Area and Endemism

Area and EndemismAuthor(s): Sydney AndersonSource: The Quarterly Review of Biology, Vol. 69, No. 4 (Dec., 1994), pp. 451-471Published by: The University of Chicago PressStable URL: http://www.jstor.org/stable/3036434 .

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VOLUME 69, No. 4 DECEMBER 1994

THE QUARTERLY REVIEW of BIJOLOGY

AREA AND ENDEMISM

SYDNEY ANDERSON

Department of Mammals, American Museum of Natural History New York, New York 10024-5192 USA

ABSTRACT

There are three major difficulties encountered by those dealing with the phenomenon ofendemism: a semantic problem, the absence of a clear conceptual framework, and an analytical problem. First, the terms endemic and endemism are used in the literature in unclear or contradictory ways. Often neither the title nor the abstract of an article makes the meaning clear. Following the usage that tends to prevail among Anglo-American zoogeographers, a species or other taxon is regarded here as endemic to an area if it occurs only in that area. To speak of a taxon as endemic in this context without specifying an area is meaningless. Since geographic ranges of taxa change with time, time must also be specified, or at least understood.

Second, a conceptual model is provided in which only changes in ranges (occurringfrequently) and speciation (occurring relatively rarely) are seen to change the percentage of endemism in any given area. At a subsidiary level, many complexfactors influence areographic changes and speciation. Among the more important of these are: distance from source to target area, size of area, geological age of area, time since isolation, environmental variety and stability, and vagility and ecological tolerance of organisms being considered. These are not all independent factors.

This complexity leads to the third and still largely unresolved problem, namely how to analyse a global biological system involving processes on both a shorter-term ecological time scale and a longer-term evolutionary time scale.

A REAS RANGING OVER more than seven orders of magnitude and repre-

sented by a number of taxonomic groups have been examined in this article to obtain a general view of the correlation between the size of an area being considered and the percentage of endemism therein.

A brief consideration of the boundary conditions of this relationship convinces one that the correlation must be positive. No species or other taxon, nor even an individual, can

exist in an infinitely small area. At the other extreme, when the entire biosphere of the Earth is considered, 100 percent of the species are endemic to it (neglecting, for all practical pur- poses, the infrequent straying of human be- ings to the moon and other such events). The interesting questions relate to what happens between these extremes. Do areas of different sizes tend to have different degrees of endemism? Do areas of a given size tend to have the same degree of endemism wherever and

The Quarterly Review of Biology, December 1994, Vol. 69, No. 4

Copyright ? 1994 by The University of Chicago. All rights reserved. 0033-5770/94/6904-0001$1 .00

451



452 THE QUARTERLY REVIEW OF BIOLOGY VOLUME 69

whenever they occur? If not, what factors influence the degree of endemism? Do different taxonomically or ecologically defined groups tend to have different degrees of endemism in the same areas or in areas of the same size? And if so, what factors influence this? These questions are addressed below.

METHODS

Examples are drawn from the literature, principally from recent years (Biological Ab- stracts for the years 1969 through 1992 were scanned), to illustrate some of the semantic problems resulting from different definitions of terms and to discuss factors that have been postulated to influence the occurrence of various degrees of endemism.

Tables 1 and 2 (pp. 464-465 and 468) include data on percentages of endemism in various subsets of biotas of different areas, and the sources of these data. These are selected examples, not an exhaustive summary of the biological literature. These data are graphi- cally summarized in Figure 1. "Southern Af- rica" is as mapped in Ellerman et al. (1953) north through Angola, Zambia, Malawi, and Mozambique. Other areas are self-evident.

A MAJOR SEMANTIC PROBLEM

The terms endemic and endemism have been and are now used with several different meanings. The original and the most common usage to date is in medical literature: A disease is referred to as endemic if it is con- stantly present to a greater or lesser degree in a particular place, as distinguished from epidemic (prevailing widely at some one time or periodically) or sporadic (occurring in a few instances from time to time). A second meaning is "belonging to or native to a particular people or country," as distinguished from introduced or naturalized. A third meaning is "restricted to a particular area." A fourth meaning is "limited to a small area." Clearly these several definitions are sources of confusion.

To quote a recent example, "we speak of these species with relatively restricted distributions as being endemic to such and such an area, and to a large extent these ranges are not randomly distributed. Rather, a group of species tends to have ranges which are more or less congruent with each other, and such an

area can be terned an endemic cente (Ridgely and Tudor, 1989: 24). This statement seems to imply that species with large geographic distributions may not be spoken of as endemics; this contradicts the third definition noted above, under which a species is endemic to an area, large or small, when occurring only in that area. To speak of a species or other taxon as endemic without specifying an area is meaningless by the third definition (the one used in this paper).

The congruence of more than one species range is of interest, but not germane to the foregoing concept of endemism as such. Con- cepts of regions, areas, or centers of endemism have attracted recent attention. For example, the term "centers of species endemism" has been used for areas formed by "clusters of endemic species with rather restricted and largely congruent ranges" (Haffer, 1981: 381). "The number of these fairly localized sympat- ric species mapped by contour lines decreases away from each center (where all species of a particular cluster coexist)" (Haffer, 1981: 381; see also Cracraft, 1985, 1991; Haffer, 1990). Armstrong et al. (1986: 13) discussed areographic "centers of coincidence" for mammals in the plains states (North Dakota south through Oklahoma). A center of coincidence "encompasses environmental conditions suit- able to all members of the faunal element, and it seems reasonable to suppose that such a center may represent the conditions under which members of the faunal element evolved their present genetic limits of tolerance." Arm- strong et al. postulated that such conditions may "have been located elsewhere in the past," therefore these centers should not be confused with "centers of origin." No species of mammal is endemic to the plains states, so no inter- pretation relating to endemism is possible. Nev- ertheless, the search for areographic patterns is similar whether the focus is on only the ranges of species, on possible place of origin, or on endemism.

C racraft (1985: 50- 5 1), expanding on Haf- fer's work with the South American avifauna, stated that areas of endemism are "defined by distributional congruence of the constituent taxa"; however, he also noted that "one species may be North American, another European, yet both are endemic to the Holarctic. What



DECEMBER 1994 AREA AND ENDEMISM 453

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P. Rico Tasmania Sumatra Argentina Palearctic Terra @ l Jamaica Cub3a Madagascar S. Afr. N. Amer. Firma Earth

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102 103 104 105 16 107 108

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FIG. 1. LOG-LOG PLOT OF THE PERCENTAGES OF SPECIES THAT ARE ENDEMIC IN AREAS OF

DIFFERENT SIZES

Lines encircle four samples of birds on islands (Mayr, 1965). The numbers 1 to 4 are each at the centroid for its sample. (1) three islands in the Gulf of Guinea, (2) six solitary and well-isolated islands, (3) twelve islands in scattered archipelagos, and (4) six single islands near mainlands or large archipelagos. Points represent: M: mammals, B: birds, A: anurans, S: serpents, L: lizards, and F: fish. Probably most area-endemism values for Australian Anura lie within the stippled area. The marginal points represent sample areas shown in Figure 2. Areas represented by Al to A3 (progressively larger sample areas A, B, and C, respectively) are in the part of the continent with the highest species density and A4 represents sample area F in a part of the continent with low species density. Areas represented are labeled across the bottom of the graph. Two unlabeled dots for Madagascar represent nonbat mammals at the top and bats below the labeled dot for all mammals.

this means, of course, is that two or more smaller areas of endemism may be nested within the larger one. Areas of endemism, therefore, appear to be organized hierarchically." What this means, also, is that neither the definition of endemism nor of areas of endemism is being applied consistently. Further attention is needed to clarify these important semantic details.

