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Each year the International Union for the Conservation of Nature (IUCN), the world's largest independent conservation organization, updates its Red Data Book which lists worldwide plant and animal species known to be endangered, vulnerable or rare. Out of approximately 950 species of bats in the world, the 1988 Red Data Book lists only 33 bat species in these categories— less than 4% of the total. This proportionately small number should lead anyone with even a remote awareness of the worldwide extinction crisis to be suspicious. Why then, does the red list stray so far from an accurate picture of the real problem?
First, consider that the IUCN red list has a substantial geographic bias toward North American species. There are 39 species of bats in North America (exclusive of Mexico),1 comprising about 5% of the worldwide bat diversity. However, five of the 33 species on the list are North American*— thus a fauna comprising only 5% of the total accounts for 15% of the number considered threatened or endangered.** Far from reflecting reality, the red list reflects our ignorance regarding the status of most species. We simply have more knowledge about the status of bats in North America than we do for most other parts of the world. In fact, our ignorance is so extreme that we are not even certain how accurate the IUCN list is for many North American species. We simply do not have the data to determine whether they are stable, increasing or decreasing, and at what rates. Given this lack of information and the fact that most bats investigated are declining, the IUCN red list gives an inaccurate and minimal assessment of the current crisis.
A different approach
Conservation biologists recently have suggested that constructing red lists has been a major tactical error.2 The mere existence of such lists can lead to the assumption that if a species is not listed, it is not in jeopardy. A great many species that are not on any threatened or endangered list, should be, but we do not know enough about them. A major problem is that to be included, the extent and rate of decline must be documented, but since in many cases, past populations have not been studied, this data is often not available. To correct this problem, it has been suggested that rather than putting together red lists, we should construct "green lists." Green lists would index species known to be secure.*** Species that are not green-listed would include those whose status is undetermined; given the grand scale of wildlife habitat loss throughout the world, we should consider all species not on a green list to be threatened and act accordingly. Thus, the burden of proof would be shifted to those who maintain that all is well with a species.
Bird conservationists are already proposing green lists. Even though much more is known about the status of the world's birds than of its bats, ornithologists concede that fewer than one third of the worldwide bird species would qualify for inclusion on a green list. This means that green lists are all the more important for bat species, since they are considerably less studied. I suspect that far fewer than one third of the world's bats would qualify for green list status.
With our ignorance as a perspective, consider some of what we do know about the status of bats— particularly, North American cave bats. Among the 39 species, cave roosting sites are essential for 18 of them, and some of the remaining 21 are occasionally found in caves. Thirteen of the 18 utilize caves year-round, both for reproduction and as winter roosts. The other five rely on caves only for hibernation, but roost elsewhere during the reproductive season. 1
All North American bats listed by the IUCN are cave dwellers, and four of the five require caves year round (the Indiana bat utilizes caves for winter hibernation only). Although it is certainly true that many cave bats are in jeopardy, there is undoubtedly a bias toward cave dwelling species because they are more easily censused. Many non-cave dwellers may be just as seriously threatened, but they are often neglected because they are much more difficult to observe.
A vulnerability to extinction
Bats have rates of population growth far lower than those of other small mammals. Many females do not begin reproducing until their second year, and most species give birth to only a single pup annually. Bats typically have long life spans (10 to over 30 years), which under normal circumstances counter their low reproductive rates. Consequently, their populations are built up over a long span of time, reducing the rate and probability of recovery from severe losses.
Bats have other characteristics which contribute to their vulnerability. One of the most significant is that they roost in large aggregations. The fact that so many concentrate into a few roost sites greatly increases their vulnerability. Mexican free-tailed bats (Tadarida brasiliensis) are an excellent example. Single cave roosts of these bats can contain tens of millions, so the loss of even one such roost would impact a significant portion of the species.
