distribution on environmental gradients: theory and a preliminary...

Distribution on Environmental Gradients: Theory and a Preliminary Interpretation ofDistributional Patterns in the Avifauna of the Cordillera Vilcabamba, PeruAuthor(s): John TerborghSource: Ecology, Vol. 52, No. 1 (Jan., 1971), pp. 23-40Published by: Ecological Society of AmericaStable URL: http://www.jstor.org/stable/1934735 .

Accessed: 09/10/2013 13:49

Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .http://www.jstor.org/page/info/about/policies/terms.jsp

.JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range ofcontent in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new formsof scholarship. For more information about JSTOR, please contact [email protected].

.

Ecological Society of America is collaborating with JSTOR to digitize, preserve and extend access to Ecology.

http://www.jstor.org

This content downloaded from 130.239.76.10 on Wed, 9 Oct 2013 13:49:45 PMAll use subject to JSTOR Terms and Conditions

http://www.jstor.org/action/showPublisher?publisherCode=esa

http://www.jstor.org/stable/1934735?origin=JSTOR-pdf

http://www.jstor.org/page/info/about/policies/terms.jsp


DISTRIBUTION ON ENVIRONMENTAL GRADIENTS: THEORY AND A PRELIMINARY INTERPRETATION OF DISTRIBUTIONAL PATTERNS

IN THEX AVIIAAUNA OF THEX CORDILLERA VILCABAM\BA, PERU1

JOHN TERBORG-I-2

Dcpartmnciit of Botany, University of Maryland, College Parke 20742

Abstract. A new theoretical approach to the study of distribution is presented in this paper. The central question concerns the types of interactions between organisms and their surroun(1- ings which may function to impose limits on the occurrence of species on a smooth unifactorial environmental gradient. The theory is constructed of a set of three complementary and mutually exclusive models which arbitrarily are given the power of accounting for all possible listributions. Each of the models predicts a different pattern of distribution within a group ot organisms and each contains twio or more unique features which serve to distinguish it from the others. In their simplest form the models state that the occurrence of species is limited respectively by: (i) physical or biological conditions that vary in parallel with the measured gra(lient, (ii) competitive exclusion and (iii) environmental discontinuities ecotoness). P're- dictions of each model include (a) the shape of population density curves, (b) the shape of congruity (faunal attenuation) curves, (c) distributional patterns at the termini of gradients, and (A ) the form of the frequency distril)ution of ecological amplitudes.

Azlpplication of the theory is demonstrated with data obtained in a study of the (listribution of bird species on a uniform elevational gradient in the Eastern Andes of Peru. A series of four expeditions to the Northern Massif of the Cordillera Vilcabamba, a vast undisturhed mountain xwilderness, provided information on the upper and lower limits of occurrence of over 410 species of forest birds. Faunal composition and the relative abundances of many species wd ere estimated at each of 15 stations through large netted samples of birds (170-604 individuals). Following a protocol described in the text, the upper and lower limits of 261 species wvere assigned to one or another of the three models. Certain limitations of method result in a small number of unavoidable errors in these assignments; hence the outcome of the parti- tioning procedure is only a first approximation. As evaluated by this preliminary analysis. the three mechanisms of distributional limitation differ appreciably in their importance in the Vilcabamba avifauna. Ecotones account for less than 20% of the distributional limits, competitive exclusion for about one-third of the limits and gradually changing conditions along the gradient for about one-half of the limits.

The study of species distributions along environmental gradients has, in the main, been the prov- ince of plant ecologists. The motivation behind their investigations was largely a desire to resolve the long-standing controversy over the commu- nity vs. continuum issue (McIntosh 1967, WVhit- taker 1967). A number of ambitions and me- ticnlonsly conducted projects has fielded a large bodv of detailed information (e.g.. Whittaker 1956, Bray and Curtis 1957, Daubenmiire 1966). But dlisagreement over methods and the interpretation of results, as well as a lack of consistency in findings from different localities, has prevented a satisfactory resolution of the main question. In this paper a new approach to the problem of gradient analysis is offered, one in which the major emphasis is directed towards the interpretation of ecological amplitudes rather than to proving or (lisproving the notion of integrated species asso- ciations in so-called communities.

Virtually any large-scale natural gradient is likely to contain a multiplicity of variables which

1 Received June 1, 1970; accepted July 1, 1970. 2 Present address: Department of Biology, Princeton

University, Princeton, New Jersey 08540.

influence the distributional patterns of plant and animal species. The difficulty of isolating the various concurrent trends has stimulated the de- velopment of a number of elegant but laborious niulticlimensional ordination techniques (e.g. WVil- liams and Lambert 1959, Orloci 1966, Crawford and Wishart 1967). Much of the complexity that has been encountered heretofore in gradient analysis has resulted from two practices: the use of temperate localities, and the use of plants. Aside from their erratic character, temperate climates vary locally in such factors as the length of the growing season, amount and duration of snow cover, etc., while plants are highly sensitive to local conditions of soil, drainage and exposure. and hence are subject to uncontrolled variation in abundance along any major environmental gradient. In the belief that distributional patterns would be relatively simple and obvious if one avoided these two handicaps, the present investigation was undertaken with birds in a nearly non- seasonal tropical locality.

It was decided to work at first on an elevational gradient because of the ease with which position in the physical continuum could be measured.



24 JOHN TERBORGH Ecology, Volume 52, No. 1

Two criteria predominated in the selection of a locality: that the entire span of the gradient be abundantly watered and that it lie wholly within an unbroken sweep of virgin vegetation. Human disturbance with its attendant modification of habitat leads to the introduction of many exotic plants, and often to marked alterations in the ranges of birds (Mayr and Gilliard 1954). After an examination of topographic maps of the Andes, a vast uninhabited mountain region in central Peru was chosen. It is the Northern Massif of the Cordillera Vilcabamba, one of the few Neo- tropical montane regions to have escaped the cur- rent wave of colonization by peasant farmers. Cut off from the central highlands by a high and precipitous range and from the lowlands by cat- aracts in the Apurimac and Urubamba Rivers, an area of more than 20,000 km2 remains to this day in a pristine state of nature. Accounts of the geography and exploration of the region have ap- peared recently in various publications (Bakeland 1964, Paddock 1967, Terborgh 1968, Terborgh and Dudley 1970).

THE GRADIENT: ITS PHYSICAL AND

BIOLOGICAL FEATURES

Entry into the Apurimac Valley is now easily gained via a road that was completed in 1963 to Puerto San Francisco del Apurimac. A base of operations for four expeditions was graciously provided at Hacienda Luisiana by its owner, Jose Parodi. Luisiana is conveniently situated on the west bank of the Apurimac at a point where the linear distance from the river to the crest of the Vilcabamba is minimal (ca. 12?39' S, 73?44' W). At the time of our expeditions one entered wilder- ness on leaving the east bank of the Apurimac. From there it was necessary to search out useable routes and cut trail in order to advance and gain elevation.

Our first season in the region (1965) was passed at Luisiana where we familiarized ourselves with a bewilderingly rich flora and fauna and made plans for an assault on the Vilcabamba. On enter- ing the Cordillera in 1966 we encountered for the first time nearly 200 additional bird species and so progressed slowly, reaching the level of 2,500 m. Two more expeditions in 1967 and 1968 carried us to the crest of the range and saw the comple- tion of the floral and faunal survey of the transect. The distance covered was about 40 kilometers and encompassed an elevational differential of 3,000 m. A chain of nine bush camps, more or less evenly spaced with respect to elevation, gave ready access to all levels on the mountain. Every camp was occupied for at least 2 weeks and some were visited on 3 years for cumulative periods of a month

22 , 1

20 -

D 18 SLOPE= -0.56? PER 100 m

At 16

1~ 4 H 22

E2 o 0

(D 6 z < 4

2

500 1000 1500 2000 2500 3000 3500 ELEVATION (METERS)

FIG. 1. Mean 0600 temperature as a function of elevation in the northern Cordillera Vilcabamba, Peru. The gradient is 0.56<C per 100 m change in elevation.

or more. The schedules of the last two expeditions were arranged so that the amount of time spent at the various levels was equitably distributed. Stated elevations are mean altimeter values for each station amended by temperature corrections based on the international standard atmosphere.