It would be interesting to plot points on a map showing the geometric centers of the geographic ranges of species of a given taxonomic group. I have never seen such a map. Any evident clustering of points could be used as the basis for defining centers of endemism in a more explicit or quantitative way than has been used up to now.

Dansereau (1957: 323) defined endemic as a taxon of very limited geographical extent,

usually local. More recently, a botanist (Hinz, 1989: 145) reviewed general concepts and various terms used for endemism and defined it as "the restricted or very localised distribution of a taxon," tracing this use to De Candolle (1820). A useful glossary of more that 60 terms, from apoendemique to vrai endemique, and published references thereto, was included by Hinz. In spite of the seeming comprehensive- ness of terms discussed, I was amazed to note that the widely used concept of endemic as confined to a specified area (regardless of size) was not clearly stated or documented. Hinz (1989: 148) did acknowledge that the concept of endemism could be applied to a family that occurred on a single continent.

A brief search revealed that endemique was used in French as early as the 16th century,



454 THE QUAR TERL Y REVIEW OF BIOLOGY VOLUME 69

with a general meaning similar to that currently prevailing in medical usage. The term endemic appeared in English as early as 1662, also with the same general meaning. By the early part of the 19th century, divergent and narrower definitions had come into use. In A Supplement to the Oxford English Dictionary [Ox- ford Univ. Press (Clarendon Press), Oxford, 1972: 943] endemism was defined as "the character or quality of being endemic; spec. of a plant or animal species, the state or condition of being indigenous only in a specified area." Also, Clements stated in 1905 (as quoted in the same source) that "since its first use by De Candolle, the term endemic has been employed . . .by phytogeographers with the meaning of 'peculiar to a certain region"' (p. 943).

In three of his major works, Charles Dar- win (indexed in Goldie and Ghiselin, 1992) used the term endemic in 22 places (the word endemism was not used). In general the meaning was either "having been produced in a specified place and nowhere else in the world" or "found nowhere else in the world." (The possibility that a species might have been produced in one place and might now occur only in some other place was not discussed.) "En- demic alpine forms" were mentioned once in the text, and thus the concept of ecological or habitat limitations was used rather than a strictly geographical concept.

The concepts of endemism as "confined to a specified area" and "confined to a small area" may coexist in an author's mind. For example, Clayton and Cope (1980), in a comprehensive analysis of patterns of diversification in Old World grasses, used the first concept of specified area consistently (always noting the geographic area being considered) when they tallied and compared numbers and percentages of endemic species in various regional floras. Nevertheless, they were led to mention "the awkward question of how widely distributed a species may be before it ceases to be endemic" (p. 145). Under the concept of specified area this question does not arise.

Since both Clements and Hinz cited De Candolle as the source of their different definitions of endemic, we need to consider De Can- dolle's own words (1820: 412).

"Among the general phenomena presented by the geographic distribution of plants, one

of the most inexplicable is the fact that in certain genera, certain families, all of the species known for a given country may occur only there. These may be termed, by analogy with medical terminology, as endemic genera (genres endemiques), in contrast with others that occur over the entire world and these may be termed as sporadic" (my translation). The countries (pays) considered by De Candolle ranged in size up to the United States of America and size as such was not mentioned. I have not reviewed the French literature enough to learn when the definition of endemic as referring to small size of distributional area came into use, but it did not begin with De Candolle (1820).

In one French review of the concept of endemism as used by botanists, Favarger (1969: 2) mentioned the earlier epidemiological connotation and then adopted a definition by Good (1947): "One speaks of an endemic taxon when its area is notably smaller than the average area for a taxon of its rank" (my translation). Good (1974: 45, in the 4th edition of the 1947 work) wrote, "In botany the word endemic is applied to any species or other taxonomic unit which is so distributed as to be confined to one particular country or region. It will therefore be seen that without further qualification the word is almost meaningless because every species is confined to some area, though that may be a very large one. In the geography of plants and animals, therefore, the use of the word is restricted somewhat conventionally to species or other units having a comparatively or abnormally restricted range. It should also properly be used with due regard for the size of the taxonomic unit under consideration. Although it is generally indescribable in words, there is an average range of families, an average range of genera, and an average range of species, these being progressively smaller, and the best practical limitation of the use of the word endemic is to restrict it to units whose ranges are obviously less than the average for their kind." As is clear from my discussion elsewhere, I think that this "limitation" was unfortunate. Good did not cite any prior use of his "best practical limitation of the use of the word endemic," and I don't know whether such use exists in the literature. The term stenotopic had been used earlier for species with small ranges (Hess et al., 1937: 121).




Most species are restricted to small areas (for discussion and summary of related theory see Anderson, 1985). Thus, each of these restricted species is endemic to some specifiable small area. It is not the smallness of the area, however, but the confinement of the species to it that makes the species endemic thereto. Also, a large area may contain many species with small ranges, all of which may be referred to as endemic to the large area, even if none of the small ranges overlap.

Endemic is also used ecologically to mean confined to a certain habitat rather than confined to a certain geographic area. Thus Wy- att (1977) discussed "granite outcrop endemics" and Baskin and Baskin (1972) discussed "cedar glade endemics." I suggest that the term habitat endemism would be appropriate in such cases. In another case (Mears, 1980), although "geographic endemism" appears in a title, the subject discussed is ecological or habitat endemism, namely the "narrow endemism" of plant species restricted to limestone or gypsum habitats.

A slightly different ecological connotation, that is, occurring in undisturbed native habitat, was used by Drew et al. (1984: 267), who referred to fruit flies "in their endemic rainforest habitat" in contrast to ecological studies of tropical fruit flies in Australia that have been confined primarily to "cultivated orchard situ- ations. "

Ecological and geographic concepts of endemism may be mixed, as in the statement that red-cockaded woodpeckers (Picoides bore- alis) are "endemic to mature open pine (Pinus spp.) forests of the southeastern United States" (Jackson, 1977: 448).

Scattered in the literature are many titles in which the term endemic is used without any obvious relevance to the subject of the article. For example, "cytogenetic study of the endemic Malagasy lemur: Hapalemur, I. Geoff- roy, 1851" (Rumpler and Albignac, 1973). The title would have indicated the content of the article more concisely and precisely if it were shortened to "Cytogenetic study of Ha- palemur."

The term endemic has been applied by ge- neticists to characteristics of animals rather than to the animals themselves; thus Pipkin et al. (1976: 265) referred to "moderately en-

demic autosomal inversions." This may mean that a certain inversion was found in samples from only a few geographic localities, but I am not certain of this. On page 264 these authors referred to "26 'highly endemic' inversions, each detected at one site only." (Site here means a geographic place, not a position on a chromosome.) In a discussion of the geographical distribution of chromosomal inversions in Drosophila, Ashburner and Lemeunier (1976) noted that inversions "fall into two major classes: rare, endemic, inversions and common, cosmopolitan inversions." They noted also that "there would appear to be a third class of rare, cosmopolitan inversions." The "endemic" inversions "are usually found in single collections of flies and are at low fre- quency in the population sampled," however, "a few endemic inversions have been found in populations distant from each other" (760 km apart in Japan).

