2651 Ecology, 80(8), 1999, pp. 2651–2661 q 1999 by the Ecological Society of America TREE SPECIES DISTRIBUTIONS IN AN UPPER AMAZONIAN FOREST NIGEL C. A. PITMAN, 1,5 JOHN TERBORGH, 2 MILES R. SILMAN, 3,6 AND PERCY NUN ˜ EZ V. 4 1 Department of Botany, Box 90339, Duke University, Durham, North Carolina 27708-0339 USA 2 Center for Tropical Conservation, Box 90381, Duke University, Durham, North Carolina 27708-0381 USA 3 Department of Zoology, Box 90325, Duke University, Durham, North Carolina 27708-0325 USA 4 Herbario Vargas, Universidad Nacional San Antonio de Abad de Cusco, Cusco, Peru Abstract. Not a single tree species distribution in the Amazon basin has been reliably mapped, though speculation regarding such distributions has been extensive. We present data from a network of 21 forest plots in Manu National Park, Peru, totaling .36 ha and sited over an area of ;400 km 2 , to explore how tree species are distributed across upper Amazonia at a variety of spatial scales. For each of 825 tree species occurring in the plots we asked three questions: (1) Does the species have a large or small geographic range? (2) Is the species restricted to a single forest type, or is it found in several? (3) Is the species locally abundant anywhere or is it scarce everywhere? The answers served to classify a subset of species under Rabinowitz’s classification scheme for rare species. Three main conclusions emerged. First, the great majority of tree species at Manu are geographically widespread. Every species identified to date occurs elsewhere in South America, outside the department of Madre de Dios; more than two-thirds of them have been collected 1500 km away in Amazonian Ecuador. Second, 15–26% of species appear to be restricted to a single forest type, when forest types are defined by historical river dynamics (i.e., terra firme forest, mature floodplain forest, swamp forest, and primary successional floodplain forest). The proportion of restricted species declined with increasing sampling effort, mak- ing 15% a more reliable figure. Third, while 88% of species occurred at densities of ,1 individual/ha over the entire network of plots, at least half occurred somewhere at densities of .1.5 individuals/ha. Extrapolating these results provides a first guess at how tree species are distributed across the western portion of the Amazon basin. We conclude with the suggestion that most tree species in the region are habitat generalists occurring over large areas of the Amazonian lowlands at low densities but large absolute population sizes. Key words: Amazon; Peru; rarity; tropical forests; tropical tree communities; tropical trees. INTRODUCTION The question of how plant species are distributed across Amazonian forests—a crucial one for ecologists, conservationists, and foresters—remains unanswered. Ecologists can point to factors that influence species distributions at small spatial scales, such as local to- pography (e.g., Hubbell and Foster 1983, Poulsen and Balslev 1991, Basnet 1992, Tuomisto and Ruokolainen 1994), and biogeographers can sketch species ranges from collection records (Prance 1982), but the hetero- geneity of forests in the Amazon basin makes com- pleting the picture difficult (Tuomisto et al. 1995). In this paper, one of a series reporting results from a network of permanent forest plots in lowland Peru- vian forests, we present empirical data on tropical tree distributions at three spatial scales: within plots (0.9– 2.5 ha), between forest types (; 400 km 2 ), and through- out Peru (.1 3 10 6 km 2 ). In doing so our aim is to fit Manuscript received 2 June 1997; revised 15 April 1998; accepted 31 August 1998; final version received 9 November 1998. 5 E-mail: [email protected]6 Present address: Department of Biology, Wake Forest University, P.O. Box 7325, Winston-Salem, North Carolina 27109 USA. together observations from different scale perspectives into a more complete picture of how tree species are distributed across upper Amazonia. Because most Amazonian tree species are locally scarce, the project is relevant to broader questions about rarity in the tropics. The low population densities of tree species in tropical forests have intrigued ecol- ogists since Wallace (1878; see also Black et al. 1950, Janzen 1970, Connell 1971, Hubbell 1979). But despite a general understanding that rare species are rare in different ways (Rabinowitz 1981, Gaston 1994), a lack of data at varying spatial scales has restricted most discussion of rarity in the tropics to a single component, local scarcity. The research we present here is intended to broaden that view, by documenting precisely how hundreds of rare tropical species are rare. The answer should be a concern not only to conser- vation biologists (Prendergast et al. 1993), but also to ecologists intent on understanding how the high species diversity of tropical tree communities originated and how it is maintained in nature. Many of the hypotheses put forward emphasize processes related to distribution patterns at intermediate to large scales, such as migra- tion, vicariance, and habitat restriction (e.g., genetic drift [Fedorov 1966], Pleistocene refugial hypothesis
Transcript
2651
Ecology, 80(8), 1999, pp. 2651–2661q 1999 by the Ecological Society of America
TREE SPECIES DISTRIBUTIONS IN AN UPPER AMAZONIAN FOREST
NIGEL C. A. PITMAN,1,5 JOHN TERBORGH,2 MILES R. SILMAN,3,6 AND PERCY NUNEZ V.4
