Adaptations for subterranean life

Subterranean mammals

Across the globe, some 300 (7%) of the extant species of mammals belonging to 54 (5%) genera and representing 10 (7.5%) families of four mammalian orders spend most of their lives in moist and dark, climatically stable, oxygen-poor and carbon dioxide-rich, self-constructed underground burrows, deprived of most sensory cues available above ground. The subterranean ecotope is safe from predators, but relatively unproductive and foraging is rather inefficient. These mammals are fully specialized for their unique way of life in which all the foraging, mating, and breeding takes place underground. These animals are called "subterranean" ("sub" means under, and "terra" means earth or soil), whereas animals that construct extensive burrow systems for shelter but search for their food (also) above ground are denoted "fossorial" ("fossor" means digger). Of course, there is a continuum from fossorial through facultative subterranean to strictly subterranean lifestyles.

The subterranean niche opened to mammals in the upper Eocene (45–35 million years ago [mya]) and then extended into upper Tertiary (Oligocene and Miocene, i.e., 33.7–5.3 mya) and Quaternary (some two mya) when in the course of global cooling and aridization, steppes, savannas, semideserts, and deserts expanded. In seasonally dry habitats, numerous plants (the so-called geophytes) produce underground storage organs (bulbs and tubers) that can be a substantial source of food for herbivorous animals. (Underground storage organs of some plants such as potatoes, sweet potatoes, yams, cassava, etc. are among the most important human staple foods.) There have been several waves of adaptive radiation when, independently in space and time, mammals in different phylogenetic lineages occupied the underground niche either to feed on geophytes (in the case of rodents) or to feed on invertebrates, which themselves find food and shelter underground (in the cases of insectivores, armadillos, and marsupial moles). Thus, two morphological and ecological subtypes of subterranean mammals have evolved. Nevertheless, they all have been subjected to similar environmental stresses and, as a consequence, have much in common. Although the subterranean ecotope is relatively simple, monotonous, stable, and predictable in many aspects, it is very specialized and stressful in others. Consequently, the adaptive evolution of subterranean mammals involves structural and functional changes, which are both regressive (degenerative) and progressive (compensatory) in nature. The mosaic convergent global evolution of subterranean mammals due to similar constraints and stresses is a superb example of evidence for evolution through natural selection, evidence obtained through comparative methods.

Who cares about subterranean mammals?

Although at least some of the underground dwellers have been known for many years, their biology has remained unstudied. This may be explained by the cryptic way of life of subterranean animals, and technical problems related with keeping, breeding, and observing them. The fact is, scientists were always more fascinated by animals coping with complicated environments and solving seemingly difficult and complex problems than by those encountered by mammals underground (sensitive vision versus blindness; echolocation in a highfrequency range versus hearing in a human auditory range; navigating across hundreds or thousands of miles versus maze orientation across tens of feet; thermoregulation in cold environments versus life in a thermally buffered burrow, etc.). Interestingly, although many preserved specimens of moles (i.e., insectivorous subterranean mammals) and mole-rats (subterranean rodents) have been collected and deposited in museums, not even the study of morphological digging specializations has received the attention it has deserved. Textbooks of biology in general and evolutionary biology in particular have brought diverse examples for convergent evolution, yet one of the most remarkable examples—convergent evolution of subterranean mammals—has rarely been mentioned.

It may be of interest to examine the literature dealing with ecology, evolution, morphological, physiological, and behavioral adaptations of subterranean mammals. Although there are some relevant scientific papers published as early as at the beginning of the nineteenth century, the real exponential growth of the research and publishing activity referring to subterranean mammals started in the 1940s. Since then, the number of publications has doubled about every 10 years. Thus, 56% of about 1,300 scientific papers addressing at least partly adaptations of subterranean mammals and published to date (March 2003) appeared after 1990, a further 25% are dated 1981 to 1990, and another 11% appeared between 1971 and 1980. The interest in adaptations of subterranean mammals

has been triggered particularly by two seminal papers on the blind mole-rat, Spalax, published in 1969, both authored or co-authored by Eviatar Nevo of the University of Haifa. In 1979, a review article (which has since become a citation classic) by Nevo stimulated considerable research into the physiology, sensory biology, communication, temporal and spatial orientation, ecology, taxonomy, and phylogeny of burrowing rodents. A second stimulus triggering the interest in subterranean mole-rats, particularly in their social behavior, came in 1981 with the pioneering studies of Jennifer U. M. Jarvis, when she reported on eusociality in the naked mole-rat, and in 1991, when a book was published on the evolution and behavioral ecology of naked mole-rats and related bathyergids. Since then, several international symposia on subterranean mammals have been convened and four books in English were published by renowned publishing houses within just two years (1999–2001).