Although the term endemic was not defined, it seems to be contrasted with cosmopolitan and to mean occurring at only one or a few places. Rare is another term with more than one meaning. For example, it may mean infrequent in a local population or occurring at few localities among those sampled. Zacharo- poulou and Pelecanos (1980: 107) used the concepts of Ashburner and Lemeunier (1976) and noted that "it is still not clear if this kind of [rare endemic] inversions are maintained or disappear quickly from natural populations. Our data favour the view that they are not maintained." So, another property of endemic inversions may be that they are temporary or transient. Whether this is intended to be an incidental rather than a defining property is unclear.

Minezawa et al. (1986) noted that "the karyotype of Bolivian monkeys so far studied was highly endemic" (p. 7), by which they meant that the karyotype in their Bolivian sample was different than in a sample from northern Colombia.

Endemic has been used also as an adjective modifying the noun (for the process of) speciation, for example, "endemic speciation [in the anuran genus Crinia] in southwestern Austra- lia." The meaning is that the biota of a specified area has resulted from speciation within that area rather than from a number of inva-




sions from outside the area (Barendse, 1984: 1238).

The undefined term "endemic biotas" was used by Rotondo et al. (1981), seemingly to mean biotas with many endemic species, although exactly how many species or what percent must be endemic to warrant the term endemic biota in any particular case was not stated. The percentage of endemism is relatively high for most groups on the Hawaiian Islands being discussed by Rotondo et al. Some species are present that are not endemic thereto. These include some fish mentioned as examples by Rotondo et al., some birds, and one mammal, the bat Lasiurus cinereus (summary in Darlington, 1957: 527). In regard to plants, Good (1974: 46) noted that about 90 percent of the species of flowering plants in the Hawai- ian archipelago were confined thereto.

The "endemic island fauna of Sardinia" was referred to by Spoor and Sondaar (1986: 399). Two human bones were present with remains of several other mammalian species that are known nowhere else, and it was noted that "the aberrant morphology [of the human bones] may be evidence of endemism, the result of the isolation of a human population on Sar- dinia." This use of the term endemism for a small and somewhat isolated human population does not seem appropriate to me under any of the definitions discussed herein.

Another interesting semantic mutation was found in the term "endemic injuries" referring (in the first degree of abstraction) to injuries caused by an endemic disease or endemic in- sect (in the medical or epidemiological sense noted above) affecting the root sprouts of aspen trees in Canada (Perala, 1984).

The confusion engendered by varied us- ages in the literature led Darlington (1957: 24) to urge considerable caution in using the term endemic. In fact, he wrote that he "would not use it [the word endemic] at all except that a very useful noun is formed from it, endemism, the existence of endemic forms." I am not pre- pared to give up the use of either of these terms, however.

It is too much to expect everyone to use the same definition; language does not work that way. Communication would be improved, scientific work would be expedited, and scien-

tific results would be more intelligible, however, if authors would indicate clearly what the intended meaning is when the term is used in a given paper or other context.

A CONCEPTUAL MODEL

I suggest the following conceptual model. Given any specified area containing represen- tatives of one or more species of some more inclusive taxonomic group such as a genus or family, the percentage of those species that are endemic to the area changes if either the number of endemic or of nonendemic species present in the area changes.

Numbers of species change only by one or more of the following processes:

(1) Splitting of one species in an area into two species (by whatever evolutionary mechanism). If one (or both) of the resulting species is confined to the area specified (i.e., is endemic thereto), this generally increases both the percentage of endemism and the species density in that area.

(2) Expansion of the range of an endemic species beyond the area, so that the species is no longer endemic. This reduces the percentage of endemism but does not change the species density (defined as the number of species present) in this area.

(3) Contraction of the extralimitalpart of the range of a species whose range initially extended beyond the area, to such a degree that the species becomes endemic to an area. This increases the percentage of endemism but, again, does not change the species density in the area.

(4) Extinction of an endemic species. Extinction may be regarded as a special case of range reduction to zero. This decreases both the percentage of endemism and the species density.

(5) Extinction within a specified area of one of the nonendemic species. This increases the percentage of endemism and reduces the species density.

(6) Expansion into a specified area of a species whose range was initially entirely outside the area. This decreases the percentage of endemism and adds to the number of species present.

The probability that process 6 will occur in- volves a host of subsidiary probabilities. Some of these may be generalized as follows. Let




us define a propagule as an animal, plant, seed, spore, or any other representative of a species that has the potential for propagating the species.

(a) The probability that a dispersing propagule from a given source area will arrive at a given target area is a function of the size of the target presented - assuming that propagules travel in linear paths and depart the source in random directions. However, if the propagule has a means of controlling its movement and detecting the target, the model becomes more complex. The distributional func- tions of islands as both "recipients" and "stepping stones" were discussed by MacArthur and Wil- son (1967: 123). These factors do seem reasonable, but their actual effects are difficult to measure.

(b) The probability that some propagule will arrive at a target area from a given source area is a function of the rate at which propagules leave the source. Rate refers to number per unit of time, not the velocity of departure.

(c) The probability that a specific propagule will arrive at a target area from a given source area is a function of the distance from the source to the target.

(d) The probability that a propagule of some species in the source area will arrive at the target area in any given period of time is a function of the number of species in the source area.

(e) The probability that a propagule of a given species in a source area will arrive at a given target area is a function of the vagility of that species, by individuals directly or via propagules in the form of seeds or spores. Va- gility was referred to by Hess et al. (1937: 76) as the "power of dispersal" or as "the capacity for . . . passive transport" (p. 122), a more restrictive definition.

(f) The probability that a species arriving at a target area will be a species not already present is a function of the number of species present at the source that are not already in the target area. If the source and the target have exactly the same biotas, the probability is 0. If the source and the target share no species, the probability is 1.

(g) The probability that a propagule of a new species arriving will survive and contrib- ute to a new population is a function of the requirements of the species and of the environmental conditions in the target area.

(7) More than one of these six basic processes may occur simultaneously or successively - for example, expansion of the range of an endemic species

beyond the specified area (process 2) and then its extinction within the original area (process 5). In other words, its entire range may move from one place to another. The net effect is a reduction in both the percentage of endemism and the species density. The reverse may occur also; a species may expand into the specified area and then become extinct outside of the area (first process 6 and then process 3). The net effect of this two-step process is to increase both the percentage of endemism and the species density. Movements of species ranges were probably not uncommon among species at the edge of arctic ice sheets, with the advances and retreats of glaciers in the Pleistocene (Guilday et al., 1964). Expansions and contractions of ranges in historic time are well documented, but it is more difficult to document a range (rather than an individual locality record) at a much earlier time.

In processes 2 through 7, the status or change in status of endemism depends on the sizes and locations of the geographic ranges of the species. The primary processes are thus areographic changes (and speciation, process 1, which itself changes ranges). By "primary" I mean conceptually most comprehensive, not causally first.

These relationships are summarized in Fig- ure 2. The total species density (= diversity or species richness) for a specified area is the sum of N2 and N3. This sum would be in equilibrium when new species arriving via processes 1 and 6 are equal to species becoming extinct (processes 4 and 5). A plus ( +) symbolizes the addition of a species while a minus ( - ) indicates the subtraction of a species. Pro- cesses involving the expansion of a range are shown with an up-arrow, contraction by a down-arrow.

To further elaborate, we may then consider factors that influence the size of, or changes in, a specific range, or the probability of occurrence of such sizes or changes in a more general sense. Consideration of these factors and their ramifications quickly leads us into nearly every aspect of the biology of the organisms being considered. This is the general conceptual framework within which I consider the question of the relationships of area and endemism.



