Tuatara: Volume 31, Issue 1, July 1991
Visual Predation by Tuatara (Sphenodon Punctatus) on the Beach Beetle (Chaerodes Trachyscelides) as a Selective force in the Production of Distinct Colour Morphs
Visual Predation by Tuatara (Sphenodon Punctatus) on the Beach Beetle (Chaerodes Trachyscelides) as a Selective force in the Production of Distinct Colour Morphs
In order to demonstrate how natural selection could have influenced the proportions of colour morphs on black and white sandy beaches in the polychromatous beetle Chaerodes trachyscelides, we carried out feeding experiments, with the tuatara Sphenodon punctatus as the predator, under different ambient light conditions and black and white backgrounds. At light levels below 0.03 lux the tuatara began to make significantly more errors in the uptake of black beetles from a black background, when contrasted with black beetles on a white background or white beetles on a black background. By placing beetles into stoppered test-tubes, stimuli other than vision (e.g. olfaction, sound, vibration) were virtually eliminated and it was shown that vision is of paramount importance to the tuatara during the hunt for food. The lowest intensity that the tuatara was found to still make attacks, albeit with numerous misses, on black and white beetles in white and black dishes, respectively, was at 0.00615 lux — a figure approximately 1/50 that of full moonlight. Under totally dark conditions no reaction to prey, using infrared viewing equipment, was noticed.
Key words: Tuatara (Sphenodon punctatus), Coleoptera (Tenebrionidae, Chaerodes trachyscelides), Polymorphism/polychromatism, natural selection, predation and feeding behaviour, evolution, vision.
Stearns (1986) in a recent review on natural selection and fitness, adaptation and constraint, lists as the three necessary conditions for natural selection to have page 2 an evolutionary effect that (a) the trait under selection must be heritable in a broad sense (b) the entities must vary with regard to the trait and (c) this heritable variability must be associated with differential reproductive success.
As usually more than a single trait at any one time in a given population of conspecific individuals is variable and more than one selective force operates on that population, any experimental approach is fraught with difficulty — unless one can justify the reduction of both the number of variable traits and the selective forces to a minimum. The apparent success of industrial melanism in certain British moths in face of predation by birds (Kettlewell, 1965) is one such famous example, but we believe the interactions between the polychromatous beach beetle Chaerodes trachyscelides (Fig. 1) and the predatory tuatara Sphenodon punctatus (Fig. 3) here in New Zealand offer as excellent an example as any, to explain how selective pressure under natural conditions operates and how, in this particular case, it can lead to the production of localized sub-populations of differently coloured beetle specimens (Figs. 1 & 2).
Although the beetle Chaerodes trachyscelides today is much more widespread in New Zealand than the tuatara, tuatara and beetle species do occur in the same habitat. From studies of the natural history of the tuatara by Walls (1981) it is well known that of the prey groups consumed by tuatara, beetles and wetas were almost constant dietary components and appeared to have been preferentially selected for. Since predator and prey are involved in an evolutionary race, with the prey becoming more difficult to catch and eat and the predator perfecting its powers of search, pursuit, capture, and killing (Taylor, 1945) it seemed an interesting exercise to examine how successful tuatara would be in the uptake of white and black Chaerodes trachyscelides beetle morphs on white and black backgrounds under different ambient light levels. The following brief characteristics introduce the two actors in this controlled drama of predator and prey on stage in the experimental dark room of Waikato University.
The predator: Sphenodon punctatus (Fig. 1)
The tuatara is one of the most archaic and unspecialized reptiles in existence (Robb, 1977). From fossil remains it is evident that its rhynchocephalian ancestors were around 200 million years ago and that in the past they occurred in Europe, Asia, America, South and East Africa and, thus, are likely to have predated the beetle used in this study, as holometabolous insects did not really “take off” until about the Cretaceous.
Tuatara once lived in many parts of New Zealand from North Cape to Bluff, but are now confined to about 30 islands off the coast of New Zealand where they frequently co-exist with seabirds like shearwaters, prions, and diving petrels. According to Hazley (1982) Sphenodon has been forced into a nocturnal way of life because its food is nocturnal, but there could have been, and probably were, other reasons like temperature, water balance, etc. While insects are its main diet it has been observed to catch and eat shore skinks and geckos (Thorensen, 1967 cited in Robb, 1977) and feathers and bones of seabird chicks have been found in tuatara faecal pellets (Dawbin, 1962).