Biased knowledge

Still, general knowledge on the subject is rather incomplete and heavily biased in several aspects. Most of the articles have been authored and co-authored by very few persons or research teams. Thus, 31% (410 out of 1,300) of the scientific papers bear a signature of one or more of just five authors (Bennett, Burda, Heth, Jarvis, and Nevo), while the most influential of them, Eviatar Nevo, has authored or coauthored 225 of them. As a consequence—since every scientist observes the world through her/his own eyes and is constrained by her/his own research possibilities (professional training, knowledge and experience, interests, affiliation, geography, available funding, etc.)—the research has many biases. Although the validity of the published data and findings is not questioned, their interpretation may be influenced by science's limited knowledge and/or ideology molded by the philosophy of the author and the world she/he lives in. However, this is a general problem of scientific research.

The taxonomic treatment is uneven in that almost 85% of all the papers on subterranean mammals and their adaptations deal with just a few species belonging to 10 (out of 54) genera (Arvicola, Cryptomys, Ctenomys, Geomys, Heterocephalus, Spalacopus, Spalax, Geomys bursarius, Talpa, and Tachyoryctes). Some of the species, like the mole (Talpa europaea), the northern water

vole (Arvicola terrestris), and pocket gophers (Geomyidae), have been studied to a much greater extent than considered here; yet most of the earlier studies on these animals have not specifically addressed subterranean adaptations. Usually, few species within (mostly) speciose genera have been studied in only a few localities within a broader geographic and ecological range of distribution. Studies are biased also as to which aspect of biology (and from which point of view) has been investigated. Thus, the (about 150) articles on the naked mole-rat (Heterocephalus glaber) primarily concentrate on the spectacular social behavior of this species, and some authors are prone to think of the naked mole-rats as if they were the only subterranean mammals. In spite of the fact that the naked mole-rat has attracted such intense interest by sociobiologists, only some 7% of all studies published on this species involved field ecological research and/or investigation of wild-captured animals. Most information on (social) behavior of the naked mole-rat has been based on the study of captive colonies. Yet, as S. Braude has demonstrated recently, long-term intensive and extensive field research may lead, at least in some aspects, to different results than the short-term study of captive animals. Interestingly, the problem of why the naked mole-rat is hairless (on both proximate and ultimate levels) has received very little attention from scientists. Similarly, although the question of whether subterranean mammals are blind or not (and if so, why do they still have miniscule eyes?) has been pertinent since Aristotle, the answer for most species is not yet known.

How to get through?

The most significant challenge is a mechanical one: soil is a dense, more or less hard and compact medium that cannot be penetrated easily. Movement through soil is energetically very costly. Vleck (1979) has estimated that a 5.3-oz (150-g) pocket gopher burrowing 3.3 ft (1 m) may expend 300–3,400 times more energy than moving the same distance on the surface. To keep the energy costs of burrowing at the minimum, the tunnel should have a diameter as small as possible. To achieve this, subterranean mammals have a cylindrical body with short limbs and no protruding appendages. Even testes of most underground dwellers are seasonally or permanently abdominal. Subterranean mammals are mostly small-sized animals weighing 3.5–7 oz (100–200 g), but ranging from 1 oz (30 g) (Namib golden mole, naked mole-rat, and mole-vole) to 8.8 lb (4 kg) (bamboo rat). In order to penetrate the mechanically resistant medium, subterranean mammals need efficient digging machinery. Subterranean rodents dig (loosen soil) primarily with their procumbent, ever-growing incisors, or use teeth and claws, whereas subterranean insectivores, armadillos, and the marsupial mole use only robust, heavily muscled and large-clawed forelimbs. In teeth-diggers, the whole skull is subservient to incisors and well-developed chewing muscles. Interestingly, subterranean rodents belonging to the suborder Hystricognathi (Bathyergidae, Octodontidae) transport loosened soil backwards by pushing or kicking the soil with hind limbs, whereas representatives of the suborder Sciurognatha (Muridae, Geomyidae) turn in the burrow and push out the loosened soil with the head. Desert golden moles as well as the marsupial mole do not dig permanent tunnels (except for their nest burrow), but "swim" through the sand. Although sand-swimming requires less than a tenth of the energy required by mammals that dig permanent tunnels through compact soil, it is still much more expensive than running on the surface. Sand-swimming at a mean velocity of 25–97 ft/h (7.6—29.6 m/h) (as recently estimated for the Australian marsupial mole [Notoryctes typhlops]