458 THE QUARTERL Y REVIEW OF BIOLOGY VOLUME 69

N2 Ni number of number of species present species at but not endemic + 6 t external in an area source

1 + 5-

t 2 3 4

N3 number of species endemic in the area

1 + 4-

FIG. 2. DIAGRAM SHOWING RELATIONSHIPS OF

NUMBERS OF SPECIES IN SOURCE

AREAS, IN SOME SPECIFIED AREA

BUT NOT ENDEMIC THERETO,

AND ENDEMIC THERETO

Processes that can change these values as discussed in the text are shown by numbers.

OTHER FACTORS

A number of factors have been suggested in the literature as correlated with or contributing to greater degrees of endemism in a given area or in a given group of organisms. Some of these contributing factors are considered in more detail below.

(A) Greater distance from sources of immigrants. Mayr (1965: 1587) used subtropical and tropical avifaunal data from six "solitary, well- isolated" islands and six "single islands near mainlands or large archipelagos" to support the hypothesis that the former had higher degrees of endemism than the latter.

In a study of birds on 15 habitat islands of paramo vegetation in the northern Andes (Vuilleumier, 1970), the distance to the near- est large island was the most important vari- able predicting (in a statistical sense) both numbers and percentages of endemic species.

(B) Larger area. Mayr (1965) theorized that smaller islands can support only smaller populations, that genetic composition therein would be "so uniform that the most minute change

of environmental conditions became fatal," and that therefore "the smaller the island the lower the percentage of endemic species should be, because most of the populations become extinct before they reach species level, or soon thereafter." Mayr used avifaunal data for 29 subtropical and tropical islands up to the size of Madagascar (6.2 x 105 km2 or about 0.4% of the Earth's terrestrial surface) to support this hypothesis. These 29 islands were divided into 4 groups, namely 6 islands that are solitary and well isolated, 6 that are single and near mainlands or large archipelagos, 3 (pre- sumably treated separately because they are near the mainland and not single) in the Gulf of Guinea, and 14 in scattered archipelagos. "The curve for each type of island has a different zero point, but the slope is the same for the four kinds of islands." The "curves" were drawn as straight lines and there was no indi- cation of how they were plotted or calculated, perhaps they were placed simply by eye. The lines as drawn were parallel and show a positive correlation between area and (percentage of) endemism. The lines were plotted on a log-log scale and thus have no zero point in- tercepts in the usual sense. Mayr noted that the area-endemism correlation shown in his figures does not hold for islands in tight archipelagos or islands in temperate zones that had a complete turnover during the Pleistocene, although no specific data were presented for such islands.

Heaney (1986, Tables 6 and 9) reported that among Philippine mammals the number of endemic species is correlated with island area. Furthermore, islands on the continental shelf of less than 125,000 km2 do not have endemic species, whereas isolated oceanic islands as small as 47 km2 often do.

In general, larger islands have more endemics and solitary and well-isolated islands have more endemics than islands near mainlands or in large archipelagos. This increase in endemism with area of islands is consistent with the theory that turnover rates of species vary inversely with area. However, in only a few cases have turnover rates been studied directly (Diamond, 1971; critiqued by Lynch and Johnson, 1974).

The relation of turnover to endemism was discussed briefly by Slud (1976: 29), with an




emphasis on Cocos Island, about 500 km south- west of Costa Rica. This is a small island that had the same four species of birds in 1891 and in 1963 and thus does not conform to the theoretical expectation that smaller islands have higher turnover rates and hence different species present at different times. Although it is possible that different species were present at various times between 1891 and 1963 and that by chance the same four were present in both of these years, the probability of this does not seem high. This paper by Slud is a rich source of data and ideas on species densities of birds in all parts of the world; however, other than the discussion noted, it presents no data on endemism.

A note of semantic caution is in order here. One concept of biotic "turnover" is (as in above papers) change (over time) in the composition of a biota at one place or in one area. An alternative concept is change (geographically) in the composition of a biota as one goes from one place to another (for example, as one pas- ses from east to west across Australia; Wes- toby, 1988).

Area has its effects on endemism on continents as well as on islands. Exell and Gon- calves (1974: 107) noted a tendency for "endemic species . . . to increase in proportion to non-endemic species in proportion to an increase in the area," although they noted the occurrence of exceptions. They also suggested that the percentage of endemism tends to increase in groups with less effective dispersal mechanisms, less tolerance to climatic and edaphic variations, and lesser capacity for competition.

Some data relating endemism to area among mammals in different macrohabitats in South America were reported by Mares (1992: 978), who wrote that "as area increases, the number of endemic species increases more rapidly than does the number of endemic genera." Presum- ably, macrohabitats (as delineated by Mares, or slightly differently by Vuilleumier, 1988, as noted below) are relatively more internally homogeneous and relatively more sharply separated than areas of similar sizes placed randomly on the continent. To the extent that this is true, we should expect degrees of endemism to be near the maximum for areas of each size considered. Mares's data are plotted

100 SOUTH AMEERICA

DRYLANDS-

WESTRIN MONTANE FORSErS ? > * NAMAZONLAN LOWLANDS -o

UPLAND SEMDECIDUOUS FORESTS

) SC SouTHERN MESOPHyrIC FORES _

ATLANTIC RAINFOREST

oS --+<

1 5 10 50 100

% OF SOUrH AMERICA

FIG. 3. GRAPH SHOWING THE RELATIONSHIP OF

SIZES OF SELECTED MACROHABITATS

IN SOUTH AMERICA AND MAMMALIAN

FAUNAL DIVERSITY

Data are from Mares (1992), except that data for the entire continent were added. Linear regression lines for species density and percentage of endemism were calculated and plotted. The lines become curves on the log scales plotted.

(Fig. 3) on log-log scales to illustrate more clearly the relationship of size of the area to diversity (numbers of species) and endemism (percentage of species that are endemic to the specified area). The Amazonian area is slightly more diverse in proportion to its area than the "drylands" and thus the "myth of Amazonian biodiversity" in Mares's title seems to be a bit of hyperbole. The idea that drylands and other areas besides the Amazonian lowlands also have significant diversity and a need for conservation, however, is an important one. Pimm and Gittleman (1992: 940) noted that "the concentration of diversity is in the western montane forest" (a conclusion also sup- ported by Fig. 3). It would be difficult to select any part of either the Amazonian rainforest or the composite drylands of the size of the western montane forest that would exhibit as much diversity, whether measured by numbers of species or the percent of endemic species. This forested area is a relatively narrow strip along the east slopes of the Andes and




10 I I

0~~~~~~~~~

% OF SOUTH AIMRCA

FIG. 4. GRAPH SHOWING THE RELATIONSHIP OF SIZES OF SELECTED MACROHABITATS IN SOUTH AMERICA AND AVIAN FAUNAL DIVERSITY

Shows relationship on same scales as used for mammalian data in Figure 3. Data are from Haffer (1990) and Vuilleumier (1988). Macrohabitats represented are: A: Andean basins savannas; B:

Llanos; F: Southeastern Brazilian forest; G: Caa- tinga, Cerrado, and Chaco; H: Amazonian forest; I: Tropics (including all of the preceding); and J: South America. The curve is the regression line from Figure 3 of species density (percentage of continental fauna) for mammals, to facilitate comparisons described in the text.

is known locally as the yungas. The Andean altiplano and adjacent sierras above 3000 m comprise a part of Mares's drylands about the size of his "upland semideciduous forests" and somewhat larger than the "western montane forest." There are approximately 52 species of native mammals on the altiplano and about 42 percent of these are endemic to the altiplano, so the diversity in terms of number of species is less, but the percentage of endemism is higher than for the western montane forest.