Wherever bats concentrate, they are vulnerable to a variety of human-caused disturbances. At least three endangered species (Indiana, Gray and Sanborn's long-nosed bats) have abandoned traditional roost sites because of cave disturbance or commercialization 3-5 Others lose their caves entirely during quarrying operations. I have personally observed numerous examples of vandalism such as burning old tires or shooting guns inside bat caves. Although intentional vandalism is well documented, unintentional disturbance often poses an even greater threat. In the temperate zone, bats typically encountered by cave explorers are either hibernating or rearing young. Disturbance as seemingly trivial as merely entering a roost area or shining a light can result in decreased chances for survival, outright death, or abandonment of the roost site. Although there is some controversy about the significance of "innocent"disturbance, my own experience has lead me to the opinion that it can be serious. The impact is somewhat species-specific, and the timing of the disturbance is crucial.
Unintentional disturbance of a maternity colony can cause individuals to abandon roost sites, particularly if it occurs early in the reproductive season when females are pregnant. As a result, females tend to break up into smaller groups, often moving deeper into the cave to less ideal roosts, where a variety of factors can greatly reduce growth rates and survival of young. In addition, disturbances can cause the outright death of young that are dropped by panicked mothers. 5
Maternity aggregations are, at least in part, a strategy for creating the high temperatures necessary to successfully raise young. Not only do clustering bats gain heat benefits from surrounding individuals, but in the case of very large colonies, they also benefit from the overall temperature increase in the cave. If the size of a colony decreases, individual thermal benefits may be lost, and it may become less advantageous, perhaps even impossible, for females to raise pups in that roost. When a colony reaches a certain low threshold number of individuals, roost temperatures are no longer sufficient for rearing young, and the roost must be abandoned.
Problems caused by disturbing hibernating bats also relate to energy requirements. During winter, bats in hibernation go for long periods without eating, allowing their body temperatures to drop, often to near freezing. The energy reserves they accumulate prior to hibernation may be only slightly more than what is needed to survive the winter. Disturbance during hibernation can cause bats to arouse prematurely, elevating body temperatures and utilizing stored energy. They may return to a state of torpor after a disturbance, but without sufficient energy to survive until spring.
Roost site disturbances also can seriously impact bat species that do not form large aggregations. For example, many tropical bats roost in hollow trees, which are being cut down as more tropical forest is converted for agriculture. For many of these species, if not for most, there are no population estimates and therefore no way of determining the impact that this loss of habitat may have on their populations.
Closer to home, it seems probable that the decline of the Indiana bat may be attributed, in part, to loss of tree roosts or feeding habitat. Indiana bats hibernate in caves and abandoned mines, and there is no question that disturbance of such sites has contributed to their decline. However, in the mid-western U.S., several large hibernating populations continue to decline even though they are now protected. 6 We can only speculate on the reasons. Indiana bats roost and give birth in tree hollows and under loose bark, and the loss of these roosts may very well be a factor in their continuing decline. This does not imply that disturbances within their hibernation roosts are unimportant. Rather, it emphasizes the importance of protecting hibernating sites so as not to add additional stress.
General habitat alteration and degradation can be important. For instance, two North American bats on the IUCN red list, in addition to being disturbed in their cave roosts, also are threatened by declining food resources. Both endangered long-nosed bats inhabit desert regions of the southwestern U.S. and Mexico, feeding on the nectar of desert flowers. Wild agaves provide a major food source during the bats' annual migrations, but these plants have been severely reduced by cattle grazing and by moonshiners who harvest them for making tequila. As long-nosed bats decline, their loss in turn threatens organ pipe, saguaro and other giant cacti. The decline of these cacti is evidently attributable, in large part, to the decline of their bat pollinators. 4,7
Modern crop and forest monocultures provide a prime example of how bat feeding habitat is lost. 1,2 Bats, as well as many other insectivorous animals, do best when varied habitats support a diversity of insect species whose differing hatching cycles assure a continuous food supply. Vast crop lands or forest plantations may produce many insects, but insects tend to hatch all at once, leaving bats without food between hatches.