and Namib desert golden mole [Eremitalpa granti], respectively) is also substantially slower than walking or running above ground (about 1,476 ft/h [450 m/h]). It would apparently be energetically impossible for these mammals to obtain enough food by foraging only underground. Indeed, in one study of free-living Namib desert golden moles, the mean daily track length was 0.87 mi (1.4 km), but only 52.5 ft (16m) of it was below the surface.

Subterranean mammals can move backwards with the same ease as forwards. The skin is usually somewhat slack, and the fur tends to be short and upright, brushing in either direction. These all may be burrowing adaptations to match frictional resistance, to facilitate moving and turning in tunnels. The extremes such as the total alopecia (hairlessness) of the naked mole-rat or the long hairs and thick pelage of the silvery mole-rat (Heliophobius argenteocinereus) are exceptions to the rule and should not be considered burrowing adaptations per se. Reduction or even absence of auricles (pinnae) may be beneficial for digging and moving in tunnels because of the reduced friction. The popular assumption that auricles are reduced or missing because, otherwise, they would have to act as shovels collecting all the dirt cannot withstand critical comparative analysis. Many burrowing rodents have rather prominent auricles and are apparently not handicapped. Probably more important than whether auricles are an advantage or disadvantage for burrowing is whether they are required for sound localization. If not needed for hearing, only then would they be reduced. The tail tends to be shortened in subterranean and fossorial mammals, yet there is no clear explanation as to the adaptive value of this feature. For instance, African mole-rats of two related genera, Heterocephalus and Cryptomys, differ in this trait markedly. Similarly, fossorial-subterranean octodontids have medium-sized tails, whereas related surface dwelling cavies have reduced tails. Vibrissae in subterranean mammals are also shorter and less protruding than in many surface dwellers. In sand-swimming golden and marsupial moles, they are inconspicuous, sometimes even missing.

How to acquire oxygen

Subterranean mammals also have to cope with problems from the burrow atmosphere. The oxygen concentration may be as low as 6%, compared to 21% prevailing in the ambient atmosphere at sea level altitude. This means that the oxygen concentration even a few inches underground may be lower than that on Mount Everest. The carbon dioxide concentration in burrows ranges between 0.5–13.5% (compared to 0.03% in the above ground atmosphere). Surprisingly, some recent measurements in foraging tunnels of three species of African mole-rats have revealed, however, that concentrations of oxygen and carbon dioxide did not differ greatly from ambient values above ground. Nevertheless, gas concentrations may change rapidly after rains, they may differ in different soil types and depths, and, above all, they must change dramatically in the immediate vicinity of the nose of a burrowing animal. Normally, there are no air currents in underground burrows. One can imagine that an animal moving through the narrow tunnel acts like a piston securing the ventilation of burrows, much like a train in a subway tunnel. As suggested by Arieli, who significantly contributed to knowledge of respiratory physiology of mole-rats, enhanced burrowing activity following rains may serve as a means of replenishing the burrow atmosphere when the hypoxic-hypercapnic situation becomes aggravated. Of course, working under such conditions becomes even more difficult.

Whereas adaptations to extreme atmospheric conditions have been extensively studied in diving mammals and in mammals living at high altitudes, much less is known in this regard about subterranean mammals. The combination of extreme hypercapnia and hypoxia normally encountered and tolerated by subterranean animals is unique. Interestingly, whereas surface dwellers respond to hypercapnic conditions by increasing breathing frequency, subterranean mammals display lower ventilation rates than would be expected. In fact, ventilation is not effective for releasing carbon dioxide from blood when there is a high concentration of it in the inspired gas. The lungs of subterranean mammals do not show any specific morphological specializations—on the contrary they seem (at least in the few species studied so far) to be rather simplified and juvenile-like. Although the oxygen transport properties of blood vary markedly among subterranean mammals, and no generalizations can be made, relatively high hemoglobin affinity for oxygen has been reported consistently for several species of subterranean rodents. Because of the higher amount of carbon dioxide inhaled, a higher concentration of this gas in the blood and, thus, also higher blood acidity can be expected. It has been shown in the blind mole-rat that urine contains high values of bicarbonates and may serve as a pathway to bind and void carbon dioxide. Further adaptations to the extreme burrow atmosphere may involve higher capillary density in muscles (including the heart), higher volume of muscle mitochondria (found in the blind mole-rat), and, particularly, low metabolic rates and relaxed thermoregulation.