Avifaunal data comparable to Mares's marn- malian data for "macrohabitats" (although not exactly the sarne macrohabitats) in South Amer- ica were published by Vuilleumier (1 988). Data are for resident terrestrial birds; migrants and water birds are omitted. I have plotted some of these data in Figure 4 on the same scales

used in Figure 3, for easier comparison. Some unexpected and striking differences between birds and mammals are evident. For birds, the percentage of endemism is greater than the percentage of the continental avifauna present in an area, with two exceptions (the entire tropical region and the lianos). This reverses the situation seen in Figure 3 for mammals. Furthermore, endemism values (percentages) for birds are generally higher than for mammals and the percentage of continental fauna present in an area tends to be lower for birds than for mammals. These relationships also reverse those found in North America and Australia (Anderson and Marcus, 1993), where birds have larger geographic ranges, lesser degrees of endemism, and higher percentages of the continental fauna present in any given place than mammals. These facts suggest some basic differences not only between birds and mammals but also between the avifaunas of South America and the other two continents. It suggests that mammals in South America may have larger ranges than birds. Geometric means or medians need to be compared, but sets of measurements are not available to an- swer this question.

In the study by Vuilleumier (1970, noted under factor A), the area of a habitat island of paramo vegetation contributed significantly in a stepwise regression to predicting the number of endemic taxa, although area was less important than either the distance to the near- est large island or the elevation. When the percentage of endemism was to be predicted, area was the second most important predictor, rather than the third. However, there is no apparent correlation between area and percent of endemism in a simple log-log plot.

(C) Geologically older areas. Preliminary data of Heaney (1986: 127) for Philippine mammals suggest that "geologically old oceanic islands have many endemic species, whereas young oceanic islands have few." Weller et al. (1990: 266) reported that "species diversity and endemism [of plants of the genus Sciedea] are greatest on the older Hawaiian Islands, suggesting that these islands were colonized first." Hess et al. (1937: 519) noted that the percentage of endemics in an island fauna is greater in older islands and (p. 88) summarized some earlier reports of Hawaiian endemism.




Miller (1984: 282) postulated that "the short geologic duration of isolation and high vagility of most of the species have limited endemism [of butterflies on the Channel Islands]."

(D) Earlier origin or isolation of the area. John- son and Raven (1973) reported that in local ecological communities the proportion of plant species that was endemic to the Galapagos Archipelago was greater in the arid transition zone and lesser in littoral and mesic zones. This was explained "in terms of zone-specific immigration and extinction rates and the very recent appearance of moist upland climates in the archipelago" (p. 893). Moist upland areas in some other archipelagos, such as the Philippine Islands, tend to have greater endemism, and they may be older.

(E) Slower rate of extinction (i.e., the probability of extinction for any given species has been less). This condition is also termed a lower turnover rate. MacArthur and Wilson (1 967: 173) noted that "the percentage of non-endemic species is probably a measure of the turnover rate" and that "it follows that percentage endemicity should increase with island area" (as noted under factor 2).

Heaney (1986) estimated extinction rates of 50% in 10,000 years in islands of 10,000 km2 and 1.1 % per 10,000 years over longer periods of 250,000 years. He estimated the colonization rate to be once in 2.5 to 5.0 x 105 years over water channels of 15 km or less between islands. These values are for nonvolant mammals (i.e., bats were omitted).

Heaney (1986) also suggested that "insular mammalian faunas typically are not in equilibrium, because geological and climatic changes can occur as rapidly as colonization and speciation" (p. 127). The model is "one of dynamic disequilibrium, in which geological and climatic processes are always a step ahead of the biotic systems, and faunas, in effect, chase their changing equilibrium point through time, always a step or two out of phase" (pp. 159- 160). Tracking models, such as the present case in which species density tracks but never quite reaches a theoretical equilibrium under changing conditions, have been discussed in the literature for a variety of biological parameters, for example evolutionary adaptation, gene fre- quencies in population biology, and range size distribution (Anderson, 1985: 5).

(F) Greater stability of the environment over longer periods of time. Exell and Goncalves (1974: 107) commented that groups having lesser tolerance of climatic variations will tend to exhibit greater degrees of endemism.

(G) Less pronounced seasonality. This is equiv- alent to the above except over a shorter time period, and seasonal fluctuations are much more regular than are longer-term environmental fluctuations.

(H) Slower rate of immigration. The immigration of a species into a specified area may be regarded as a special case of the expansion of the range of that species. The rate of immigration is correlated with factor A, the distance to a source. Assuming that other things are equal, the greater the distance the lower the probability that a new species will arrive.

(J) More species in thefauna. I have not found any reference that clearly stated this particular correlation. The number of species present in any sample area, however, will be equal to or greater than the number within any smaller area within the larger area. The species density at a given point can be no greater than the number present in any larger area that includes that point. In some cases larger areas contain not only more species but a higher percentage of endemics. Amphibian data from Australia (in Fig. 1) show increasing endemism within progressively expanded sample areas, and mammalian and avian data from South America (in Figs. 3 and 4) show a tendency for greater endemism in larger areas, even when they are separate and ecologically different. A continent does have both a higher degree of endemism and more species than any smaller part of the continent, but no theoretical reason has been advanced for why an increase in the number of species alone should increase endemism.

(K) The area is more topographically varied. This allows or contributes to the production of a greater number of different environmental conditions.

(L) The area includes a greater variety of habitats. The effect of topography is via habitats, although habitats can vary in the absence of topographical relief.

(M) A reduction in generalfavorability of environmental conditions. This may increase endemism. For example, Roberts (1981: 123), in a study




of Carboniferous brachiopods in eastern Aus- tralia, noted that "faunas associated with a sudden lowering of temperature suffer a significant drop in diversity but are character- ized by a high level of endemism." Roberts commented that this is related to reduction in sizes of ranges. If ranges are somewhat scattered (or noncongruent, as is generally the case), then a reduction in average range size would be accompanied by a decrease in the number of species at any one place and the smaller range sizes would increase the probability that any given range would fall within any specified area (i.e., would be endemic thereto).

(N) A taxonomic group having lower vagility is considered. Vagility is used here in the broad sense of powers of dispersal, both active and passive. Endemism is more common in some groups than in others. For example, in an analysis of Australian vertebrates (Anderson and Marcus, 1992), birds and bats were shown to have lower percentages of species endemic in Australia than do certain other groups. Mam- mals are intermediate between birds and the "lower" vertebrates in the incidence of endemism. It might be argued that since birds have greater mobility than mammals, and bats greater than rodents, this aspect of vagility contributes to the difference in endemism. Miller (1984) attributed the low endemism of butterflies on the Channel Islands to their vagility, in part. In comparisons, at the family level, of birds and mammals in the world's major faunal realms, Lenglet (1977) found that birds had lower percentages (29 % in the Neotrop- ics) of endemics than mammals (41%). In mammals, the greatest percentage of endemic families was in the Australian realm (48% compared with the 41 % noted for the Neo- tropics). Greater vagility is one of the ways in which birds in general differ from mammals, but other factors are probably involved here also.

Lack (1976: 226-227) studied birds of Ja- maica and suggested that "neither the number of resident species, nor the degree of endemism, are determined by difficulties of dispersal." He emphasized ecological factors, especially competition. Vuilleumier (1977) reviewed Lack's book and argued that competition was over- emphasized.

