The species-area function, S = cAz, relates the number of species counted (S) to the area surveyed (A); c and z are constants. The function is reasonably consistent across different well-known animal and plant groups in different areas (33).
It suggests a simple recipe: if the original habitat area, AO, is reduced to An, the original number of species, SO, should decline to Sn, where SnISo = CA0Z/cAoz or (An/Ao)Z. This expression is independent of c; z is often taken to be 1/4. We estimate forest reduction, A 1872/A1620 to be 1/2; thus 16% of the region's species should have become extinct.
This simple recipe makes a critical assumption: we suppose that the same function applies equally to cases where habitats are actively being destroyed as to the counts of species in areas of different sizes. The recipe also begs our asking how good is the approximation of z 1 /4. We can estimate z using data on the current bird distributions. In doing so, we recognize that the estimate will reflect the extinctions and range reductions already caused by deforestation. We can also contrast our estimate of z to values derived from other studies. To estimate the number of species lost (rather than just the percentage), we also require an estimate, S.-the number of species before deforestation. This would seem to be almost trivial for a fauna as well-known as eastern forest birds. Interestingly, it is the interpretation of SO that has created the confusion.
Value ofz. Using Peterson's range maps (34), we counted the number of native terrestrial species per state and for 31 eastern states combined. Contrasting any one state with the total area gives a z value. The highest of the 31 values (z = 0.28) compares Florida's species list (95) and area (-1.4 x 105 kM2) to the total list (215) and area (-2.9 x 106 kM2). The lowest value (0.09) comes from comparing a small, central state (Maryland; 140 species, 2.5 x 104 kM2) with the total list and area. Maryland, being central, has many species from both north and south, while geographically isolated Florida is relatively species poor. The 31 values are not statistically independent of each other, but statistical inference is not the issue. Each value suggests the consequence of a scenario of forest reduction. Hypothetically, were Maryland the sole habitat reserve left after the total destruction of all other eastern forests, we might expect it to shelter more surviving bird species than if Florida were the sole reserve. Neither scenario is even approximately correct. Forests have been lost throughout the eastern region, so some intermediate value of z would seem to be sensible.
These estimates of z are flawed. We include the species lost from the region in the total count, but we do not know how many species are now missing from each state's modern total. Interestingly, there is an increasing arithmetic contradiction in adding many extinct species to these totals. The more we add, the smaller will be the z value we will calculate. A small z value then predicts that the state should have lost few species following deforestation.
Eliminating the contradiction is easy using an iterative procedure, for which we present only the last step. Suppose that Maryland had lost 8 species. We add those 8 to the state's total and recalculate z as 0.08. Given this value, Maryland should have lost 8 species following a 50% deforestation. The values (z = 0.08, 8 species) are not contradictory, but other pairs are. Suppose Maryland had lost 75 species and so once would have held all the eastern species. One recalculates z as 0.0. Consequently, no species should have become extinct following a 50% loss of its forests, yet we supposed that 75 were.
Across all 31 states, comparable calculations show that z values are not changed perceptibily by this process. This is not the circular argument it might appear. If each state now held few species and if those species were unique to the state, then the z values we calculate would be large and the predictions of each state's losses would also be large. We do not observe this pattern. This alone constrains the value of z, even in our ignorance of the original species ranges.