How to regulate temperature

The microclimate of the subterranean ecotope is rather stable. Particularly in the nest chamber, which in giant Zambian mole-rats (Cryptomys mechowi) is usually 23.6 in (60 cm) (in some cases, even 6.6 ft [2 m]) below ground, there are minimal daily or seasonal fluctuations in temperature and humidity. This constant temperature enables a lower basal rate of metabolism. In the thermally buffered environment of the underground "incubator," it is possible to abandon complex and complicated morphological and physiological mechanisms of thermoregulation. Indeed, subterranean mammals tend to hypothermia (lowering the body temperature—on average 89.6–96.8°F [32–36°C]). Body temperature is partly dependent

upon the ambient temperature. This relaxed thermoregulation (heterothermia) is most pronounced in the smallest (and the only hairless representative) among the subterranean mammals, the naked mole-rat. High relative humidity (about 93%) in underground burrows results in a relatively low vapor pressure gradient and low rate of water loss through exhalation or through the skin. This is beneficial for water balance as these animals do not drink free water, but instead obtain water from the food they consume.

However, high humidity and relatively high temperatures, which can occur on sunny days in shallow foraging burrows, may result in thermoregulatory problems. In the absence of evaporative and convective cooling, overheating and thermal stress would seem to be inevitable, since burrowing is energetically demanding and most mammals can tolerate dry, warm climate better than humid, warm climate. Subterranean mammals living in warmer environments have high thermal conductance, which means that the animals may exchange heat (cool or warm themselves) relatively easily through direct physical contact between themselves and the soil. As in poikilothermic reptiles, behavioral thermoregulation is of particular importance in heterothermic mammals. Thus, the animals can adapt timing and duration of their working activity to ambient temperatures in shallow burrows. Comparative and experimental physiological research of thermoregulation and energetics has a long tradition since McNab in 1966 first compared the metabolic rate of five subterranean rodent species and emphasized their shared adaptive convergence syndrome: low resting metabolic rate (involving also lower

ventilation and heart rates than would be expected on the basis of body size), low body temperature, and high thermal conductance. Since then, additional physiological data have been obtained on diverse species of subterranean mammals supporting the earlier conclusions by McNab.

How to avoid rickets

The underground ecotope is dark. Apart from the consequences for sensory orientation and communication, absence of light also influences some physiological functions. One of them is mineral metabolism. On the one hand, subterranean rodents have an especially high requirement for calcium because their large teeth are constantly worn down during digging. In the African mole-rat, Cryptomys, the visible part of the incisors regenerates completely every week. Also, calcium may be excreted in high concentrations as calcium carbonate through urine, a mechanism to deplete tissues of carbon dioxide. On the other hand, it is common knowledge that vitamin D (and principally D₃, cholecalciferol), which is needed for effective absorption of calcium from the gut (its deficiency causes rickets), is synthesized in the skin by the action of sunlight. Rochelle Buffenstein and colleagues have demonstrated that several species of African mole-rats, although in the perpetual state of vitamin D₃ deficiency due to their lightless environment, have evolved other physiological mechanisms to absorb calcium effectively (indeed, up to 91% of minerals can be extracted) from their diet.

How to tell time

Light-dark rhythm (photoperiod) is known to regulate production of the hormone melatonin that, in turn, regulates circadian (meaning around a day, as in a 24-hour period) rhythms by a feedback mechanism. In surface-dwelling vertebrates (including human), melatonin is produced during dark hours. It can therefore be expected that subterranean mammals living in constant darkness would display high melatonin levels. This does seem to be the case, yet the role of melatonin in regulating activity rhythms in subterranean animals remains obscure.