Climate.-Temperature is the climatic variable most closely associated with elevation (Fig. 1). Diurnal fluctuation in the shade of the forest was roughly 50C at most camps. Differences in cloud cover produced more variation in maximum than in minimum temperatures. Dawn readings at any camp seldom digressed more than ? 0.60C from the mean. We have no data on seasonal trends in mean temperature but records from other localities at about the same latitude indicate that the maximum disparity between monthly means should fall within 3?C (Richards 1952, Janzen 1967). Every year we experienced one or two southerly storms in July or early August during which the temperature fell as much as 80 below normal for a day or two. These were generally accompanied by heavy rain and strong winds and probably constituted the most extreme weather of the year.

Rainfall records for the Cordillera Vilcabamba simply do not exist. The best indication of local conditions comes from Pichari in the Apurimac Valley about 30 km north of Luisiana where annual precipitation is reputedly 3 m. Much of this falls in the December to March rainy season but heavy rains are commonplace at all times of year. Even during the June to August dry season it is seldom that as much as 2 weeks passes without a soaking shower. Year-round avail- ability of soil moisture is attested by a paucity of deciduous trees.

Above 1,500 m in the Cordillera Vilcabamba



Winter 1971 DISTRIBUTION OF PERUVIAN BIRDS 25 rains are very frequent at all times of year to the extent that a succession of 3 dry days is note- worthy. Near the crest of the range hail, sleet or off-and-on showers are the daily routine. As- sociated with such a high frequency of precipitation is an increased degree of cloud cover, particularly during the daylight hours. Upwards of 3,000 m, an uninterrupted hour of sunshine after 0900 is a depressingly rare occurence. Lacking more explicit information we can assert only that the entire gradient receives an abundance of moisture on a year-round basis. It is also clear that daytime humidity and cloudiness are positively correlated with elevation.

Anyone accustomed to the weather of the temperate zone is likely to be impressed by the wind- lessness of the tropics. In our experience strong breezes accompanied the passage of thunder storms and southerly storms. Otherwise the movement of air was seldom rapid enough to flutter leaves and then usually insufficient to stimulate an ane- mometer capable of registering a velocity of 2 mph. These observations apply to all elevations and discount the possibility that exposure to wind is a significant variable on the gradient.

Zonation of vegetation Anyone who were to walk our transect would

not fail to notice a striking zonation of forest types which differ both in physiognomy and composition. In considering the possible interactions of vegetation and bird distribution we shall distinguish what appear to be the four principal vegetation types, while recognizing that for other purposes a plant ecologist might wish to divide the whole into many more parts. It is important to emphasize that the four zones can be distin- guished on the basis of physiognomy alone, so that analogous zones may be discerned in another locality having an entirely different flora. Of further consequence is that in the Cordillera Vilca- bamba, and at other localities we have visited, the interfaces between zones are sharply defined and except for the lowest, are notably unaffected by topographic conditions (e.g., ridge tops, slopes, ravines). The elevation at which a particular boundary (ecotone) occurs, however, may vary widely on different mountain ranges in accordance with local conditions.

Lowland rainforest.-With the exception of the river floodplain, which has a distinct flora and fauna, the natural vegetation of the Apurimac Valley floor is tall rainforest (Terborgh and Weske 1969). In relation to montane vegetation its most notable feature is an abundance of giant trees, many of which attain a diameter of 3 m or more and heights of 50 to 60 m. The understory

is sparse and open and contains many ferns, arums and Cyclanthaceae. Lianes are abundant in the middle and upper tiers of the forest while epiphytes are numerous only on the branches of old trees.

Montane rainforest.-Opposite Luisiana the slopes of the Cordillera Vilcabamba pitch abruptly into the valley floor at an elevation of 650 m. Eco- logical conditions on the slopes are sufficiently distinct that the entire stratum of giant emergents (the A story of Richards 1952) drops out at this juncture. Trees composing the upper canopy of montane rainforest are of more uniform stature, rarely exceeding 35 m in height and 1 m in diameter. Perhaps because of the lower canopy, the understory is noticeably more dense than that of lowland rainforest. Tree ferns suddenly appear in abundance and grasses of various kinds become prominent in the foliage near the ground. Epiphytes are not conspicuously more numerous than in the lowland forests. For the purposes of this investigation the two forest types are distin- guished by the presence or absence of large trees (> 50 m).

Cloud forest.-An extremely regular weather pattern in the Apurimac Valley results in the daily formation of the dew point at a nearly constant elevation. From this level (1,380 m) upwards to the summit ridge, the slopes of the range are inter- mittently bathed in slowly rising clouds. Often the clouds are so thick as to obscure the tops of trees from the ground and wet enough to produce a fine soaking mist. Below the 1,380-m level the forest canopy is rarely if ever immersed in clouds by day, though predawn mists are frequent. Consequently there is at this point an abrupt discontinuity in the canopy environment, coincident with which is an ecotone of such contrast as to be obvious to the unsophisticated eye. Epiphytes of many families crowd the branches of the taller trees and dense thickets of climbing bamboo (Chusquea spp.) bar passage through the understory. An acidic mat of leaf litter and humus accumulates above a layer of compacted soil. Of several possible criteria, the appearance of thick moss jackets on the trunks of most trees is the one which we consider to be the best diagnostic indicator of the lower limit of cloud forest (Fig. 2).

Monte chico.-In climbing the Andes, or for that matter, other humid tropical mountains, one eventually passes from tall forest into a contracted elfin forest, which in Peru is called "monte chico." The transition is usually abrupt, though the elevation at which it occurs varies greatly from one mountain system to another. In the Cordillera Vilcabamba this ecotone lies at about 2,550 m, the exact level being somewhat lower on ridges than on gently dipping slopes. Our criterion for



26 JOHN TERBORGH Ecoloyv. Volume 52. No. I

FIG. 2. View of the epiphyte-laden canopy of the upper cloud forest at ca. 2,400 m. Among the plants visible are mosses, lichens, ferns, orchids, bromeliads and ericaceous epiphytes.

monte chico is the absence of trees taller than 15 m, though several other features deserve mention. There is a striking tendency toward microphyllous foliage especially at the upper reaches near timberline. The trees and shrubs are densely branched with short internodes and petioles and present a compact outline. Ericaceae, Compositae and Orchidaceae are among the more prominent plant families. A number of species and genera which are epiphytic in cloud forest grow freely on the deep accumulation of sphagnum that carpets the ground in the monte chico zone. Except on sharp ridges and steep slopes the soil is overlain by an acidic peat layer that varies between 0.3 and 1.3 mr in thickness.

Above 3,000 m in the Cordillera Vilcabamba monte chico gives way increasingly to patches of tall grassland so that the vegetation comprises an irregular mosaic (Fig. 3). For this reason the timberline transition from arborescent vegetation to pure grassland is ill defined in many places. Only along the exposed crest of the range at elevations greater than 3,500 m is one clearly above the limit of trees.

OFTI.

Al ..e +~~~~~~~~~~~~~~~~~~~~~~~~~~~~~P

FIG. 3. A portion of the net line along the summit ridge of the Cordillera Vilcabamba at ca. 3,500 m. A nearly invisible net runs across the picture and is sus- pended from an upright pole at the lower right. Notice the tall grass understory, low scattered trees and compact microphyllous foliage.