What value of z should we expect? Rosenzweig (33) suggests at least three broad categories of values. Archipelagos where rises in the sea level have isolated once-continuous blocks of habitat provide a model close to the habitat fragmentation process. They typically yield estimates of z -1/4. The largest values (z -0.6-1.0) are for very small easily counted woodlots or similar habitat patches. The smallest patches may contain very few individuals and obviously few species. Which species survive often will be a matter of chance, so different species will remain in different fragments. Progressively aggregating areas will quickly increase the species list. Similarly, progressively aggregating species lists across widely separated, oceanic islands also yield high values of z, because the species have evolved independently on different islands. Conversely, the smallest estimates of z (often
Birds of Eastern North America. The 31 states running from Louisiana north to Minnesota and east to the Atlantic, plus Kansas and southern Ontario, are home to 215 native species of terrestrial birds (34). Of these, we consider that only 160 belong to the eastern forests. Our choice is subjective and others would produce slightly different lists. These differences will not alter our key arguments. We exclude all introduced species: 16 species that occur in open, typically grassland habitats on the western fringes of the area; 7 species that occur only in nonforested, subtropical habitats in Florida; and 3 species of the marine fringe that are rarely found away from salt marshes. We have included Minnesota, Michigan, and the northern New England states because they have some deciduous forest, but we exclude 25 species from the boreal forests in the northern part of these states. One of these, Kirtland's warbler (Dendroica kirtlandii), is a critically endangered species found only in Michigan. The remaining species are eastern forest species to varying degrees. We return to the meaning of "varying degrees" presently. On request, we will provide a complete list of the species we included and excluded. There are four well-known extinctions in eastern North America: passenger pigeon (Ectopistes migratorius), Carolina parakeet (Conuropsis carolinensis), ivory-billed woodpecker (Campehilus principalis), and Bachman's warbler (Vermivora bachmanii). [The isolated Cuban subspecies of the ivory-billed woodpecker is also now extinct (35).] Bachman's warbler has not been reported since 1984 despite exhaustive, intensive field surveys in its former breeding range (36). One species is critically endangered: red-cockaded woodpecker (Picoides borealis). Ornithological exploration began well before the peak period of deforestation, suggesting that few, if any, extinctions were overlooked. Certainly, 5 "species" Audubon portrays in The Birds of America (1827-1838) are not members of the current fauna (37). They are small-headed flycatcher (Musicapa minuta), Cuvier's wren (Regulus cuvieri), Blue-mountain warbler (Sylvia montana), carbonated warbler (Sylvia carbonata), and Townsend's bunting (Emberiza townsendi). These birds have puzzled ornithologists and many doubt whether they are true species. Parkes (37) concludes that they are probably hybrids, birds in juvenile plumage, or, in one case, an individual lacking the normal carotenoid pigments. We do not count them in our totals.
With 160 species and a 50% loss of forest, the species-area function (with z = 1/4) predicts -26 extinctions. It is this prediction, some six times greater than the well-documented extinctions, that has caused so much controversy. Does this discrepancy cast doubt on the predictions of species losses from habitat reduction? It does not for two reasons.
The first reason is that not all the 160 species require deciduous or coastal pine forest. In excluding species on the borders of these habitats, we have tried to be conservative. Others might exclude even more species. And while we have excluded species of the grasslands to the west, we still include species of the open areas within these forests. Sixteen species occur only in open habitats, including marshes and farmland, within the region: northern harrier (Circus cyaneus), shorteared owl (Asioflammeus), horned lark (Eremophila alpestris), marsh wren (Cistophorus palustris), sedge wren (Cistophorus platensis), loggerhead shrike (Lanius ludovicianus), red-winged blackbird (Agelaius phoeniceus), yellow-headed blackbird (Xanthocephalus xanthocephalus), eastern meadowlark (Sturnella magna), bobolink (Dolichonyx oryzivorus), lark sparrow (Chondestes grammacus), vesper sparrow (Pooecetes gramineus), savannah sparrow (Passerculus sandwichensis), grasshopper sparrow (Ammodramus savannarum), and Henslow's sparrow (Ammodramus henslowii). The brown-headed cowbird (Moluthrus ater) has thrived on agriculture. Chimney swifts (Chaetura pelagica) and 6 species of swallows feed with equanimity above forests, fields, and even urban areas. Others may wish to exclude these 23 species, and perhaps several other species, such as northern bobwhite (Colinus virginianus), that thrive in early successional forests. There is no undisputed definition of an obligate eastern forest dweller.
Reducing the list to those species found only in mature forests may seem to be special pleading. Certainly, most of the 160 are dependent on forests of some kind. Even ifwe excluded another 23 species from our forest total, we would still predict 22 extinctions (= 16% of 137). This is still five times more than the observed number.
The second, more significant reason is the difference between global and local extinction. Those who point to the small number of observed extinctions in the eastern forests mean global extinctions-species that are lost everywhere (4-6). The predicted number of extinctions is based on the total number of species. However, most of these would not become globally extinct even if all the eastern forests were cleared. Their distribution across, say, the relatively intact boreal forests of Canada makes them invulnerable to forest losses in the United States.
We have not counted the local extinctions in the eastern forests. Typically, no one else has either. We may not feel local extinctions as keenly as global extinctions and thus they are less familiar. There are also three technical reasons why local extinctions are hard to count.