Permanent darkness in subterranean burrows makes sight and eyes rather useless and, apart from the fact that it precludes visual orientation in space, it also makes orientation in time problematic. Virtually all surface-dwelling mammals exhibit more or less pronounced circadian cycles of activity and diverse functions. These cycles are maintained by an endogenous pacemaker synchronized (entrained) by the socalled zeitgeber (time-giver). The most universal zeitgeber is the light-dark cycle perceived by photosensors. Considering the stability of the environment, constant availability of plant food, darkness underground, and poor sight or even blindness, one might expect that herbivorous subterranean rodents would not exhibit distinct diurnal activity/sleeping patterns. Field and laboratory studies on American pocket gophers (Geomys bursarius and Thomomys bottae) and African mole-rats (Heliophobius argenteocinereus and Cryptomys hottentotus) have revealed dispersed activity occurring throughout the 24 hours, for instance, arhythmicity and lack of distinct sleep-wake cycles. Interestingly, there are some other species of subterranean rodents that exhibit endogenous circadian activity rhythms that are free running in constant darkness and synchronized by light-dark cycles. These animals have been found to be either mostly diurnal such as the east Mediterranean blind mole-rat (Spalax ehrenbergi species complex), the East African mole rat (Tachyoryctes splendens), and the Kalahari mole-rat (Cryptomys damarensis); or predominantly nocturnal such as the African mole-rats (Georychus capensis and Heterocephalus glaber) and the Chilean coruro (Spalacopus cyanus).

There is no apparent correlation between the circadian activity pattern, on the one hand, and the degree of confinement to subterranean ecotope, development of eyes, seasonality of breeding, or social and mating systems, on the other. It should be noted, however, that findings in the same species have frequently been inconsistent. Available data have been obtained by different examination methods and may not be fully comparable. Moreover, there may be differences between individuals, sexes, and populations, between seasons of the year and habitats, as well as between the laboratory and the field. The methodological problem can be demonstrated in the example of the naked mole-rat, which had been considered to be arrhythmic by previous authors, yet was shown to display clear circadian rhythms and ability to synchronize them by the light-dark cycle if given an opportunity to work on a running wheel in the laboratory. There is a similar finding in Cryptomys anselli. Further studies of activity patterns in other species of mammals are clearly needed. A possible zeitgeber determining digging activity can be also temperature and humidity, which may fluctuate in shallow tunnels (although certainly not in deep nest chambers), as well as consequent changes in activity of invertebrates, which may affect foraging activity of moles.

The blind mole-rat, which is visually blind and has degenerated eyes, still has a hypertrophied retina and a large harderian gland in which the so-called circadian genes as well as the recently discovered photopigment melanopsin are expressed in high concentrations, and these apparently contribute to regulation of photoperiodicity. In other words, the double function of any vertebrate eye changed: instead of sight and circadian functions, only a circadian eye remains.

The ability to perceive and recognize the length of the photoperiod is important for seasonal structuring of reproductive behavior. It has also been suggested that melatonin may suppress production of gonadotrophins, hormones which, in turn, control activity of gonads and, thus, the sexual behavior and reproductive biology. Nothing is known about this aspect in subterranean mammals. Also unclear is how circannual (approximately one year) cycles are synchronized in subterranean mammals. These cycles are associated particularly with seasonal breeding in solitary territorial animals. It is assumed that the length of the photoperiod may play a role in seasonal breeders from temperate zones. Nevertheless, factors triggering breeding in mammals with long gestation from the tropics (where there is minimal variability in the daylight throughout the year) remain unknown and enigmatic in many cases. This is also the case for the eastern African silvery mole-rat. Alternating rains and drought represent the main periodic environmental factor. However, as shown recently, mating takes place at the end of the rainy and beginning of the dry season so that there is a substantial lag between the onset of rains (and subsequent softening of the soil and change of vegetation that could provide a triggering signal) and onset of breeding behavior.