In totally dark conditions young (Meyer-Rochow, 1988) and mature (Wojtusiak, 1973) tuatara do not react to prey, suggesting that vision is the dominating sense in prey detection. Though the large eyeball in itself and the type of “vertical slit’ pupil are not necessarily characteristic of an exclusively nocturnal animal but rather of one that forages at night and at other times also utilizes bright sunshine (perhaps for basking), the retina of the tuatara has been reported to be rod-dominated as expected for a nocturnal feeder (Walls, 1942). An ultrastructural investigation of the retina, presently being undertaken by Collin and Meyer-Rochow, should page 3 determine the proportions of single, twin, and dwarf cones which Underwood (1970) after “careful scrutiny of Walls’ excellently fixed material” claims also exist in the retina of the tuatara.
Chaerodes trachyscelides is a flightless, tenebrionid beetle, approximately 7 mm long, which is widely distributed in New Zealand on sandy ocean beaches (Somerfield, 1966). There is no sexual dimorphism, but the species is polymorphic with regard to colouration. On black beaches, for example iron sand at Raglan (New Zealand west coast, North Island) the beetle's elytra are brown-black, while on the white beaches, like for example, Whangamata (New Zealand east coast, North Island) they are creamy-white. Spotted and mottled forms occur on beaches of intermediate sand type or, in smaller numbers, together with the uniformly coloured ones.
During the daytime, the beetles irrespective of their colour, are found under piles of seaweed up to 30 cm below the sand surface. They can be seen on the sand surface at night. The only obvious difference in the habitat of the black and white populations of Chaerodes trachyscelides appears to be the colour of the surrounding sand and not in the overall biology or life style of the beetles. Slightly more sensitive eyes were found in black individuals by Meyer-Rochow and Gokan (1988), which was regarded as a consequence of the greater attenuation of light in black sand. Structurally, however, the photoreceptors of black and white colour morphs were virtually identical.
Predation of conspicuously coloured individuals has been suggested by Meyer-Rochow and Gokan (1988) as the major force in producing the distinct polychromatism, but the two authors did not provide any factual evidence for their notion. The colour polymorphism in this beetle, irrespective of its evolutionary origin, is likely to be enhanced by the restriction of gene flow from population to population due to the low mobility and limited range of the beetle (Chaerodes trachyscelides is flightless and can exist only in a narrow band of seashore, where physical conditions like humidity of the sand, salinity, temperature, sand grain properties, slope etc. are just right).
Materials and Methods
Two juvenile tuatara were obtained from Victoria University of Wellington where they were hatched in April 1987. Throughout all experimental observations they were left in their usual habitat. This consisted of a 30 × 40 cm terrarium containing soil, leaf litter, a rock, a piece of bark, and a water dish. At the time of the experiment the tuatara were approximately 10 cm long. The results from only one tuatara (the same male in all observations) were used as this animal seemed tamer than the other one and also did not become satiated as quickly as the second individual. Satiation levels were determined well before the onset of any experimental series, so that by staying well below satiation level we were able to eliminate satiation as a complicating factor from the experiment.
Beetles had been dug up from under seaweed piles during midday on the coasts of Whangamata (white sand beach) and Raglan (black sand beach) and transferred by hand with some of the sand from the collecting site into white plastic containers. The beetles were kept in large lidded buckets in a room with a constant temperature of 13°C. Black or white beetles, one at a time, were presented to the tuatara under different light intensities on a black/white sectored flat dish and separate black and white dishes measuring 9.2 cm in diameter. Under very dim lights the reactions page 4 of the tuatara to the prey was observed through an infra-red viewer. The following situations were each tested 10 times at 8 different light intensities, namely 200, 4.5, 2.25, 0.5, 0.125, 0.03, 0.0125 and 0.0062 lux:
white beetle on a white dish (w/w)
white beetle on a black dish (w/b)
black beetle on a white dish (b/w)
black beetle on a black dish (b/b)
The first three light intensities were measured directly using a high performance photometer, but for the dimmer light levels under which the tuatara could operate, sophisticated photomultiplier equipment, in connection with computer processing, would have been required as conventional selenium-based photometers give no, or only highly inaccurate, readings under such conditions. Without the bulky and costly photomultiplier equipment, the second best was the photographic method. This method is based on the facts that at each increasing F-stop the amount of light admitted is halved and that a doubling of the duration of light-exposure corresponds to the widening of the aperture by one F-stop. For example: a 2-second exposure at F 2.8 admits the same amount of light as a 4 second exposure at F 5.6. However, considering a 2-second exposure at F 5.6 would have halved the amount of light, a 2-second exposure at F 11 would have reduced the light amount to 1/4, at F 22 to 1/8 etc. Using the human eye to match identical shades of grey in a series of photographs allows us to calculate the amount of light for each setting, provided that we can measure one or more of the brighter light levels accurately with a photometer. It is, of course, essential that film type, paper grade, developing and fixation times remain identical for the entire series of measurements.