Another comparison between vertebrate groups (birds and reptiles) was made by Schwartz (1969) on satellite islands near His- paniola. His numbers indicate that endemism, at least at the subspecies level, was higher among reptiles than among birds. In this case vagility also may be an important factor.

Among plants, dispersal capacity via seeds or other propagules is comparable to animal vagility (Exell and Goncalves, 1974).

(0) A taxonomic group in which the species have smaller geographic ranges is considered (on continents). It may be noted that the same correlation noted under factor E between group and vagility also exists between these same groups and the sizes of their geographic ranges.

(P)A taxonomic group in which the species tolerate a lesser range of environmental conditions is considered. Hess et al. (1937: 121) used the term ecological valence for the amplitude of range of conditions under which the animal may exist. Exell and Goncalves (1974: 107) commented that groups of plants having lesser tolerance of edaphic variations will tend to exhibit greater degrees of endemism. They will also tend to have smaller geographic ranges.

(Q) The rate of speciation has been higher (i.e., the probability of a split for any given species has been greater).

Factors A to Q are not independent; they are in fact interrelated in many complex ways. Other factors and correlations exist.

DISCUSSION

We now consider some sample areas (the sizes of which are given in Table 1) and how some of the factors noted above may have contributed to their endemism. Some exceptions to general patterns or predictions are noted also.

In Madagascar, 81 % of the 101 species of native terrestrial mammals are endemic. Of the volant mammals (bats) only 32% (7 of 22 species) are endemic to Madagascar. The nonvolant terrestrial mammals are 94 % endemic (data from Honacki et al., 1982). En- demism in birds is 85 % (Mayr, 1965) or less. Vuilleumier (1986: 590, using data from Keith, 1980) noted 75% for breeding birds only, or 60 % if migrants and accidentals are included in the total count. Why is Madagascar excep- tional in having a higher percentage of endemism for birds than for bats?




Baffin Island in the Arctic has roughly the same area as Madagascar but has only nine terrestrial mammals, none of which is endemic to Baffin Island (data from E. R. Hall, 1981). In this case the fact that a given island has an area of fairly large size is relatively unim- portant in determining the taxonomic diversity and the endemicity of its fauna, in contrast to other factors, such as a relatively homogeneous environment, a harsh climate, a small pool of circumpolar arctic species to draw upon, and the recency of glaciation and hence of arrival of the current fauna.

The Yukon Territory of Canada is also about the same size as Madagascar or Baffin Island and lies at about the same latitude as Baffin Island. However, the Yukon differs in not being an island, in not having been completely glaciated, and in being adjacent to unglaci- ated areas (in Beringia to the west and areas in central North America south of the drift border of glaciation). Immigrants could have survived in the Yukon or entered it from these areas with relatively little impediment in the way of barriers. The Yukon Territory has 64 species of terrestrial mammals, none of which is endemic (Youngman, 1975).

The Andean altiplano, a continental area roughly the same size as the island of Mada- gascar, also has a high percentage of mammalian endemism (23 of 54 species or about 42 %o). This statement is based on my familiarity with the area (see comments under B above). The altiplano might be regarded as an island sur- rounded by quite different terrestrial habitats instead of water, so that the theories of island biogeography might be expected to apply. The idea that the fauna is in a dynamic equilibrium with continual immigration or reimmi- gration compensating for extinctions in an ecological time scale, however, is questionable because there is no source continent or com- panion island in an archipelago to provide the immigrants. Immigrant species, as opposed to individuals, may be drawn from surround- ing areas, but considering the different conditions and largely different mammalian faunas in these areas, events on a slow evolutionary time scale are probably more important than those on a shorter-term ecological time scale. This is a bit oversimplified. A more detailed analysis of mammals such as that done by

Vuilleumier (1986) for the avifauna would be interesting. There are more species of birds, a smaller percentage of endemics (but a higher absolute number, 48 vs. 23), more migrants, and more accidentals than among mammals. In the "Paramo, Puna, and Andino Alpine" biome (Vuilleumier, 1986: 588, 590), 48 of 318 species are endemic, or 12%, and if migrants, accidentals and peripherals were omitted, this number rises to 29 %T. This biome is comparable to the "altiplano" used in my less precise tally of mammals and clearly shows the much higher percentage of endemism in the mammalian fauna than in the avifauna.

In the plains states of central North America, from North Dakota south through Oklahoma, an area of 9.7 x 10' kM2, there are 146 species of freely ranging mammals (native and feral introductions), none of which is endemic to that area (Jones et al., 1985).

Some mammalian and avian data for four islands in the Greater Antilles (Cuba, His- paniola, Puerto Rico, andJamaica) are given in Table 1 and Figure 1. The percentage of endemism is higher for mammals than for birds in the two larger islands, whereas the reverse is found in the two smaller islands. A number of the mammals included in the tallies for Cuba and Hispaniola are species of insectivores and rodents that are now extinct. If these were excluded from the tally, the percentage of endemism would be lower for mammals. The currently surviving species in the native mammalian fauna are mostly bats.

On the island of New Caledonia in the south Pacific Ocean, the only native species of mammals, as contrasted with human and introduced, are bats. One of the five species of bats (20%) is endemic. Mayr (1965) graphed the percentage of species of birds on New Caledo- nia that are endemic thereto as 36 %. Some- what different numbers are 16 of 68, or 24 %, said to be endemic or shared only with the Loyalty Islands (Darlington, 1957: 525). Vuil- leumier and Gochfeld (1976: 239) mentioned 18 endemic species. I have not gone back to the original sources and compared lists of species in order to resolve these discrepancies.

On the smaller south Pacific island of Lord Howe, corresponding figures for mammals and birds are, respectively, 50 % (two native species of bats, one of which is endemic) and




TABLE 1 Samples used in Figure 1

Area Group km2 Species Endemic Percent Source species endemic

Earth's surface 5.1 x 108 Land surface 1.5 x 108 Australia Anurans 7.7 x 106 174 165 95 Anderson and Marcus, 1992

Birds 732 605 65 Lizards 436 417 96 Snakes 123 101 88 Marsupials 129 119 92 Bats 58 28 48 Rodents 55 47 85 All mammals 244 195 80

Tasmania Mammals 6.8 x 14O 31 3 10 Maps in Strahan, 1983 Birds 17 Mayr, 1965 Breeding birds 104 14 14 Ridpath and Moreau, 1966

North America Anurans 2.4 x 107 North of Mexico only Fish 764 711 93 Fresh water only Amphibians and reptiles 97 Mammals 2.6 x 107 87 South through Panama Birds 1719 785 46 AOU, 1983 Passeriformes 880 479 54 Others 839 306 36

Cuba Mammals 1.1 x 105 33 16 48 E. R. Hall, 1981 Bats 23 5 22 Birds 28 Mayr, 1965

Hispaniola Mammals 0.7 x 105 30 15 50 E. R. Hall, 1981 Bats 15 2 13 Birds 26 Mayr, 1965

Puerto Rico Mammals 9.0 x 103 17 2 12 E. R. Hall, 1981 Bats 15 1 7 Birds 18 Mayr, 1965

Jamaica Mammals 1.1 x 104 20 4 20 E. R. Hall, 1981 Bats 18 4 22 Birds 37 Mayr, 1965 Land birds 66 27 41 Lack, 1976 Water birds 40 1 2 Lack, 1976

continued

6 % endemic. The number of species of native, resident land birds was only about 15, and 8 of these are now extinct (Darlington, 1957: 525). Comparable figures for Tasmania are 10% endemism for mammals and 17% for birds.