In lieu of specific measurements, an anecdotal account will have to suffice as evidence of extremely low plant productivity in the alpine grassland. In August 1967 a party of three expedition members made a hike along the summit ridge through waist-high grass. As the grass easily yielded before us it was not necessary to use a machete to open the way. Nearly a year later, in July 1968, we returned to the same ridge and were startled to find our track still clearly visible. The grass remained parted and pressed down just as we had left it, and nothing had grown up to fill the space.

THEORY

Given the setting described above, that of a sharply zoned vegetation superimposed on a con- tinous physical gradient, one may inquire into the various factors that may enter into the determination of animal distributions. In this section we shall examine the implications of three plausible mechanisms, each of which has been evoked by other authors in less explicit form in attempts to explain particular distributional limits. Each mechanism is mutually exclusive of the other two and the three are complementary. \Vhile it is



Winter 1971 DISTRIBUTION OF PERUVIAN BIRDS 27

possible to think of other models to add to the set, in practice we have found it necessary to limit the number to three and to treat them in such a way as to include all observed distributions within their scope. The manner in which this is accomplished will be explained at an appropriate place later in the paper.

A simple statement can express the premise that underlies each model. The statements carry a number of implications which can be deduced logically or graphically. The set of implications that follows from each statement is unique; that is, the sum of the implications that forms any single model predicts a pattern of distribution that is distinguishable on one or more grounds from the patterns predicted by the other models. An exposition of the models follows seriatim.

Model I. Distributional limits of species on a gradient are determined by factors in the physical or biological environment that vary continuously and in parallel with the gradient.-Implicit in this statement are the absence of exclusion reactions between competing species and effects of discontinuities in the habitat, i.e., ecotones. Each species will show a characteristic optimum position on the gradient where it reaches maximum abundance. On either side of the optimum, abundance will decline more or less rapidly depending on the ecological amplitude of the species. Since optima will fall at random on the gradient, faunal turnover will be highly regular and will be determined only by the mean ecological amplitude of the several species present (Fig. 4a). A derivation of the form of what shall be called the congruity curve is given in the appendix. By eco-

logical amplitude we mean the range of conditions included within the limits of a species' occurrence on an environmental gradient, as measured in units of the gradient variable. For example, when the gradient is one of elevation, a species that is found between 1,500 and 2,500 m has an amplitude equal to 1,000 m.

Included within the scope of this model are all relevant features of the environment that vary in the specified manner with the gradient (elevation). These features may be physical, such as temperature, degree of cloudiness, etc., or biological. Of the many conceivably important biological variables, we can offer as examples three that appear to us to vary in the correct manner with elevation: 1) net annual plant productivity, 2) density of insects and 3) importance of epiphytic plants in the vegetation. The first and second of these decrease and the third increases upwards on the gradient.

Model II. Distributional limits of species are determined by competitive exclusion.-This model is simply a restatement of the Gaussian theorem as applied to spatial distributions. When the ecological requirements of closely related species are sufficiently similar, their coexistence will be unstable and their populations will be forced to occupy mutually exclusive domains (Fig. 4b). The abundances of two such species will fall off sharply in the zone of contact instead of trailing off gradually as is implied by the first model. We shall refer to the resulting truncation of the population density curves as a repulsion interaction. The points on a gradient at which excluding species meet will fall at ecotones only coincidentally.

MODEL I 100

z z w~~~~~~~

0 0 z 1

4W

z~~~~~~

GRAD I ENT : GRADI ENT FIG. 4a. Properties of model I. The left-hand drawing illustrates that the abundances of

different species and their ecological amplitudes on an environmental gradient are independent of one another. The righthand drawing portrays the expected random or smooth turnover of species along the gradient. Each "congruity curve" represents the degree of faunal sim- ilarity found in samples taken at higher and lower values of the gradient in comparison to a central or reference sample (see the Appendix for further explanation).




MODEL II

100

wI ccG I z ow z a

Im M~~~~~~~~~~~~~~~~~~L

C

FIG. 4b. Properties of model II. Population density curves are truncated where competitors meet (repulsion interaction). Mean amplitude of the species in replacing series of three is less than that of species in series of two (amplitude compression). Since species are expected to replace each other at random points along the gradient, smooth congruity curves are predicted.

Hence the turnover in a whole fauna will be random and give rise to smooth congruity curves. Closely related species may replace one another sequentially in series of two, three or more. Mu- tual exclusion on a gradient must eventually lead to crowding in the larger series since all natural gradients encompass a finite range of conditions. Because of this spatial restriction, the amplitudes of species in the larger series should, on the average, be reduced in relation to species that are not repulsed by an adjacent competitor. This effect will be termed amplitude compression.

The reader may have noticed that the construc- tion of this model is based on an extremely narrow concept of competition. Only a single type of interaction is included; that which leads to spatial exclusion of congeneric species. While this is an important and easily recognized form of competition, it is but one of many possible kinds of competitive interactions (in the broadest sense) that could restrict a species' ecological amplitude.

A form of competition which is undoubtedly of importance, especially in diverse tropical faunas, may be termed diffuse competition: that which comes from all related and nonrelated coexisting species that share a common pool of limited re- sources (Terborgh and Diamond 1970). Further, the more relaxed definitions of biological competition encompass most types of interspecific interactions, including predation and parasitism. Pres- ence of the latter sorts of competitors on an environmental gradient could confine a species to the region of maximum fitness near its environmental optimum. Wherever diffuse competition

or the inroads of predators or parasites is more intense at one end of a species' amplitude than at the other end, it could lead to truncation of the abundance curve towards the former end.

Since, at the empirical level, it is difficult at best to implicate these kinds of interactions as probable causal mechanisms in limiting the distributions of species, we have found it necessary to exclude them from the competition model as presently constituted. Where distributional limits are imposed by the effects of one of these kinds of interaction, the instances will not be discriminated by our criteria and in practice will be relegated to one of the other two models, usually Model I. The problem of surmounting some of these weaknesses of the competition model will be the subject of future papers.

Model III. Distributional limits are determined by habitat discontinuities (ecotones).-If the spread of species populations is blocked by habitat discontinuities there will be massive faunal turnover at ecotones. Were all the species on a gradient so constrained, the faunal congruity curves would be nearly flat except at ecotones where sharp breaks would occur (Fig. 4c). Population density curves would thus tend to assume a square wave shape since available evidence indicates that the total density of individuals is nearly constant across ecotones.

A resume of the properties and implications of these models is given in Table 1. Species whose distributions are restricted by competitive exclusion are predicted to be replaced abruptly by congeners, and to show repulsion interactions and




MODEL mI l00 I lEcOTONE ECOTONE:

z ~~~~~~~z Z 0 W

m z~~~~~~~~~~ 4 IL~~~~~~~~~~~.

* GRADIENT E * GRADIENT - FIG. 4c. Properties of model III. Population density curves are sharply truncated at eco-

tones, giving rise to square-wave rather than bell-shaped curves. High rates of species turnover at ecotones produce steep, nearly discontinuous congruity curves.

TABLE 1. Predictions of three models of species distribution on environmental gradients. Predictions unique to the given model are in italics

Model

Distributional feature Gradient Competition Ecotone

1. Population density curve.? normal repulsion interaction truncation 2. Mutual exclusion .none &es none 3. Amplitude compression .none yes none 4. Congruity curves .smooth, symmetrical smooth, symmetrical dicontinuous 5. Amplitude distribution curve .? normal skewed right variable 6. No species near terminus .reduced not reduced not reduced 7. Species loss near terminus .not reduced reduced reduced 8. Species gain near terminus .reduced reduced reduced 9. Mean amplitude near terminus ....... ............... reduced constant constant

amplitude compression, all features unique to the competition model. Where ecotones impose an insurmountable ecological barrier, the population density curves of the affected species should be truncated at the ecotones, and if appreciable num- bers of species are involved the faunal congruity curves will contain conspicuous discontinuities. These predictions establish criteria by which species responding in accordance with two of the models can be recognized. For the time being the remaining model will have to serve as a repository for all data that is not explained by the other two. Thus we recognize that the present scheme yields only a first approximation to a complete solution to the interpretation of distributions.