For each of the first measurements (200 lux to 0.125 lux) every attack on a beetle, in each experimental situation, was successful the first time the attack was made, e.g. for w/w in 0.125 lux the tuatara successfully attacked and seized the beetle the first time the attempt was made for each of the 10 tests. The same applies to w/b, b/w, and b/b.
At 0.03 lux every attack on a beetle was successful with the first attempt in each situation except for b/b. For b/b the tuatara tended to miss the beetles, on average three times, before actually succeeding in seizing it.
At 0.0125 lux, for each situation, no attempt on a beetle was successful the first time. For w/b there was an average of 1.8 misses; b/w recorded 3.2 misses; w/w scored 4.9 misses and b/b had 6.1 misses.
At 0.00625 lux for w/w and b/b no real attack on a beetle during any test was recorded. The tuatara remained motionless, seemingly unaware of any prey nearby. Under the more contrasty conditions of w/b and b/w no first attempted attack on a beetle was successful.
In total darkness (see also Meyer-Rochow, 1988) no feeding attempt whatsoever was observed under any of the experimental conditions, suggesting that the tuatara reacted to the introduction of prey purely visually and that olfaction or sound were not involved.
The results of the attacks on beetles of different colouration on black or white dishes under various light intensities by tuatara are summarized and presented in tabulated form (Table 1).
In order to test the hypothesis that visual discrimination guides prey detection and selection in the tuatara, we carried out three additional series of experiments. In the first we offered the tuatara a choice between a mealworm and a beetle of similar colouration under 200 lux of light. In 8 out of 10 trials the tuatara page 5 ignored the crawling beetles and attacked the mealworm. We then placed a beetle into a stoppered test-tube and offered that, on its own, to the tuatara about 5 cm away from it. The tuatara reacted in the characteristic fashion, approached the prey in the usual way and each time attempted to seize the beetle. In the third trial series a mealworm and a beetle were placed into separate stoppered test-tubes, which were then placed in a dish approximately 5 cm away from the tuatara. As previously recorded when mealworm and beetle were not confined to the glass tube, the tuatara turned to the beetle very briefly on only one occasion, but in all other tests turned to the mealworm instead and tried to seize it.
Conclusion and Discussion
The experimental results support the hypothesis that polychromatism could increase phenotypic survival in the face of visual predation, first recognized by Poulton (1890, cited in Croze, 1970) and that natural selection may have been responsible for the perfection of some colour polymorphism in the beach beetle Chaerodes trachyscelides. In combination, all observations suggest that vision is of paramount importance to the tuatara. The tuatara can and does discriminate between food items. Its detection depends on environmental brightness and contrast between prey item and its background. If contrast is high, then food uptake is possible down to light intensities of at least 0.00615 lux. Full moon, in comparison, has a light intensity of approximately 0.2-0.3 lux, but moonlight intensity does not drop linearly with the decrease in reflecting surface area of the moon phases, so that at third quarter, for example, moonlight is only 1/10 as bright as full moonlight (Jackson, 1951).
Colour polymorphism and differently coloured sub-populations in a species are phenomena that can be encountered in most animal phyla (Drake, 1966). Mettler and Gregg (1969) address the question of the various selective forces leading to colour polymorphism and its maintenance in the snail Cepaea. Cain and Sheppard (cited in Mettler and Gregg, 1969) found a connection between the phenotypic composition of the population of Cepaea and the kinds of habitats they lived in. The commonest varieties were the least conspicuous in their habitat.