In Argentina in southern South America, there are 257 terrestrial species of mammals, 15% of which are endemic (Olrog and Lu- cero, 1981; Honacki et al., 1982). In comparison, there are about 863 terrestrial species of birds in Argentina, of which 14 or 1.6% are endemic (Meyer de Schauensee, 1966). Oce-

anic species and accidentals were not included in the tallies.

In the European part of Eurasia, in an area of 1.1 x 10t km2, there are 362 species of birds, and only one (the finch Serinus citrinella) is endemic (Peterson et al., 1983).

In the Palearctic Region (Corbet, 1978), an area of 4.9 x 107 kM2, there are 554 species of terrestrial mammals, 67 % of which are endemic. Data on Palearctic birds (Vaurie, 1959, 1965) include 1133 species, 23 of which are oceanic species not included in the total when calculating percentage of endemism. Among




TABLE 1 Continued Area Group km2 Species Endemic Percent Source

species endemic

Madagascar Bats 5.9 x 105 22 7 32 Honacki et al., 1982 Nonbats 80 75 94 Mammals 101 82 81 Birds 84 Mayr, 1965 Breeding birds 299 180 60 Vuilleumier, 1986

Baffin Isl. Mammals 6.1 x 105 9 0 0 E. R. Hall, 1981 Yukon Terr. Mammals 5.3 x 105 64 0 0 Youngman, 1975 Palearctic Mammals 4.9 x 107 554 369 67 Corbet, 1978

Birds 1110 372 34 Vaurie, 1959, 1965 Passerines 579 239 41 Others 531 133 25

Southern Africa Mammals 6.0 x 106 318 91 29 Ellerman et al., 1953 Birds 978 143 15 Passerines 518 106 20 B. P. Hall and Moreau, 1970 Nonpasserines 460 37 8 Brown et al., 1982

Urban et al., 1986 Fry et al., 1988

Argentina Mammals 2.8 x 106 257 39 15 Olrog and Lucero, 1981 Honacki et al., 1982

Birds 863 14 2 Meyer de Schauensee, 1966 Java Mammals 1.3 x 105 61 7 11 Heaney, 1985

Resident land birds 289 30 10 MacKinnon and Phillipps, 1993 Sumatra Mammals 4.1 x 105 110 7 6 Heaney, 1985 Borneo Mammals 7.3 x 105 124 30 24 Heaney, 1985 Philippine Mammals 3.1 x 105 165 98 59 Heaney et al., 1987 Archipelago in toto Nonvolant mammals 93 79 85 Heaney, 1985

Fruit bats 23 14 61 Heaney and Rickart, 1990 Murid rodents 46 43 96 Heaney and Rickart, 1990 Resident land birds 312 45 MacKinnon and Phillipps, 1993

556 169 30 Dickinson et al., 1991 New Caledonia Bats 1.6 x 104 5 1 20 K. F. Koopman (pers. commun.)

Birds 36 Mayr, 1965 Birds 68 16 24 Darlington, 1957

Lord Howe Island Bats 1.0 x 10' 2 1 50 K. F. Koopman (pers. commun.) Birds 15 1 6 Mayr, 1965

Passeriformes, 239 of 579 species (or 41 %o) are endemic and of other orders 133 of 531 species (or 25 %) are endemic. The prevalent pattern in which mammals display a greater percentage of endemism than do birds in a given area is evident here.

The islands of the Philippine Archipelago have long been of biogeographic interest. Data on birds (Dickinson et al.,1991) and on mammals (Heaney et al., 1987) are found in Table 1 and Figure 1. Dickinson et al. cited comparisons with amphibians (31 of 56 or 56% are endemic to the archipelago) and with vascular plants (6300 of 9000 or 70 % are endemic). The

rank order in increasing degrees (%o) of endemism is thus birds, mammals, amphibians, and vascular plants, and the range is from 30% to 70%.

There are degrees of insularity. The change from land to water at the edge of Madagascar (or any other island in the usual sense) is abrupt. Although the change from highland to low- land (and all of the accompanying environmental changes) at the edge of the Andean altiplano is more gradual, it is still abrupt enough that many species boundaries occur there. Thus, the faunal composition changes almost entirely in a short distance, although the change is




less abrupt in the south than in the north. Since most changes within continents are less abrupt, we may predict that the percentage of endemism in continental areas of a given size will be generally less than in islands of the same size.

In comparisons of different areas or different groups in the same area, attention to sources of data and criteria for selecting data to be tallied are important. For example, in birds one should consider the following questions. Are tallies based on breeding species, perma- nent residents, migratory or part-time residents, land birds only, accidentals, occasional or casual occurrences, escapees, introduced individuals or now established populations, specimen records only, sight records, photo- graphs, or recordings of vocalizations? Are exactly the same geographic areas considered? Tallies for North American birds are based on the 6th American Ornithologists' Union (AOU) checklist, but Hawaiian records, accidental occurrences, oceanic species, and introductions, unless well established, were disregarded. A species confined to North America except for accidental occurrence outside the continent was included in the tally of North Ameri- can endemics, while a species occurring outside of North America and accidentally within North America was not. The coverage of the 6th checklist extends south through Panama and includes the Greater and Lesser Antilles south through Grenada, and thus is comparable with mammalian data from E. R. Hall (1981), whereas earlier checklists did not include Middle America and the West Indies. The inclusion of oceanic species would have added about 66 nonendemic species to the total of 1719.

The effect of area on endemism within a continent was examined using data on Aus- tralian Anura. Two points were selected, one in an area of maximum species density on the east coast and the other on the Australian Bight, where a minimum species density occurs. Three circles were drawn around each point, with each circle enclosing four times the area of the preceding (Fig. 5). The numbers of species present and the percentages of these that were endemic within each circle were tallied. These values are among those plotted in Figure 1. The well-known area-

Fc 1000 km I

FIG. 5. SAMPLE AREAS IN AUSTRALIA FOR

MEASURING AREA-ENDEMISM

CORRELATION IN ANURA

diversity increase (in the number of species with increased size of sample area; Anderson and Marcus, 1992) is less rapid than the increase in the numbers of endemics; therefore the percentage of endemism increases with area. The two sets of circular sample areas were selected to represent the extremes of endemism for areas of any given size, so most other sample areas for Australian anurans would have endemism values between the "curves" plotted.

I say "most" because it is possible to carefully select an area, such as the precise range of a species with a small range within an area of low species density (for example, the ranges of the species Ranidella riparia or Litoria gilleni), and observe endemism percentages of 8 and 12, respectively, in areas of about 2 x 1O' km2. These values lie well above the A1-A2-A3 line of Figure 1. However, if circular areas of this size were picked at random within Australia, and probably within other continents as well, such extreme values would be found less often than one in a thousand. The most extreme case is a species living by itself in a very small range (such as the North American Devils Hole pupfish, Cyprinodon diabolis, which is confined to a single limestone pool in southern Ne- vada), in which case the percentage of ende-




mism for fish is 100 % for an area of less than 1.0 x 10-2 km2.

Within a continent, theoretical considerations other than those emphasized in island biogeography may lead to the prediction of the same area-endemism correlation. If this occurs, in the future we should ask whether the different theories can be integrated or, if not, which theories are most general or useful and under what circumstances.