How to find the way

Subterranean mammals construct, occupy, and maintain very long and extensive burrow systems. An average subterranean mammal (single, weighing 5.3 oz [150 g]) controls about 203 ft (62 m) of burrows. Of course, there are speciesspecific, habitat, and seasonal differences. This also implies that an average mole-rat living in a group consisting of 10 family members has to be familiar with at least 2,034 ft (620m) of burrows. The longest burrow systems were found in Cryptomys mole-rats and coruros. Yet, the burrow system is a complicated, complex, three-dimensional network. Although there is evidence that subterranean mammals have an extraordinary spatial memory based on well-developed kinesthetic sense (controlled, in part, by sensitive vestibular organs), this fact does not explain how subterranean mammals can steer the course of their digging and what, in absence of visual landmarks, is the nature of external reference cues for the kinesthetic sense. In 1990, the first evidence that Zambian mole-rats (Cryptomys anselli) show directional orientation based upon the magnetic compass sense was published. In a laboratory experiment, mole-rats collected nest materials and built a nest in a circular arena. They showed a spontaneous tendency to position their nests consistently in the southeast sector of the arena. When magnetic north was shifted (by means of Helmholtz coils), the animals shifted the position of the nest accordingly. This laboratory experiment on mole-rats has become the first unambiguous evidence for magnetic compass orientation in a mammal and a paradigm for further tests of magnetic compass orientation in small mammals.

Convergent spontaneous directional magnetic-based preference for location of nests in the laboratory was demonstrated also in taxonomically unrelated blind mole-rats from Israel. In 2001, Nemec and associates observed, for the first time in a mammal, structures in a brain (populations of neurons in colliculus superior), which are involved in magnetoreception in Cryptomys anselli.

The problem of orientation underground was addressed as recently as 2003, when it was reported that blind mole-rats could avoid obstacles by digging accurate and energy-conserving bypass tunnels. Apparently, the animals must possess both the means to evaluate the size of the obstacle as well as the ability to perceive its exact position relative to the original tunnel that it will rejoin. At present, information about potential sensory mechanisms can be only speculated.

How to find food

Subterranean mammals are animals that live and forage underground. However, the underground ecotope is low in productivity, burrowing is energetically demanding, and, in addition to these costs, foraging seems to be inefficient. It is widely assumed that subterranean rodents must forage blindly without using sensory cues available to and employed by surface dwellers. Indeed, vision is ineffective underground, there are no air currents to transmit airborne odorants over longer distances, high frequency sounds are damped by the soil, and low frequencies cannot be localized easily; touch and taste are only useful on contact. Carnivorous and/or insectivorous subterranean mammals such as moles can dig a stable foraging tunnel system into which prey may be trapped. Moles running

along existing burrows can locate prey by hearing their movement in the tunnel system. Prey animals may also leave scent trails that the insectivorous predator can follow. In most cases, the food is detected at encounter or in the immediate vicinity through touch. The most spectacular example for this type of foraging is the star-nosed mole (Condylura), with its Eimer-organ-invested rostral tentacles. Mason and Narins have shown that the Namib golden mole may use low-frequency vibrations produced by isolated hummocks of dune grass and orient its movement toward the hummocks and the invertebrate prey occurring there. However, in contrast to the prey of moles, tubers, bulbs, and roots are stationary and silent.

It has been demonstrated that subterranean rodents are able to dig in relatively straight lines until they encounter a food-rich area and then make branches to their tunnels to harvest as much as possible from this area. Tunneling in relatively straight burrows conserves energy because the animals do not search in the same area twice. Because geophytes are generally distributed in clumps and patches, extensive burrowing around one geophyte upon encountering it increases the chances of encountering another. Although this dual strategy has been described and its functional meaning recognized in different species of subterranean rodents, sensory mechanisms that may underlie the switch from linear to reticulate digging have not been addressed until a recent study. It has been shown that subterranean rodents can smell odorous substances leaking from growing plants and diffusing around the plant through the soil. Thus, herbivorous mammals are able to identify the presence of the plants and possibly even to identify particular types of plants specifically. They may be able to orient their digging toward areas that are more likely to provide food sources.

How to find a partner

In order to reproduce, mammals have to find and recognize an appropriate mate (belonging to the same species, opposite sex, adult, in breeding mood, sexually appealing). Monogamous mammals undergo this search once in life; solitary mammals have to seek mates each year. Subterranean mammals do not differ in this respect from their surface-dwelling counterparts. In 1987, two research teams reported, simultaneously and independently, the discovery of a new, previously unconsidered, mode of communication in blind mole-rats: vibrational (seismic) signaling. The animals can put themselves into efficient contact through vibrational signals produced by head drumming upon the ceiling of the tunnel. Communicative drumming by hind feet was reported for solitary African mole-rats (Georychus and Bathyergus). This behavior, however, could not be found in another solitary African mole-rat, the silvery mole-rat (Heliophobius). It can be speculated that seismic signaling evolved in those solitary species that disperse and look for potential mates underground. Subterranean mammals that usually occur at lower population densities and whose burrow systems are far apart from each other have to cover larger distances (which would be impossible to do by digging) in order to find a partner. They dare to carry out their courting above ground. These mammals such as the silvery mole-rat, the naked mole-rat, or the European mole have not invented seismic communication. Moles wandering at the surface in hopes of finding a burrow of a female probably are led by olfactory signals.