The ecological amplitudes of the species inhabiting a gradient can often be expressed in terms of some convenient unit e.g., meters of elevation or depth, parts per thousand of salinity, etc. When the distributions of all the species in a group are known, their ecological amplitudes can be plotted as a frequency diagram (cf. Fig. 5). Contempla-

tion of the three models leads to the conclusion that each predicts a different frequency plot. The amplitudes of species that are responding only to the gradual change in conditions along a gradient will cluster approximately normally about the mean value as each species is similarly exposed to the opportunity of expanding into regions of higher and lower intensity of the controlling factor. The extent to which any species may become specialized or generalized with respect to any one gradient, however, is subject to obvious limitations. Exces- sive specialization that leads to a very narrow amplitude must increasingly expose the population to the risk of extinction. Stochastic fluctuations in population density will impose an ultimate limit on specialization. Empirically we find that this limit falls between 100 and 200 vertical meters for the species-rich Vilcabamba avifauna. At the opposite end of the adaptational spectrum is found the extreme generalist. Provided that successful existence at different points on a gradient requires some degree of divergent adaptation, the maximum




extent to which any interbreeding population may enlarge its distribution will be regulated by the rate of gene flow within the population. This, in turn, is dependent on a number of factors of which the most important is a species' dispersal tendency. The amount of adaptation required for an incre- ment of increase in amplitude may also be expected to vary. For a few species such as swifts which freely use the airspace over the entire 3,000-m Vilcabamba slope, the gradient poses no great adaptational challenge. For the great majority, however, it does, as we note in the fact that only a handful of species occurs over an elevational differential of more than 2,000 m. Since diametri- cally opposed evolutionary strategies appear to be involved in the determination of ecological amplitude in species responding to a gradient, a high variance in amplitude is to be anticipated.

Within a group of species whose distributional limits are prescribed by competitive exclusion interactions, the frequency distribution of amplitudes could take on a variety of forms, but whenever there are a number of compressed species the curve will be skewed to the right. There is no predicting the form of the amplitude distribution curve of species limited by ecotones since these boundaries may fall at any point on a gradient.

Although the remaining predictions included in Table 1 have so far been of little use in practice, we include them for their intrinsic theoretical interest. Heretofore we have regarded gradients as continua, and so they may be treated in their middle sections, but we shall now consider the reper- cussions of their eventual termination. To species responding to ecotones, a terminus is simply another ecotone and has no special significance.

Series of mutually excluding species, whose members are compressed within the confines of a limited gradient, represent another trivial case because the termini effectively act as unbreachable ecotones. However, some distinctive patterns can be expected in a set of species whose distributional limits are determined by the gradient itself, because of the disadvantage of possessing an environmental optimum that lies close to a terminus. Adaptation to an extreme position on a gradient implies a truncated amplitude and hence an increased probability of extinction. From this rea- soning we may infer that the number of species present will decline somewhat towards a terminus and that the number of additional species encountered will fall to zero before the terminus is reached. Since it is likely that a few species will persist near termini in spite of somewhat truncated amplitudes, the fauna inhabiting the imme- diate vicinity of a terminus might show a slightly reduced mean amplitude. Species loss should con-

28

24 -

20 2

to 16- W

0~ O12

0 z

8

4

0 0 1Q00 2000o 3000

AMPLITUDE (METERS) FIG. 5. Frequency distribution of elevational ampli-

tudes of 207 species in the montane avifauna of the Cor- dillera Vilcabamba, Peru. Data are included only for species whose upper and lower limits are adequately known and which do not occur on the Apurimac Valley floor. The mean amplitude is 741 m. Strong indications of more than one peak in the frequency distribution sug- gest that two, three or possibly more separate mechanisms are involved in its determination.

tinue unabated up to any terminus for there is no direct way in which a gradient-dependent population could be influenced by an extralimital boundary.

RESULTS AND DISCUSSION

Testing of the stated predictions of the models requires two kinds of data: (i) quantitative mea- sures of the abundances of individual species at different points on a gradient and (ii) knowledge of the entire fauna at several points so that congruity curves may be constructed. In dealing with birds, observational data such as song censuses and sight records may be used, although a more ob- jective method is desirable for greater consistency and reduced bias, especially in estimating abundances. For this reason, the results that follow have been obtained largely through the use of mist nets. These devices capture a random sample (for any given species) of birds flying in the airspace between 0.2 and 2.0 m above the ground. The four Vilcabamba expeditions have exploited this technique to obtain large samples of birds at 15 levels on the transect (Table 2).

Since the ecotone model of species distribution uniquely predicts discontinuities in faunal congruity curves, we may begin the inquiry by exam- ining curves based on net samples taken at 11 elevations (Fig. 6). Each curve represents the attenuation of the fauna contained in a sample of 219 to 300 birds as measured by samples captured




TABLE 2. Size and elevation of niist net samples

Median elevation Year and number of birds captured of net line (meters) 1965 1966 1967 1968 Total

585 185 99 284 685 273 273 930 212 198 194 604

1,350 370 370 1,520 293 125 418 1,730 181 135 316 1,835 114 145 259 2,095 206 206 2,145 169 159 136 464 2,215 170 170 2,640 245 194 439 2,840 302 149 451 3,220 101 76 177 3,300 168 143 311 3,510 219 219

Total 185 1,143 1,969 1,664 4,961

above and/or below the sample in question. Ex- trapolation of the curves shows a faunal congruity of about 82% at the levels of the 11 samples against which the comparisons were made. Less than 100% congruity is obtained because a sample of 300 does not include all the potentially nettable species at any elevation on the transect. In only one set of net lanes (at 930 m) did we succeed in accumulating a sample of over 600 birds, enough to permit a check of the extrapolated values by a determination of the congruity in two independent samples of 300 from the same location. The agreement, as can be seen in Figure 6, is entirely satisfactory, indicating that the extrapolations pro- vide fair approximations of the true shapes of the curves.

Inspection of the empirical curves reveals a consistent smoothness and symmetry, in accord with the predictions of models I and II. The only exception to constant or slightly concave slopes is found between 585 and 685 m across the lowland to montane rainforest ecotone. It is still unclear to us why the only resolvable ecotone effect should come at a point where the vegetational change affects mainly the upper canopy, rather than the understory from which the samples were captured. A second notable result is a trend towards reduced slopes on both the uphill and downhill sides of the curves representing the samples taken at higher elevations. An interpretation of this will be attempted later.

As most of the sampling stations were separated by vertical distances of 200-500 m, the possibility remained that ecotone effects were being blurred as an artifact of the low sampling density. Hence we undertook a thorough investigation of one ecotone; that at which montane rainforest and cloud forest meet. The bird faunas through and on both sides of the transition were sampled with a long net line that ran continuously between the elevations of 1,270 and 1,540 m. The catch of 663 birds was divided into four nearly equal samples, two above and two below the 1,380-m boundary. Congruity curves based on these data are as smooth as those based on more widely spaced samples, and confirm the lack of any faunal discontinuity coincident with the ecotone (Fig. 7).

A more sensitive test for faunal perturbations on a gradient can be devised from the information contained in congruity curves. One simply mea- sures the slopes of a set of such curves on both

500100102002030030

80

z 4

Li-

500 1000 1500 2000 2500 3000 3500 ELEVATION (METERS)

FIG. 6. Faunal congruity curves on the elevational gradient of the Cordillera Vilcabamba, Peru. Samples of approximately 300 birds were taken at each of eleven elevations. Each curve is constructed by comparing the faunal lists of all other samples to the list of a reference sample which represents the peak of the curve. To compute the points, the number of species each sample contains in common with the reference sample is divided by the total number of species in the reference sample and converted to a percentage. Duplicate samples at 930 m had 82% of species in common, so this is assumed to be the faunal congruity that would be found for duplicate samples at all elevations. Hence, all the curves peak at 82% for the reference elevation, but these extrapolated peaks are shown as dashed lines.