Insecticides have had a negative impact on many bat populations. 8 At least two likely effects are direct poisoning and changes in the food resource base of insectivorous bats. Direct poisoning by DDT (now banned for use in the U.S.) and other organochlorine pesticides has been widely implicated in the declines of many populations.9-11 At present, we know little regarding the long-term effects on the insect prey base of bats. While pesticide poisoning has clearly been a factor in bat decline, there has been a tendency to over-emphasize its importance, distracting attention from other, more significant, causes.5,9,12 This does not exonerate pesticides, but rather points to what are often even more important causes of bat population decline: roost site interference and the reduction of feeding habitat.
Protecting critical habitat
From what we know about the impact of human activities on bat populations, roost site disturbance, vandalism and habitat destruction have all had severe effects, particularly on cave dwelling bats. Given the special problems of cave dwellers, I believe that the strategy of red lists and green lists may also be applied to cave habitat just as effectively as to the species that occupy them. People who visit caves, both professionally or for sport, need to be acutely aware of the potential damage they can do to the resident bats. There are caves which should be designated as "red caves"and not be visited by people at any time or only during certain times of the year. Designated "green caves"would be those not important to bats or other endangered animals, and these would be open to visitation any time.
Bats select cave sites because they fulfill very specific requirements, involving cave structure, air circulation patterns, temperature profiles and location relative to feeding sites. 5,13 Since these requirements are highly specific, suitable caves are relatively rare. For many bat populations, there may be only one or two acceptable roost sites, making these sites absolutely essential to their survival. Less than 5% of the caves surveyed in the southeastern U.S. were found suitable for Gray bat maternity or hibernating use. These caves must be placed on our cave red list. Conversely, the vast majority of caves do not satisfy these requirements and are not important as bat roosts. These can be placed on the green list, unless they contain other endangered animals.
The major problem is determining which caves belong on the green versus the red list. One obvious criterion is that major hibernation and maternity roosts of endangered bats or those of unknown status should be red-listed, at least during the seasons when bats require them. Many caves not occupied by bats, and for which there is no evidence of prior occupancy, would be green-listed. Judgments will have to be made, often with only limited information. It can be argued that historically important roosting sites that are now abandoned should be red-listed, at least temporarily, in the hope that they may be reoccupied. Caves with only small colonies should be red-listed also for the purpose of gene pool conservation. Caves essential to migrants during seasonal movements should be red-listed during the relevant seasons. On the other hand, there may be no harm in green-listing some caves that contain relatively small numbers of abundant, widely dispersed species (such as those of eastern pipistrelles), particularly if those caves are of interest to sport cavers.
Listing caves for no access or restricted use can be controversial. In the United States, several local grottos of the National Speleological Society already have constructed such lists or are in the process of evaluating them. These people should be supported in their efforts.
The original idea of constructing red lists was probably a good one at the time and, no doubt, has helped save many species from extinction. Today, however, this approach may not be enough. Conservationists worldwide acknowledge that many wildlife species and their habitats are in an accelerated rate of decline for many reasons, but mostly human related. Thinking in terms of green lists broadens our concern and emphasizes the critical need for more information on the status of most species.
Gary F. McCracken is an Associate Professor in the Department of Zoology and the Graduate Programs in Ecology and Ethology at the University of Tennessee, Knoxville. He has studied genetics and behavior of bats since 1976.
NOTE: This article is based, in part, on McCracken's lecture, "Special Problems with Bats,"presented at the 1988 annual convention of the National Speleological Society.
*The five species listed by the IUCN as endangered are the Indiana bat (Myotis sodalis), Gray bat (M. grisescens), Big-eared bat (Plecotus townsendii), Sanborn's long-nosed bat (Leptonycteris sanborni) and the Mexican long-nosed bat (L. nivalis).
**The official U.S. Endangered Species List, our own "red list,"contains even fewer bat species than that of the IUCN. The 1987 List includes only 11 bats worldwide. Three of the species listed (Indiana, Gray, and two subspecies of big-eared bats) are from the continental U.S. Sanborn's and Mexican long-nosed bats are scheduled to be added to this list in 1988.