Attention has focused on species, but the concept of endemism is equally applicable to genera, families, or other higher categories. Mares (1992) documented that "as area increases, the number of endemic species increases more rapidly than does the number of endemic genera" for South American mammals. Given that our classification is a nested hierarchy, it is necessarily true for all cases and all areas in any time period, that any taxon has a range that is equal to or greater than the range of the largest subsidiary taxon. Data for families, genera and species of the world's mammals are in Table 2 (Krzanow- ski, 1986). Even at the geographic scale of the New World versus the Old World and the taxonomic scale of orders, the reduction of the percentage of endemism as one goes from species to genera and genera to families is evident. The Old and New Worlds are not clearly separated habitats for marine mammals the way they are for terrestrial mammals; the degrees of endemism are correspondingly lower for marine mammals.

SUMMARY

Now let us return to some questions raised in the introductory paragraphs. Do areas of different sizes tend to have different degrees of endemism? Yes, larger areas tend to have higher degrees of endemism. Do areas of a given size tend to have the same degree of endemism wherever and whenever they occur? No, there is great variation. Since they do not, what factors influence the degree of endemism? Many factors, some of which are listed below, influence the degree of endemism. Do different taxonomic or ecologically defined groups tend to have different degrees of endemism? Yes, for example, mammals generally have higher percentages of endemism than do birds, but there are exceptions. And if so,

what factors influence this? Groups in which the species have larger geographic ranges, lesser vagility, or lesser tolerance for environmental variation also have lower percentages of endemism.

The percentage of endemism in any specified area depends on its location and its size, on the group of organisms under consideration, and on its position in geological time. The percentage for a given area and group can change over longer periods of time because of speciation within the area, or over shorter times by any of several changes in areographic parameters (previously listed as processes 2 to 7), all involving the expansion or contraction of ranges of the species involved, including contraction to the point of extinction. Thus area, both that specified for study and that of the individual species therein, is highly relevant to any thorough consideration of endemism. Area and endemism are inti- mately linked.

The causes of areographic changes are many and varied. Greater degrees of endemism (i.e., a higher percentage of the endemic taxa of whatever group is being considered in a specified area) tend to occur (A) in areas that are more distant from sources of immigrants (from the mainland or other islands in the case of islands or that are isolated in other ways on continents), (B) in larger areas, (C) in geologically older areas, (D) when isolation of the area is less recent, (E) when the rate of extinction has been slower (i.e., the probability of extinction for any given species has been less), (F) if the environment has been more stable over time, (G) if seasonality is less pronounced, (H) if the rate of immigration has been slower, (J) if the fauna or flora includes more species, (K) if the area is more topographically and hence (L) environmentally varied, (M) if the general favorability of environmental conditions changes, (N) if a taxonomic group whose members have greater vagility is considered, (0) if a taxonomic group whose members have smaller range sizes is considered (on continents), (P) if members of the group tolerate a narrower range of environmental conditions, and (0) if the rate of speciation has been faster (i.e., the probability of a split for any given species has been greater). This list does not exhaust all possibilities, but serves to illustrate



468 THE QUAR TERL Y REVIE W OF BIOLOGY VOLUME 69

TABLE 2 Endemism in New and Old World Mammalia

(species, genera andfamilies, from Krzanowski, 1986)

Group World New Old Shared % of world % endemic to fauna World World fauna present New Old

endemics endemics New Old World World

World World

Species of: Marsupialia 263 84 179 0 32 68 100 100 Insectivora 395 68 325 2 18 83 97 99 Chiroptera 918 278 640 0 30 70 100 100 Primates 181 47 133 1 27 74 98 99 Carnivora 270 81 162 27 40 70 75 86 Pinnipedia' 34 7 10 17 71 79 29 37 Cetacea 77 8 12 57 84 90 12 17 Sirenia 5 2 2 1 60 60 67 67 Perissodactyla 18 3 15 0 17 83 100 100 Artiodactyla 187 24 159 4 15 87 86 98 Rodentia 1721 771 946 4 45 55 99 99 Lagomorpha 62 24 37 1 40 61 96 97

Total of above 4097 1390 2610 97 36 66 93 96 All 20 orders 4179 1419 2663 97 36 66 94 96

Genera of: Marsupialia 71 15 56 0 21 79 100 100 Insectivora 65 11 53 1 18 83 92 98 Chiroptera 175 75 93 7 47 57 91 93 Primates 51 16 34 1 33 69 94 97 Carnivora 108 20 61 27 44 81 43 69 Pinnipedia' 18 1 2 15 89 94 6 12 Cetacea 39 3 6 30 85 92 7 17 Sirenia 3 0 1 2 67 100 0 33 Perissodactyla 6 0 5 1 17 100 0 83 Aitiodactyla 77 12 59 6 23 84 67 91 Rodentia 397 141 245 11 38 64 93 96 Lagomorpha 12 2 8 2 33 83 50 80

Total of above 1004 295 621 88 37 69 80 89 All 20 orders 1037 308 641 88 38 70 78 88

Families of: Marsupialia 16 3 13 0 19 81 100 100 Insectivora 7 2 3 2 57 71 50 60 Chiroptera 17 6 8 3 53 65 67 73 Primates 14 3 10 1 29 79 75 91 Carnivora 12 0 4 8 67 100 0 33 Pinnipedia' 3 0 0 3 100 100 0 0 Cetacea 9 0 0 9 100 100 0 0 Sirenia 2 0 0 2 100 100 0 0 Perissodactyla 3 0 2 1 33 100 0 67 Artiodactyla 8 1 4 3 50 88 25 57 Rodentia 35 17 13 5 63 51 77 72 Lagomorpha 2 0 0 2 100 100 0 0

Total of above 125 32 57 36 55 75 45 59 All 20 orders 139 37 66 36 53 73 51 65 ' Includes Otariidae, Odobenidae, and Phocidae.




the complexity involved. Furthermore, these factors are not independent, but interact in complex ways.

In our understanding of the phenomenon of endemism there is a useful conceptual hierarchy in which changes in geographic ranges and speciation are the major considerations. Both areographic changes and speciation, however, are caused or influenced by many secon- dary and tertiary factors involving properties of both the environment and the organisms being considered. The relationships are those of a network and not of a linear branching tree. A precise and quantitative (i.e., mathe- matically expressed) theory embodying all of these relevant factors and generalized to apply to any group of organisms would be welcome. Data are now sufficient to suggest numerous interesting correlations and possible causes, but not to quantify or even rank them in any convincing way.

Philosophically, biologists should resist the temptation to formulate unique and untest- able "explanations" or answers to questions

such as "why is a certain percentage of species in the avifauna of Madagascar endemic thereto?" Instead, individual cases should be used to suggest generalities or hypotheses for further testing and to suggest places, times, and groups of organisms that may offer the most interesting and critical tests.

ACKNOWLEDGMENTS

I am grateful to George Barrowclough for providing reference materials on birds, to Fiona Fra- ser for carefully compiling data from these sources, and to Karl Koopman for data on bats. The librari- ans and others at the Southwestern Foundation for Biomedical Research in San Antonio and Western Michigan University in Kalamazoo were very helpful. Julio Gisbert, of Madrid, kindly reviewed a draft of this paper. Fran?ois Vuilleumier carefully reviewed a semifinal draft and offered many helpful suggestions; however, the responsibility for their application here is mine. Mary LeCroy provided helpful bibliographic assistance. Muriel Williams shepherded this through a variety of computer files and printouts. The American Museum of Natural History has, since my retirement, continued to support my research by providing office, library, and secretarial services.

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