change their color in response to external and internal conditions, including temperature, exposure to light, and individual health and excitatory state (Smith, 1946). Some lizards, like chameleons and anoles, can even change color to more closely match their current substrate. Anoles change color by shifting the distribution of pigments between different skin layers. Melanin is located in melanophores, cells distributed several layers below the surface of the skin. The melanophores also send branches up to just below the inner surface of the skin. Anoles can change color from green to brown by moving the dark melanin pigment from deeper cell bodies to the branches just below the skin surface (Smith, 1946).
Although there are apparently no studies of color-changing mechanisms in the lizard species that live at white sands, it is clear that some species are able to change color, at least on a small scale. Bundy (1955) found that bleached earless lizards held in the laboratory get slightly darker when it's cold and slightly lighter when it's hot. Similarly, Lowe and Norris (1956) found that Cowles prairie lizards darken slightly when it's cold. As discussed above, these responses may help the lizards regulate temperature by increasing heat absorption when the animal is cold and decreasing it when the animal is hot. Because these lizards are able to change color over the short term, it is theoretically possible that individual white lizards at white sands have changed color to match their current white habitat as chameleons and anoles do, rather than having a light color that is reasonably fixed.
Bundy (1955) attempted to determine whether color is fixed or flexible in the bleached earless lizard. He collected white bleached earless lizards (H. maculata ruthveni) from the dunes and non-white individuals of H. maculata from areas near the dunes. He photographed all animals to record their color and then placed them into laboratory cages with either white quartz sand or finely ground black cinders. None of the lizards in Bundy's experiment changed colors to match the ground color in their current cage. Although the lizards did change color with temperature, as described above, the bleached earless lizards never got as dark as the darker subspecies, and the darker subspecies never got as white as the bleached earless lizard.
Smith (1943) and Lowe and Norris (1956) also held bleached earless lizards in the laboratory with different-colored sands. The lizards in those experiments also failed to change color to match the color of their current substrate. Similarly, Cowles prairie lizards and little striped whiptails held in the laboratory for up to two years did not change color (Lowe and Norris, 1956). These results suggest that the lighter-colored lizards within the dunes are white because they have genes that code for fixed light color and that, unlike chameleons and anoles, they do not change color to match their current background (Table 2).
Mechanisms of color change in other dune-field animals
There have been few attempts to distinguish between the alternative mechanisms for color change in white species other than lizards. However, some observational evidence, and an understanding of the mechanisms of color deposition in different taxa, suggest the likely mechanisms of color change for some other dune-field animals (Table 2). Some amphibians, like reptiles, can quickly change color to match their current substrate (Zim and Smith, 1987). Consistent with this general phenomenon, Stroud and Strohecker (1949) reported that the spadefoot toads they caught on the dunes were "completely white except for black eyes and black marks on the under-side of the hind feet." When they brought these toads into the laboratory, they gradually darkened to "the color typical of the species." Thus, these toads appear to match the color of their current substrate by quickly changing color rather than having fixed white coloration (Table 2).
In mammals, fur color is determined by the amount of pigment in the hairs. Once the pigment is deposited in each hair, fur color cannot be changed until the current coat is molted and replaced by another coat. Thus, just as we cannot change our hair color without external dyes, other mammals cannot change their fur color over the short term. However, even between molts, dune-field mammals may not change color to match their current background. Benson (1933) collected dark-colored pocket mice (Perognathus intermedius rupestris) from the Valley of Fires malpais and held them in the laboratory for several years on differently-colored substrates. Although the mice molted several times in the lab, individual color was fixed. Thus, malpais pocket mice, and probably white sands pocket mice, seem unable to change color to match their substrate (Table 2).
In insects, color is usually determined by the amount or type of pigment deposited in the cuticle and epidermis. Like mammals, insects could hypothetically change color between molts by changing the amount or type of pigment (Chapman, 1969). In fact color changes between molts like that often occur to facilitate camouflage in other insects (Chapman, 1969). There is a second method by which insects can change color. Some insects can change their color over the short term (e.g., from day to night) by moving pigment in epidermal cells closer to or further from the exterior (Chapman, 1969). Such short-term color changes typically occur in response to light or temperature (Chapman, 1969).
No one seems to have reared white insects from White Sands under controlled conditions with different-colored substrates, so it is too early to conclude whether color is fixed or flexible in these insects. Stroud (1950) did report on color changes in three insects, suggesting that the white insects use two different mechanisms to become white. He reports that the white locust Cibolacris parviceps arida at White Sands is "said to be able to change its color from one instar to the next in accordance with the color of the substrate" (p. 676). This report is consistent with Chapman's general observation that "the colours of grasshoppers and related insects tend to have a general resemblance to the prevailing colour of the environment...and a change in the environment leads to a change in the colour of the insect." In contrast, Stroud (1950) suggests that the color of the two white camel crickets at White Sands is probably fixed as a result of genetic differences between the white and the related brown subspecies. However, Stroud did not cite evidence to back up his reports, so it is not clear how he justifies these conclusions.
From the available evidence, white animals in the dunes appear to use all three mechanisms of color change (Table 2). The white spiders may derive their light color from the substrate itself. The toad, and possibly some insects, flexibly change color to match their current environment. The lizards and mammals seem to have individually fixed color that apparently evolved because better-camouflaged individuals were more likely to survive and reproduce. To confirm these tentative conclusions, controlled experiments should be done with more dune-field animals to test whether individuals held in the laboratory change color to match their substrate and to determine whether white individuals bred in the laboratory have white offspring.
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