***A good criterion for inclusion on a green list might be: known not to be declining in numbers now, and unlikely to decline substantially in the next decade.
1. Barbour, R.W. and W.H. Davis. 1969. Bats of America. Univ. of Kentucky Press.
2. Diamond, J.M. 1988. Red books for green lists? Nature, 332:304-305.
Imboden, C. 1988. Green lists instead of red books? World Birdwatch, 9(2):2.
3.Humphrey, S.R. 1978. Status, winter habitat, and management of the endangered Indiana bat, Myotis sodalis. Florida Sci., 41:65-76.
4. Wilson, D.E. 1985. Status Report: Leptonycteris sanborni, Hoffmeister. Sanborn's long-nosed bat. Rept. to U.S. Fish and Wildlife Service.
5. Tuttle, M.D. 1979. Status, causes of decline, and management of endangered gray bats. J. Wildl. Manag., 43:1-17.
6. Clawson, R.I. 1987. Indiana bats, down for the count. Bats, 5(2):3.
7. Proposed Rule, U.S. Fish and Wildlife Service, Federal Register, 52(128):25271-25275.
8. Stebbings, R.E. 1988. Conservation of European Bats, Christopher Helm, London, 246 pp.
9. Clark, D.R., Jr. 1981. Bats and environmental contaminants: a review. U.S. Fish and Wildlife Service Spec. Sci. Rept. #235.
10. Luckens, M.M. and W.H. Davis. 1964. Bats: sensitivity to DDT. Science, 146:948.
11. Geluso, K.N., J.S. Altenbach, and D.E. Wilson. 1981. Organochlorine residues in young Mexican free-tailed bats from several roosts. Amer. Midl. Nat. 105:249-257.
12. McCracken. G.F. 1986. Why are we losing our Mexican free-tailed bats? Bats, 3(3):1-2 & 4.
13. Tuttle, M.D. and D.E. Stephenson. 1978. Variation in the cave environment and its biological implications. Proc. Nat'l Cave Management Symp. (R. Zuber, J. Chester, S. Gilbert, and D. Rhoades, eds.), pp. 108-121.
Almost nothing is known about the behavior or status of Mastiff bats(Eumops perotis) Since they roost in cliff-face crevices and feed high about the ground, they are rarely seen except at a few select drinking sites. Mastiff bats are no longer found in many previously occupied sites and may be endangered, though past and present observations are too few to determine their status. PHOTO BY MERLIN D. TUTTLE
Indiana bats (Myotis sodalis) hibernate in just a few critical caves, packing into tight clusters where they are extremely vulnerable to disturbance. This endangered species is believed to have declined by 55% in less than 10 years. PHOTO BY MERLIN D. TUTTLE
Left: The U.S. Fish and Wildlife Service coordinates and carefully plans censusing for endangered bats, conducting them at two-year intervals to minimize disturbance. Cave-dwellers such as these endangered Gray bats (Myotis grisescens) return year after year to the same roosts and are easily observed and censused, so their decline is more likely to be noticed.
Right: Tree-dwellers such as the Red bat (Lasiurus borealis) are far less predictable and roost individually, well camouflaged in foliage. Some tree-dwellers may be endangered, but we lack observations to document their status.
Above: Long-eared myotis bats (Myotis evotis) are found from Mexico into Canada, though never in abundance. Almost nothing is known of their biology or behavior. Some biologists fear that they may be threatened, but no records exist that would enable determination of status.
Right: Western pipistrelles (Pipistrellus hesperus) are considered one of the most abundant bats of arid regions in western North America, yet they too are poorly studied and have never even been seen in a natural roost. Population status trends are unknown. PHOTOS BY MERLIN D. TUTTLE
Most of the U.S. population of Mexican free-tailed bats (Tadarida brasiliensis) rears young in just 12 caves, each of which contains many millions. Therefore, loss of a single cave roost could have major impact on the entire species population. Here, thousands of square feet of cave walls are covered with bats– up to 500 per square foot. PHOTO BY MERLIN D. TUTTLE