100 ,LOWER LIMIT OF

CLOUD FOREST

z

:2 i

0

500 1000 1500 2000 ELEVATIO N ( METERS )

FIG. 7. Faunal congruity curves based on samples closely spaced about the lower limit of cloud forest in the Cordillera Vilcabamba, Peru.

the uphill and downhill sides at some given level of congruity (we used 50%), and notes the corre- sponding elevations by projecting the points onto the abscissa. A plot of these data is analogous to a derivative spectrum and serves to scan the entire gradient for irregularities in the faunal turnover rate (Fig. 8). Advancing upwards from the valley floor, the species gain (upper half of the figure) reaches 3% per 10 vertical meters in the vicinity of the lowermost ecotone and then quickly settles down to a nearly constant 1 % per 10 m. Perhaps as a consequence of the abrupt appearance of a number of species at 600 m, the rate of species loss is noticeably reduced between 750 and 1,100 m (lower half of the figure). A small and possibly insignificant increase in the rate of species loss coincident with the lower limit of cloud forest (-1.3% vs. an average of ca. -1.0%) may reflect a slight ecotone effect. Above 2,000 m the loss and gain rates drop somewhat below 1.0% and appear to decrease slowly towards timberline. This last result will be taken up again after further relevant information has been introduced.

With the single exception of the few species involved in the high gain rate at the lowland- montane rainforest transition, it can be concluded that faunal turnover is continuous with elevation and hence that the ecotone model can account for the distributional limits of only a minor fraction of the bird species present in the Cordillera Vil- cabamba.

We shall now turn to a consideration of evidence that pertains to the pattern prescribed by the com-

petition model. Distributions which terminate because of competitive exclusion interactions ought to conform with the following three predictions: (i) mutual exclusion of congeners in linear series along the gradient, (ii) repulsion interactions, and (iii) amplitude compression in the larger series.

The first prediction is abundantly fulfilled by data of the kind shown in Figure 9. The forest- dwelling avifauna of the Cordillera Vilcabamba and Apurimac Valley floor (exclusive of all mator- ral species which do not enter into these results, see Terborgh and Weske 1969) amounts to somewhat more than 410 species. Of these, at least 180 (44%) are met without overlap, either above or below or on both sides by congeners. Exclusion interactions involve pairs (> 50), triplets (16) and quartets (6) of species. These series fall into 68 genera and 29 families, revealing a wide- spread evolutionary pattern in Andean birds. Ele- vational segregation of congeners has also been shown to occur on a large scale in the avifauna of the New Guinea highlands (Diamond 1969).

While in the midst of charting distributions in the field we became puzzled by apparent gaps between certain pairs of replacing species. A number of these are shown in the examples included in Figure 9. Some are surely due to experimental error while others were upheld by strenuous but unsuccessful efforts to find either species in the unoccupied zone. The large hiatus indicated between Grallaria erythroleuca and G. rufula is likely to be in error because Grallarias are notoriously difficult to observe and rarely enter nets. On the




+ 3.0 1LW 2 LOWER o LIMIT OF F-LOWER LIMIT '-LOWER LIMIT

MONTANE I OF I OF RAIN FOREST CLOUD FOREST MONTE CHICO

I I o I II

z no

elvton in thIodleaVlaabPr.Pit

Z I

tI .0 - ~ I

<c t s

c-I.0 I

500 1000 1500 2000 2500 3000 ELEVATION (METERS)

FIG. 8. Rates of faunal attenuation as a function of elevation in the Cordillera Vilcabamba, Peru. Points indicate the slopes of the congruity curves in Figure 6 at the 50% congruity level. Species gain with elevation is shown in the upper part of the figure (positive values) and species loss is shown in the lower part. These cor- respond, respectively, to the downhill and uphill halves of the congruity curves.

other hand, the narrow gap between the two Myioborus warblers is probably real, or at least represents a zone of great scarcity, for both are abundant and conspicuous where present. We do not wish to delve into the possible interpretations of this phenomenon for the time being, yet it de- serves mention for its novel implications. R. H. MacArthur has devised a theoretical scheme which predicts that competing species in a continuum will be separated by vacant zones under certain conditions (pers. commun.).

Especially favorable circumstances are required to demonstrate repulsion interactions between replacing congeners. The species must both be common and efficiently netted. Yet in a majority of the cases for which suitable data are available, the population density curves are conspicuously truncated on the side(s) towards an excluding congener (Figs. 10, 11 and 12). Generalizing from the examples for which sufficiently detailed information is at hand, it appears that repulsion interactions are a frequent but not universal corollary of mutual exclusion.

Arguments in support of the notion of compe-

Coeligena (Trochilidae) C. coeligena C. violifer

E. Eubucco (Capitonidae) richardsoni

mav E. versicolor. Veniliornis (Picidae)

Vaffinis V. di nis V. nigriceps

X. gutta- Xiphorhynchus (Dendrocolaptidae) tus, X.ocellatuiz 1111111 111ri X. triangularis

Thripadectes (Furnariidae) T. melanorh nchus T. holostictus T. scrutator

1 - ~~~11,1111111111111111111"1111111111 HIM11111 G erythro- Grallaria (Formicariidae) / leuca

G. guatemalensis G. Suamigera /

Scytalopus (Rhinocryptidae) G. rufula S. femoralis S. unicolor

Cacicus (Icteridae) C.holoseri- C. cela C. uropygialis ovC. leucorhamphus ceus-

Myioborus (Parulidae) M. miniatus M. melanocenha us_

Iridisornis (Thraupidae) I. analis I. reinhardti

600 1000 1400 1800 2200 2600 3000 3400 ELEVATION (METERS)

FIG. 9. Elevational replacement of congeneric species in 10 families of birds. Series of two, three and four replacing species are represented. Note the apparent hiatuses between some pairs of species and the consistency with which the uppermost species possesses the broadest amplitude.

tition between closely related species in nature are more often based on circumstantial fact than on tested hypotheses. Exclusion on a gradient, for example, is often put forth as confirming evidence, but it may be merely circumstantial and falls short of proving the case. Of the three explicit predictions of the competition model, that of amplitude compression is the one that most rigorously upholds the assumption of a state of tension between populations. It offers the only possibility for a direct comparison of sets of species that are presumed to be in competition with a set that is presumed not to be, or at least to a lesser degree.

If competition were the only factor to limit distributions then one could expect species which lacked competitors to occupy the entire gradient and those which formed excluding series to show reduced amplitudes in accordance with the length of the series. In such a case the amount of amplitude compression would be in strict proportion to the length of the excluding series. Obviously the real world is not so simple, for only five species span the entire gradient and fewer than two dozen




0.331 H-ECOTONE I 0.06 2. 3 MANAKINS

1. Pipra fasciicauda /.05 \ /2. Pipra chloromeros

0.05 _ / \ / \ 3. Pipra pipra 4. Machaeropterus

pyrocephalus w 0.04 5. Pipra caeruleocapilla z 4.. 5.

ZO0.03 1 m I Ar

0.02,

0.011

5010 500 2000 ELEVATION (METERS)

FIG. 10. Population density curves for species in the family Pipridae (Manakins). The ordinate represents the fractional abundance of the species in net samples. Species 1, 2 and 3 are of nearly equal size and distinctly larger than species 4 and 5. The large species show some overlap but this is due entirely to individuals in female or juvenile plumage. There is an hiatus between the two small species which taxonomists place in separate genera.

fill even half of it. The mean amplitude for all 207 species whose limits are well known and do not reach the lower terminus is 741 m (Table 3). These are the species whose amplitudes are por- trayed in Figure 5. Species occurring on the valley floor are excluded because their amplitudes are arbitrarily truncated at 585 m; the real terminus is at sea level. Taking 741 m as a standard amplitude it could then be argued that competition alone should not lead to compression in series of fewer than four species, because nearly four of the standard amplitudes can be accommodated in a 3,000-m gradient. We may thus draw two con- clusions from the data presented in Table 3: (i) Strong compression is apparent, even in series of two, but only in the lower-altitude members of the series and (ii) the members of excluding series are not able to spread at will along the gradient to achieve a compressionless accommodation.