Seeing, or not seeing

Sensory perception plays a pivotal role not only in spatial and temporal orientation, foraging, and recognition of food, but also in communication with conspecifics. Like their surface dwelling counterparts, subterranean animals also must find and recognize a mate, recognize kin or intruders, and be warned of danger. This all is very difficult in a monotonous, dark world where transmission of most signals and cues is very limited. Some senses such as sight are apparently useless, whereas others have to compensate for their loss. One of the most prominent features of subterranean mammals is, no doubt, reduction of eyes and apparent blindness. The question of whether and what subterranean mammals see has been studied by Aristotle, Buffon, Geoffroy, Cuvier, and Darwin, among others. Still, today, no general unambiguous reply can be given. Thus, for instance, in comparing two of the most specialized subterranean rodents, the east Mediterranean blind mole-rat (Spalax) and the African mole-rat (Cryptomys), both are strictly confined to the underground and are of similar appearance, externally. They both have very small eyes and they both are behaviorally blind, yet whereas the eyes of the blind mole-rat are structurally degenerated and lie under the skin, the eyes of the African mole-rat are prominent, only miniaturized but in no respect degenerate; on the contrary, they are fully normally developed. As has been shown by several research groups, they also use different kinds of cone-pigments. Whereas the degenerated subcutaneous eye of the blind mole-rat has apparently adapted to a function in circadian photoreception, the function of a normally developed eye of the African mole-rat remains enigmatic.

Interestingly, whereas spalacines and bathyergids in the Old World lost their sight and have become completely subterranean, their New World counterparts, geomyids and octodontids, converged to similar habitats and habits retaining their eyes and sight. Unfortunately, the eyes and the sight of most subterranean mammals have not yet been studied.

As do blind people, blind subterranean mammals compensate for loss of sight by well-developed somatosensory perception, which was shown in the blind mole-rat, in the star-nosed mole, and in the naked mole. This somatosensory perception is over-represented also in the brain cortex where it occupies areas dominated in seeing mammals by visual projections.

How to hear underground

For communication and orientation in darkness, acoustic signals seem to be predestined, as exemplified by bats and dolphins. However, high sound frequencies (characterized by short wavelength), which can be well localized by small mammals and which are employed in echolocation, are quickly dampened underground. Low frequency sound, on the other hand, is characterized by long waves and cannot be localized easily. Indeed, it was demonstrated that, in a burrow of the blind mole-rat, sounds with a frequency of about 500 Hz were more efficiently transmitted than sounds of low and higher frequencies. Although nothing is known so far about the effect of the tunnel diameter, soil characteristics, temperature, and humidity, it is assumed that acoustic features of all burrows are rather similar. Consistent with the results of these measurements, the vocalization of all nine species (representing six genera) of subterranean rodents studied so far was also tuned to a lower frequency range. Corresponding with acoustics of the environment and with vocalization characteristics, the hearing of five species (of five genera) of subterranean mammals studied exhibited its highest sensitivity in the lower frequency range (0.5–2 kHz). This is quite unusual among small mammals, because hearing and vocalization in related surface dwellers of a comparable body size are usually much higher: about 8–16 kHz, or higher. The hearing range of subterranean mammals is very narrow, and frequencies of about 16 kHz and higher cannot be perceived (similar to humans). Frequency of 500 Hz is characterized by a wavelength of 27 in (68.6 cm). To be able to localize this frequency (to which hearing is tuned), an animal would need to have a head of a corresponding width; this is not possible. However, the transmission of airborne sounds in a tunnel is unidirectional, anyway. Consequently, animals that are confined to their underground