(i) While global extinctions are obvious, local extinctions are not: we do not have range maps for 1620. Certainly, we can document some local extinctions. For example, the peregrine falcon (Falco peregrinus) does not appear in the list of 160 species. Peterson classifies it as extinct in the area we consider, though it has been reintroduced since the publication of his book. An eastern race of the greater prairie chicken (Tympanuchus cupido)-the heath hen-is extinct. In general, our inadequate historical knowledge limits such examples and we will likely underestimate their true number.
(ii) Local extinctions are reversible. Some species will have returned as the forests recovered.
(iii) Even if we had historical range maps, their interpretation would be difficult. Species may persist locally at very low numbers because the flow of individuals from outside the locality can rescue a population otherwise headed for local extinction. With such immigration, a population might last for many decades at a level far below that needed for independent persistence. It is very difficult to answer the question, "What if that flow of immigrants were discontinued?" Equally difficult is to ask, "What would have happened to the 160 species if they were restricted only to the eastern forests-and could not be rescued from outside?" Under such a scenario, quite likely the bald eagle (Haliaeetus leucocephalus), peregrine falcon, northern goshawk (Accipiter gentilis), wild turkey (Meleagris gallopavo), ruffed grouse (Bonasa umbellus), and other large and thus typically uncommon species would have now declined to extinction. (Or else in small and fragmented ranges, their survival would depend on our active intervention.) There are problems enough in predicting the fate of currently endangered species with fragmented ranges (§, ref. 38), without pondering their hypothetical nineteenth century analogs. Rather, we pose a question that we can answer. How many species could become globally extinct if all the eastern forests were felled? This question asks which species are found only in these forests. We have posed this question to many of our colleagues; without exception, the answer has surprised them.
Only 9 species are found almost exclusively in the states that comprise the eastern forests: chuck-will's-widow (Caprimulgus carolinensis), red-cockaded woodpecker, fish crow (Corvus ossifragus), Carolina chickadee (Parus carolinensis), brownheaded nuthatch (Sitta pusilla), yellow-throated warbler (Dendroica dominica), worm-eating warbler (Helmitheros vermivous), Swainson's warbler (Limnothlypis swainsonii), and Bachman's sparrow (Aimophila aestivalis). We estimate that an additional 12 species have >75% of their ranges in the eastern forests: red-bellied woodpecker (Melanerpes carolinus), Acadian flycatcher (Empidonax virescens), wood thrush (Hylocichla mustelina), blue-winged warbler (Vermivora pinus), golden-winged warbler (Vermivora chrysoptera), pine warbler (Dendroica pinus), prairie warbler (Dendroica discolor), cerulean warbler (Dendroica cerulea), prothonotary warbler (Protonotaria citrea), Louisiana waterthrush (Seiurus motacilla), Kentucky warbler (Oporonis formosus), and hooded warbler (Wilsonia citrina). Three more species are mostly eastern in distribution but they penetrate the prairie states in interspersed woodlands: white-eyed vireo (Vireo griseus), yellowthroated vireo (Vireo flavifrons), and scarlet tanager (Piranga olivacea).
Of the extinct species, the warbler and parakeet were strictly eastern forest species, the pigeon ranged to the west, and the woodpecker was once found in Cuba. Depending on whether one adopts a strict or a loose definition of eastern forest species, there were between 11 and 28 species restricted to the region. It is only these species that were at risk of extinction from forest clearing. The possible extinction rates range from 2/11 = 18%, if one defines eastern forest birds strictly, to 4/28 = 14% otherwise. Adding red-cockaded woodpecker to the list (on the grounds that it would go extinct without our intervention) and the numbers become 27% and 18%, respectively.
These data are not the counter example they are claimed to be. Rather, they are in remarkable accord with the predictions of the simple "habitat reduction predicts species loss" theory we have outlined. Indeed, three of the four rates just calculated exceed the prediction of species loss from deforestation (16%). The addition of any one of Aububon's missing birds to the total of extinct species would obviously increase the observed extinction rate. So would the addition of Kirtland's warbleranother species that would surely be extinct without active conservation efforts.
We have one caveat. There are too few species restricted to the eastern forests to calculate an empirical estimate ofz based on them alone. There is no reason to expect a dramatically different value of z for this subset of species, however, (33).