T-tests of the significance of differences between the means of various groups of species yield the following results(Table 4):

1) Uppermost members of the three- and fourfold series possess significantly greater amplitudes than lower members, but the difference is not significant for twofold series. Evidence for a general

trend towards expanded amplitudes in the upper half of the gradient has already been presented. By breaking the fauna into subsets it becomes clear that both monotypic forms and the uppermost members of replacing series contribute to the phenomenon detected in the congruity curves. (We use monotypic here in the restricted context of the Vilcabamba fauna for species having no congeners present on the gradient.) The mean amplitude of 16 monotypic species whose upper limits lie above 3,000 m is 1,348 m while that of 18 monotypic species whose upper limits lie between 2,000 and 3,000 m is only 815 m. The difference is significant at the 0.001 level. Consideration of the possible meaning of these results will be taken up at a later point.

2) Amplitudes of the lower members of series are all significantly reduced in comparison with the mean of monotypic species, but there are no significant differences between the set of monotypic species and the sets of uppermost species.

3) Lower members of two-fold series possess significantly greater amplitudes than the lower members of three- and four-fold series, but the means of lower members of the three- and fourfold series are not significantly different.




0.05 k-ECOTONE FLYCATCHERS 2.

I. L.amaurocephalus

0.04 I.2. L. superciliaris

0.04 p4. 5.z 3. L. taczanowskii

F 1ne 4. P. pelzelni z I of .03 spe5. P. ruf iceps

z I :D

'< 0.02 I *ECOT0 NE

0.01

0.00 I- - J

500 1000 1500 2000 2500 3000 ELEVATION (METERS)

FIG. 11. Population density curves for species in family Tyran~nidae (Flycatchers). Species 1 and 2 overlap broadly, but 2 reaches maximum abundance in the absence of 1. Both 1 and 2 appear abruptly above the lowland-montane rainforest ecotone. Truncation of the curves (repulsion interaction) is apparent in the zones of replacement of species 2 and 3 and of species 4 and 5. The genera are Leptofogon~ and Pseudotriccus.

The latter two findings substantiate the existence of amplitude compression in the lower members of series of replacing congeners. As the competition model predicts, the compression is pro- gressive, but because few of the series have expanded to fill the entire gradient the degree of compression is less than proportional to the length of the series. It is of interest to note that the compression experienced by the lower members of fourfold series (56%) restricts their amplitude, and hence mean population size, to less than half of that of species having no obvious competitors in the fauna. If it is presumed that the probability of extinction is increased by reduced amplitude, then it is clear (i) why the number of series drops off rapidly with increasing length and (ii) why there are no series containing more than four members. (Parenthetically, it should be mentioned that a fivefold series in Grallaria is probable in other localities where G. andicola lives in scattered patches of brushwood at elevations around 4,000 m.)

Of the three models that were proposed to account for species distributions on environmental gradients, we have considered evidence pertaining to two: the ecotone and competition models. Un-

fortunately the gradient model offers no means of directly and unequivocally identifying species whose limits conform to its precepts. However, if the distributional limits that concur with the features of the other two models can be identified, the remaining limits, by default, can be assigned to the gradient model.

With these limitations of method in mind, it will be of interest to partition the upper and lower limits of netted bird species in accordance with the following procedure. (i) Distributions that extend to either the upper or lower terminus of the gradient cannot be assigned to any of the models and hence are set aside. (ii) Limits that, within 10 vertical meters, coincide with one of the three above-mentioned ecotones have been assigned to that model. Examples are the lower limits of Leptopogon atmaurocephalus and L. superciliaris (Fig. 11 ) and the lower limit of Basileuterus coronatus (Fig. 12). (iii) Limits which lie at the boundary between two replacing congeners, whether or not they are separated by an hiatus, have been assigned to the competition model. (iv) In view of the general paucity of ecotone effects, congener pairs that happen to meet at ecotones have been presumed to do so coincidentally




WARBLERS 4

0.08 1. B. rivularis

2. B. chrysogaster 5.

3. B. tristriatus 3.

0.06 4. B. coronatus w 0 5. B. luteoviridis

z 0 z M 0.04

< ECOTONE-

I.

0.02 2.

0.00 - A 500 1000 1500 2000 2500 3000 3500

ELEVATION (METERS) FIG. 12. Population density curves for species in the genus Basileuterus, Parulidae (War-

blers). Species 1 and 2 overlap but are of different size, occupy different habitats and forage at different levels in the vegetation. Species 2, 3 and 5 replace each other without overlap, while species 4, which differs in size from both 3 and 5, reaches maximum abundance in the replacement zone. Notice that the lower limit of species 4 coincides with the ecotone.

and accordingly have been assigned to the competition model. (v) All remaining limits are arbitrarily assigned to the gradient model.

The outcome of this procedure reveals that the three presumed mechanisms of amplitude determination differ appreciably in their importance in the Vilcabamba avifauna (Table 5). Ecotones account for less than 20% of all distributional limits, a result that must come as a surprise to anyone familiar with the importance of habitat in predicting the census of North American bird species (MacArthur, MacArthur, and Preer 1962). Moreover, the stated figures are likely to represent overestimates since it can be expected that some of the included limits fell at ecotones coincidentally.

Approximately one-third of all limits are as- cribed to competitive exclusion. In this case some underestimation is probable because of the omis- sion of several replacing series of related species whose members have been placed by taxonomists in separate genera. (Examples are to be found among the guans, toucans, antbirds, etc.). A fur-

ther underestimation would result should the occurrence of any appreciable number of species be restricted by diffuse or other nonobvious kinds of competitive interactions. These considerations lead to the conclusion that, in the densely packed avifauna of the Andes, competition determines at least twice as many distributional limits as do ecotones. Where the pressure of high diversity is relaxed, as on islands or at temperate latitudes, the importance of competition is likely to be con- siderably reduced. Under such circumstances one could expect that ecotones would assume a more prominent role, as species amplitudes would in general be broader.

To the gradient model, partly in consequence of its composite and residual character, have been assigned the largest number of limits. An in- triguing result is that environmental factors associated with the gradient are apparently more important in determining upper limits (56%) than in determining lower limits (43%). We shall now turn to the implications of this finding and to




TABLE 3. Mean amplitudes and amplitude compression in certain ecologically defined groups of species in the Vilcabamba avifauna

Mean Amplitude amplitude compression

Species group N (meters) (%) Al species ........................ 207 741?31 Monotypic total ................... 64 833 ?60 0 Monotypic

upper limits > 3,000m ........... 16 1,348?115

Monotypic 2,000 m < upper limit < 3,000m. 18 815 ?86

Monotypic upper limit < 2,000m ............ 30 570?58

Series of 2 upper members .................. 35 723 ?64 lower members .................. 19 613 ?53 26.4

Series of 3 uppermost members ............. 12 947 ?88 lower members ................. . 17 440 ?61 47.2

Series of 4 uppermost members ......... .... 3 980 ? 171 lower members ................. . 14 363 ?103 56.4

the interpretation of distributional patterns in the upper portion of the gradient.