burrows do not need auricles for directional hearing. Some scholars would tend to label this restricted hearing as degenerated. However, looking at the morphology of the middle and inner ear, many progressive structural specializations enabling tuning of hearing to the given lower frequency range are observed. Indeed, several papers have described diverse morphological features of the middle and inner ear, as well as the expansion of auditory brain centers, which can be found consistently in non-related species of underground mammals and provide an example of convergent evolution. However, while the ear is clearly a low-frequencytuned receiver, apparently the evolution has not fully utilized all the possibilities, as demonstrated in ears of desert animals, to enhance the sensitivity. On the contrary, some features of the external ear canal, eardrum, and middle ear ossicular chain indicate that sensitivity has been secondarily and actively reduced. Too little is known about the acoustics of burrows, and also the suggestion of Quilliam, 40 years ago, that sound in burrows can be amplified as in an ear-trumpet, has not yet been tested. Should there really be such a stethoscope effect, reduction of sensitivity (in order to avoid deafening) would have to be considered an adaptation in the same way as its increase is in other species.

How to avoid tetanus

Humid, thermally stable soil swarms with many microorganisms (bacteria, fungi, protozoans), eggs, and larval stages of diverse helminths and arthropods, many of which are pathogens. A renowned representative is Clostridium tetani, a bacterium that is particularly prevalent in soil contaminated with animal droppings and that, after entering wounds, causes a serious disease, tetanus. Subterranean mammals are parasitologically understudied, and the results are inconsistent and do not allow any generalization. Many more factors probably influence whether an animal will be infected or infested by parasites. Higher lung infection by adiaspores of Emmonsia parva was reported in burrowing voles, as compared to more surface-dwelling mice. Yet, the preliminary examination of Spalax and Cryptomys provided variable, inconsistent results. The ectoparasites in African mole-rats are, however, very rare, and infestation with endoparasitic helminths is unusual. Surely, the examination of the immune system of subterranean mammals may be of great interest and importance for human medicine. At least, the few existing studies of Spalax do suggest the opening of new research horizons.

Living in a safe, predictable world

The underground ecotope is not only challenging, it is also quite safe from predators. Certainly, naked mole-rats would not be able to survive in any other ecotope than in the safe, humid, and ultraviolet-light-protected underground burrows. No wonder that convergent patterns can be seen also in life histories of subterranean mammals. They all show tendencies to K-strategy, breed rather slowly, have slow and long prenatal and postnatal development, slow rates of growth, and unusually long lifespans (an age of over 25 years has been recorded in the naked mole-rat in captivity, and there is an African mole-rat, Cryptomys anselli, that is at least 22 years old and is still breeding). On the proximate level, slow growth is surely correlated with low metabolic rates. However, the effect of phylogeny is very strong and phylogenetic relationships can best explain the length of pregnancy and many other parameters of life histories, such as mating behavior and mating system, as well as social systems.

In spite of all the similarities of the subterranean ecotope, there are differences in many of its biotic and abiotic parameters in different geographic regions and different habitats, which in turn also influence underground dwellers. Thus, subterranean mammals may serve not only as an example for convergent evolution but they provide cases to study adaptive divergence as well.

Last, but not least

Last, but not least, it should be mentioned that 40 million years of evolution underground, including hypoxia tolerance, light absence, etc., may prove important to biomedical research and human gene therapy. Subterranean mammals may become unique laboratory and model animals of the next generation.

Resources

Books

Bennett, Nigel C., and Chris G. Faulkes. African Mole-rats. Ecology and Eusociality. Cambridge, UK: Cambridge University Press, 2000.

Lacey, Eileen A., James L. Patton, and Guy N. Cameron, eds. Life Underground. The Biology of Subterranean Rodents. Chicago: University of Chicago Press, 2000.

Nevo, Eviatar. Mosaic Evolution of Subterranean Mammals: Regression, Progression and Global Convergence. Oxford: Oxford University Press, 1999.

Nevo, Eviatar, and Osvaldo A. Reig, eds. Evolution of Subterranean Mammals at the Organismal and Molecular Levels. New York: Wiley-Liss, 1990.

Nevo, Eviatar, Elena Ivanitskaya, and Avigdor Beiles. Adaptive Radiation of Blind Subterranean Mole Rats. Leiden: Backhuys Publishers, 2001.

Sherman, Paul W., Jennifer U. M. Jarvis, and Richard D. Alexander. The Biology of the Naked Mole-rat. Princeton, New Jersey: Princeton University Press, 1991.

Hynek Burda, PhD