Predation of conspicuously coloured individuals, in the case of Cepaea and the famous melanic forms of various British moths, e.g. Biston betularia (Kettlewell, 1965), by birds, emerged as one of the major selective forces “preventing” as Abercrombie et al. (1980) put it “change in some directions … producing evolutionary change in other directions”. It now seems possible that predation by a nocturnal and visually-guided predator like the tuatara could be responsible for the fact that black beaches in New Zealand are populated by black morphs of the beetle Chaerodes trachyscelides, whereas white beaches are dominated by white colour morphs. The tuatara in this context does, of course, not mean that it is the only predator of the beach beetle, but rather is used as an example of one known predator for which we have real data. If temperature as in the intertidal snail Nucella lapillus (Etter, 1988) was a major selective force, one would have expected white beetles of high reflectivity to be more common on the extremely hot black sand, whereas on white sand this would have been of lesser importance.
Our results clearly demonstrate the difference in the degree of ease with which white beetles on a black background are detected and eliminated by predation in comparison to, for example, black beetles on a black background. Black beetles on white sand and white beetles on black sand are more conspicuous than matching colour pairs throughout the period of twilight and in the apparent absence of other adaptations, such as differences in crawling and digging speeds and differences in the beetles’ sensory system to detect the approach of a predator, would fall prey more easily than forms matching the background in body colouration. Tuatara, page 6 in turn, may learn to preferentially feed on conspicuously coloured individuals even if they can see the others, simply because fewer seizing attempts and, thus, less energy are required in making a successful strike.
Darwin (1975) has suggested that if a carnivorous or herbivorous animal is to be modified, it will almost certainly be modified in relation to its prey or food or in relation to the enemies it has to escape from. This is true not only in the case of the colour morphs of the beach beetle (which are likely to be preyed upon by birds and skinks as well), but also for the tuatara. The tuatara is fairly well camouflaged in its natural habitat and according to Croze (1970) predators have special behaviour patterns which seem to enhance their camouflage, like remaining completely motionless, waiting for prey to move into their vicinity. To some extent this is true for the tuatara and it would have been nice to know if tuatara populations near or on dark surfaces are of darker colouration than those living on islands with white or lighter substrates.
Our results underscore Dawbin's (1962) suggestion that detection of food by tuatara seems to depend mainly on sight and confirms earlier observations by Wojtusiak (1973) and Meyer-Rochow (1988) that no food detection in adult and juvenile tuatara, respectively, takes place in totally dark conditions. The light levels our tuatara still operated under were considerably lower than those prevailing at full moon and even quarter moon, which suggests that background illumination from stars may be sufficient for tuatara to hunt. The tuatara's well-known extremely low temperature preferendum may work in favour of its eyes' sensitivity, for Aho et al. (1988) were able to show that in the toad Bufo the behavioural threshold was about 1/8 that of a human and that a film link existed between thermal events at a molecular level and their behavioural consequences.
Because of a lack of electron microscope studies of the retina of the tuatara and a lack of optical and electrophysiological data, the anatomical or physiological basis of this extraordinarily high light sensitivity is not yet entirely clear. Conflicting reports exist on the presence and proportions of rods, single, twin, and dwarf cones in the tuatara retina (Underwood, 1970), which is why we have recently begun to examine the retinal ultrastructure (Collin and Meyer-Rochow, in preparation). Olfaction, though clearly of no importance in our trials, according to Walls (1981) may be responsible for the observed uptake of petrel eggs and carrion by tuatara. However the assertion by the same author that the tongue which manipulates prey in the tuatara's mouth, was not physically important during the actual capture of prey, could not be confirmed by us. We clearly saw and photographed (Fig. 3), the extension of the tongue during food uptake, but in all other phases of the feeding process, e.g. initial approach, cocking of the head, the darting grab followed by slow chewing and swallowing, we agree with previous authors (Dawbin, 1949, 19962; Walls, 1981).
We wish to thank Waikato University photographer Ross Clayton for help with the photographs and Dr M. Thompson of Victoria University for having made available the tuatara. The results of this paper were written up in the pleasant and quiet surroundings of Scott Base, Antarctica during the long wait for good news.
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|Light intensity||No. of trials||Mean number of misses before successful capture|
|“-” indicates that no attempt whatsoever was made to attack and seize the prey.|
* Present address: Regional Sophisticated Instrumentation Centre, North-East, Hill University, Bijni Complex, Shillong, 793003 Meghalaya, India, but from September 1991: Department of Zoology, The University of the West Indies, Mona-Campus, Kingston 7, Jamaica.