From an inspection of the congruity curves (Fig. 6) it was concluded earlier that ecological amplitudes tend to expand towards the upper terminus of the gradient. By projecting the 50% congruity levels of these curves onto the abcissa it is possible to examine this trend in quantitative detail (Table

6). A broadening of both tails of the curves for samples taken above 2,000 m indicates an increase of more than 50% in the mean amplitude of species living near the top of the range. Thus the results that were obtained for the uppermost members of replacing series of congeners and for monotypic forms whose upper limits lie above 3,000 m (Table 3) are typical of the fauna as a whole. These findings contradict the predictions of all of the models, two of which (competition and ecotone) anticipate no change in mean amplitude while the third (gradient) implies a reduced amplitude near a terminus. How is this discrep- ancy to be reconciled?

Implicit in the theory is an equality of evolutionary opportunity and packing of niches at all points on a gradient. In the light of the now well- established relationship between area of habitat and species diversity (MacArthur and Wilson 1967), it is clear that the two termini of the Vil- cabamba gradient are very different from the view- point of evolutionary opportunity. The world's richest pool of bird species exists in the Amazon basin, where probable climatic oscillations during the Pleistocene apparently gave rise to a com- paratively recent burst of speciation (Haffer 1967, 1969). Topographic maps of the Andes reveal, on the other hand, that humid habitat between the limits of 2,000 and 3,500 m exists mainly on steep slopes as a narrow involuted belt, the total area of which would constitute only about 1%o of that

TABLE 4. Results of t-tests of the differences between selected pairs of means shown in Table 3

Series of

2 3 4

Species group upper lower uppermost lower uppermost lower

Monotypic-total 0.4>P P=0.02 0.5>P>0.4 P <0. 001 P>0.5 P=0.001 >0.2

Series of 2-lower 0.4>P _ - 0.05> 0. 05 > members >0.2 P>0.02 P>0.02

Series of 3-lower - 0.05 > members P>0.02 P<0.001 _ _ P>0.5

Series of 4-lower _ 0.05> _ P>0.5 P=0.02 members P>0.02

TABLE 5. Assignment of upper and lower distributional limits of Vilcabamba birds to three models. Netted species only: total species = 261; total limits = 522

Lower limits Upper limits

At termius Gradient Competition Ecotone At termius Gradient Competition Ecotone

Number of limits 68 83 69 41 48 119 59 35 Per cent of limits within termini -43%o 36% 2% 56%7 28%o 16%o




TABLE 6. Vertical distance to 50%o congruity levels above and below the sampling stations. Data in meters was taken from the abscissa of Figure 6

Vertical distance to 50% congruity level

Elevation of sample above below sum

585 .............. 225 - - 685 .............. 365 90 455 930 .............. 415 315 730

1340 .............. 270 370 640 1520 .............. 330 350 680 1730 .............. 310 315 652 2155 .............. 425 405 830 2640 .............. 730 425 1155 2825 .............. 600 470 1070 3300 .............. - 830 - 35101. 875

of the Amazonian rainforest. Between the Ama- zonian plain and 2,000 m, the slope of the terrain is generally more gradual, there being considerable expanses of plateau, foothills and montane valleys. Thus we are forced to consider the probable influence of a strong gradient in area of habitat running in parallel with the elevational gradient on the eastern slopes of the Andes. Biogeogra- phers have long held that the tropical montane avifauna of the continent was derived from the lowlands (Chapman 1921), a notion that is well substantiated by close generic and familial affin- ities.

In order to achieve a clear comprehension of the unexpected distributional patterns near the upper terminus of the gradient, it will be worth- while to digress for a moment to consider, hypo- thetically, the mode of origin of the upper members of replacing congeneric series. Two populations having a common lineage which have diverged to the species level in allopatry may sub- sequently expand their geographical ranges until contact is established along a more-or-less broad front. If the species are so similar ecologically that coexistence is unstable, then further range expansion into sympatry can be accomplished only through some mode of displacement or ecological segregation, elevational exclusion being one of the possibilities. When this occurs in montane forest, the usual outcome is that the species whose elevational optimum is higher becomes the upper member of a replacing pair. Because the two species share a common ancestry, their optima will, at least initially, lie rather closely on the gradient. This kind of accommodation is possible only for pairs of species whose intrinsic optima and elevational limits are sufficiently different. The extremely narrow amplitudes of some species in replacing series suggests that the minimum necessary difference between optima is not great, on

the order of 100-200 m. Competition between species whose optima are closer must usually lead to the complete exclusion of one, since the amount of inhabitable space on the gradient left for the weaker competitor is unlikely to suffice for the maintenance of a stable population. When optima are close together the resulting repulsion interaction should be particularly conspicuous. Thus the continued coexistence of two excluding species on a gradient implies selection favoring the divergence of their respective optima. But in the special case at hand, in which the fauna of the entire gradient has been derived from one terminus, only the distal (uppermost) member of any replacing series is presented the opportunity of expanding into an open domain. Lower members may evolve higher optima only as the uppermost member itself advances on the gradient. We may thus fairly regard the upper slopes of the Andes as an evolutionary sink, offering competitor- free expansion to species that develop higher optima. Whatever species were to experience a lower pressure of competition on the uphill side would spread in that direction as far as its toler- ance to the conditions permitted. Should the gradient actually offer such open-ended possibilities for expansion, then one would expect pre- cisely the two results obtained: greater amplitudes towards the open end of the gradient and a higher proportion of gradient-limited distributions on that side. Thus even on continents it seems necessary to evoke MacArthur and Wilson's equilibrium theory to account for present-day distributional patterns; equal close packing of niches at all points on environmental gradients cannot be assumed.

An alternative explanation of increased amplitude at the upper end of the gradient, also based on equilibrium theory, should be mentioned. It was previously pointed out that plant productivity appears to be extremely low in the cold cloudy climate of the crest of the range. The resulting slow rate of energy flux through the ecosystem must impose a correspondingly reduced ceiling on animal population densities. Two lines of circumstantial evidence support this presumption for avian populations. The catch rates of mist nets were distinctly reduced above 3,000 m. In itself this is weak evidence since the performance of net lines is quite variable at constant elevation. Sub- stantiation comes from the record of observations. The author routinely made from 100 to 300 bird sightings a day in virtually any kind of habitat up to 1,500 m. At 2,000 m the average fell to about 50 sightings, and above 3,000 m, 20 sightings constituted a good day. On numerous occa- sions experienced observers spent half-days in the vicinity of our upper camps without seeing a sin-




gle bird. To one who has been on the scene this is convincing evidence of a gradient in bird density that parallels the putative gradient in plant productivity. If these suppositions are correct they imply that any species having a given narrow amplitude would have a much lower probability of long-term survival at 3,000 m than at 1,000 m. Consequently, even moderately compressed species would quickly be eliminated from zones of low density, leaving a fauna whose mean amplitude was appreciably greater than average. It is likely that both this and the evolutionary mechanism described earlier contribute to the expanded mean amplitude at higher elevations, though only the evolutionary hypothesis can account for the excess of gradient-determined upper limits.

One of the predictions of the gradient model (Table 1) is that the number of coexisting species will decline somewhat near the terminus of a gradient. This question has been investigated by comparing the number of species in 50-bird samples taken at the three upper camps (2,840, 3,220 and 3,510 m) where the vegetation is uniformly less than 8 m high and where there is no significant variation in foliage height profiles of the habitat. Only a hint of a trend is apparent in the results, which give for each of the three camps, respectively, the mean number of species per 50- bird sample and in parentheses the number of independent samples used in computing the mean; 23.9 (9), 22.7 (6), 22.0 (4). Longer species lists for the lower camps may only reflect a greater amount of time spent there and a higher overall density of birds. In any case, a small effect is to be expected because it would involve merely a fraction of the gradient-limited component of the fauna, which, in the present instance, includes only about half of the species present. For the time being the issue must stand unresolved. A better test of the prediction should be possible with a more easily sampled group of organisms which included a greater proportion of gradient-limited species.

As a final consideration we will return to the amplitude frequency distribution (Fig. 5) and inquire into its interpretation. Three pronounced peaks are evident: at 300-400, 700-800 and 1,300- 1,400 m. Each can now be associated with one or more of the sets of species that have been defined in the preceding discussion (Table 4). The principal peak (700-800 m) reflects the mean of all species and specifically the mean of monotypic forms whose upper limits lie between 2,000 and 3,000 m (815 m). A minor rise at 500-600 m lies at the mean of monotypic forms whose upper limits lie below 2,000 m (570 m). Coinciding with the first maximum (300-400 m) is the mean of

the highly compressed lower members of fourfold series (363 m). With few exceptions the last peak (1,300-1,400 m) is comprised of species whose upper limits lie at or near the top of the gradient, many of which are included in the group of monotypic forms reaching 3,000 m or more whose mean was found to be 1,348 m.

What was initially suspected on a priori grounds has thus been confirmed empirically; namely, that the amplitude frequency distribution results from the addition of several more or less homogeneous but mutually interdependent frequency distributions, each with a distinct mean. Although the problem of interpreting ecological amplitudes is complex, we hope that a way has been opened to its eventual solution.

ACKNOWLEDGMENTS

At the conclusion of a work of several years' duration it is difficult to pay proper tribute to the many people who have contributed to the project in one way or another. Particularly I am grateful for the enthusiasm and un- flagging spirit of my comrades on four long expeditions into one of the world's last great wildernesses. The physical demands of exploration are great at times and often comfort has to be sacrificed to expediency. Thus it is a special pleasure to thank my expedition mates: Theodore R. Dudley, John S. Knox, William S. Russell and John S. Weske. As the ornithologist on these expeditions, John Weske is personally responsible for gather- ing much of the data reported here. Most of the work of moving equipment and supplies over nearly 40 kilometers of steep trails fell on our several Peruvian assistants, among whom Klaus Wehr, Manuel Sanchez and Hum- berto Santana handled numerous additional responsibil- ities. An indispensable asset throughout our explorations was the secure base of operations and generous hospitality given to us at Hacienda Luisiana in the Apurimac Valley by its owner, Jose Parodi.

Finally, we wish to acknowledge the continued interest and financial support of the three institutions that gave life to the expeditions: the Chapman Fund of the Amer- ican Museum of Natural History, the American Philo- sophical Society and the National Geographic Society.

LITERATURE CITED

Bakeland, G. B. 1964. By parachute into Peru's lost world. National Geographic 126: 268-296.

Bray, R. J., and J. T. Curtis. 1957. An ordination of the upland forest communities of southern Wisconsin. Ecol. Monogr. 27: 325-349.

Chapman, F. M. 1921. The distribution of bird life in the Urubamba Valley of Peru. U. S. Nat. Mus. Bul. 117: 1-138.

Crawford, R. M. M., and D. Wishart. 1967. A rapid multivariate method for the detection and classifica- tion of groups of ecologically related species. J. Ecol. 55: 505-524.

Daubenmire, R. 1966. Vegetation: identification of typal communities. Science 151: 291-298.

Diamond, J. M. 1969. Preliminary results of an orni- thological exploration of the North Coastal Range, New Guinea. Amer. Mus. Novitates 2362: 1-57.

Haffer, J. 1967. Speciation in Colombian forest birds




west of the Andes. Amer. Mus. Novitates 2294: 1-57.

. 1969. Speciation in Amazonian forest birds. Science 165: 131-144.

Janzen, D. H. 1967. Why mountain passes are higher in the tropics. Amer. Naturalist 101: 233-249.

MacArthur, R. H., J. W. MacArthur, and J. Preer. 1962. On bird species diversity. II. Prediction of bird census from habitat measurements. Amer. Naturalist 96: 167-174.

MacArthur, R. H., and E. 0. Wilson. 1967. The theory of island biogeography. Princeton Univ. Press, Princeton, N. J. 203 p.

Mayr, E., and E. T. Gilliard. 1954. Birds of central New Guinea. Bull. Amer. Mus. Natur. His. 103: 311- 374.

McIntosh, R. P. 1967. The continuum concept of vegetation. Botan. Rev. 33: 130-187.

Orloci, L. 1966. Geometric models in ecology. I. The theory and application of some ordination methods. J. Ecol. 54: 193-215.

Paddock, F. K. 1967. A search for Inca ruins in south- eastern Peru. Explorer's J. 45: 34-41.

Richards, P. W. 1952. The tropical rainforest. Cam- bridge Univ. Press, Cambridge. 450 p.

Terborgh, J. 1968. Bird species diversity on an elevational gradient in neotropical forest. Amer. Phil. Soc. Yearbook 1967: 298-302.

Terborgh, J., and J. M. Diamond. 1970. Niche overlap in feeding assemblages of New Guinea birds. Wilson Bull. 81: 29-52.

Terborgh, J., and T. R. Dudley. 1970. The biological exploration of the Northern Cordillera Vilcabamba, Peru. National Geographic Soc. (in press).

Terborgh, J., and J. S. Weske. 1969. Colonization of secondary habitats by Peruvian birds. Ecology 50: 765-782.

Whittaker, R. H. 1956. Vegetation of the Great Smoky Mountains. Ecol. Monogr. 26: 1-80.

1967. Gradient analysis of vegetation. Biol. Rev. 42: 207-264.

Williams, W. T., and J. M. Lambert. 1959. Multivari- ate methods in plant ecology. 1. Association analysis in plant communities. J. Ecol. 47: 83-101.

APPENDIX

The shape of the congruity curve for gradient-limited species is easily derived from three assumptions: (1) optima fall at random along the gradient, (2) population density curves are symmetrical about their maxima, and (3) amplitudes are normally distributed. Assumptions 1 and 2 are explicitly stated tenets of the model, while the third assumption is made somewhat arbitrarily to facilitate the derivation. Although the postulates of the model do not predict any particular array of amplitudes, it is reasonable to suppose, in the absence of competition and ecotones, that the distribution of amplitudes would be unimodal, if not normal. Empirically it can be shown that even fairly large departures from a normal distri-

' I I I I I I ' ' ' .

0 1 2 5 8 12 16 20 24 20 16 12 8 5 2 1 0

I

1- t~~~~

- GRADI ENT

FIG. 13. Graphical derivation of the form of the congruity curve (inset). See text for explanation.

bution of amplitudes lead to only minor alterations in the shape of the congruity curve, as is indicated also by the generally good agreement between the theoretical curve and those constructed from our data on Vilcabamba birds (Figs. 6 and 7). The following derivation rests on the exposition of an example; its generality supposes an in- ductive extension of the example.

Assume a gradient in some measurable factor, the values of which can be expressed on a linear scale (Fig. 13). When the sampling interval (in gradient units) is sufficiently broad, the number of species whose optima will fall within the interval will be approximately constant. Here the number is taken to be four. If the species are normally distributed with respect to amplitude, there will be on the average in each set of four, two whose amplitudes approximate the mean and one each whose amplitudes are somewhat greater and shorter than the mean. The sets of horizontal lines in the figure represent these stipulations. For simplicity the optima of each group of four species are shown to coincide at the midpoint of the sampling interval (vertical bars).

The fauna of the central sampling point (assuming zero sampling error) is composed of the 24 species whose amplitudes include that value of the gradient. These species are indicated by the solid horizontal bars. Their number decreases monotonically at sampling stations on either side of the central sample in accordance with the counts given at the top of the figure. Plotted against the gradient in the insert, these results assume the form of an isoceles triangle somewhat splayed out at the base.

Empirical curves may be distorted by departures from the assumptions listed above and by at least two kinds of presently unavoidable methodological errors. (i) Less- than-perfect sampling efficiency reduces the height of the peak at the central sampling position and hence slightly lowers the slopes of the congruity curves. (ii) Inclusion of species whose amplitudes are limited by factors other than the gradient in question may alter the properties of the curves in a variety of ways (e.g., ecotone effects).



distribution on environmental gradients: theory and a preliminary...

Documents