1Department of Botany, Box 90339, Duke University, Durham, North Carolina 27708-0339 USA2Center for Tropical Conservation, Box 90381, Duke University, Durham, North Carolina 27708-0381 USA
3Department of Zoology, Box 90325, Duke University, Durham, North Carolina 27708-0325 USA4Herbario Vargas, Universidad Nacional San Antonio de Abad de Cusco, Cusco, Peru
Abstract. Not a single tree species distribution in the Amazon basin has been reliablymapped, though speculation regarding such distributions has been extensive. We presentdata from a network of 21 forest plots in Manu National Park, Peru, totaling .36 ha andsited over an area of ;400 km2, to explore how tree species are distributed across upperAmazonia at a variety of spatial scales. For each of 825 tree species occurring in the plotswe asked three questions: (1) Does the species have a large or small geographic range? (2)Is the species restricted to a single forest type, or is it found in several? (3) Is the specieslocally abundant anywhere or is it scarce everywhere? The answers served to classify asubset of species under Rabinowitz’s classification scheme for rare species. Three mainconclusions emerged. First, the great majority of tree species at Manu are geographicallywidespread. Every species identified to date occurs elsewhere in South America, outsidethe department of Madre de Dios; more than two-thirds of them have been collected 1500km away in Amazonian Ecuador. Second, 15–26% of species appear to be restricted to asingle forest type, when forest types are defined by historical river dynamics (i.e., terrafirme forest, mature floodplain forest, swamp forest, and primary successional floodplainforest). The proportion of restricted species declined with increasing sampling effort, mak-ing 15% a more reliable figure. Third, while 88% of species occurred at densities of ,1individual/ha over the entire network of plots, at least half occurred somewhere at densitiesof .1.5 individuals/ha. Extrapolating these results provides a first guess at how tree speciesare distributed across the western portion of the Amazon basin. We conclude with thesuggestion that most tree species in the region are habitat generalists occurring over largeareas of the Amazonian lowlands at low densities but large absolute population sizes.
The question of how plant species are distributedacross Amazonian forests—a crucial one for ecologists,conservationists, and foresters—remains unanswered.Ecologists can point to factors that influence speciesdistributions at small spatial scales, such as local to-pography (e.g., Hubbell and Foster 1983, Poulsen andBalslev 1991, Basnet 1992, Tuomisto and Ruokolainen1994), and biogeographers can sketch species rangesfrom collection records (Prance 1982), but the hetero-geneity of forests in the Amazon basin makes com-pleting the picture difficult (Tuomisto et al. 1995).
In this paper, one of a series reporting results froma network of permanent forest plots in lowland Peru-vian forests, we present empirical data on tropical treedistributions at three spatial scales: within plots (0.9–2.5 ha), between forest types (; 400 km2), and through-out Peru (.1 3 106 km2). In doing so our aim is to fit
Manuscript received 2 June 1997; revised 15 April 1998;accepted 31 August 1998; final version received 9 November1998.
5 E-mail: [email protected] Present address: Department of Biology, Wake Forest
University, P.O. Box 7325, Winston-Salem, North Carolina27109 USA.
together observations from different scale perspectivesinto a more complete picture of how tree species aredistributed across upper Amazonia.
Because most Amazonian tree species are locallyscarce, the project is relevant to broader questionsabout rarity in the tropics. The low population densitiesof tree species in tropical forests have intrigued ecol-ogists since Wallace (1878; see also Black et al. 1950,Janzen 1970, Connell 1971, Hubbell 1979). But despitea general understanding that rare species are rare indifferent ways (Rabinowitz 1981, Gaston 1994), a lackof data at varying spatial scales has restricted mostdiscussion of rarity in the tropics to a single component,local scarcity. The research we present here is intendedto broaden that view, by documenting precisely howhundreds of rare tropical species are rare.
The answer should be a concern not only to conser-vation biologists (Prendergast et al. 1993), but also toecologists intent on understanding how the high speciesdiversity of tropical tree communities originated andhow it is maintained in nature. Many of the hypothesesput forward emphasize processes related to distributionpatterns at intermediate to large scales, such as migra-tion, vicariance, and habitat restriction (e.g., geneticdrift [Fedorov 1966], Pleistocene refugial hypothesis
2652 Ecology, Vol. 80, No. 8NIGEL C. A. PITMAN ET AL.
[Haffer 1969, Prance 1982], or community drift [Hub-bell and Foster 1986a]), or invoke processes that mayhave opposite effects at different spatial scales (den-sity-dependent mortality [Janzen 1970, Connell 1971,Schupp 1992] or the intermediate disturbance hypoth-esis [Connell 1978, Hubbell 1979, Salo et al. 1986]).Recent data sets from intermediate and large spatialscales will play an increasingly important role in testingthose hypotheses (Phillips et al. 1994, Clark et al. 1995,Clinebell et al. 1995, Duivenvoorden and Lips 1995,Ruokolainen et al. 1995, Duivenvoorden 1996, Lie-berman et al. 1996).
The patterns that emerge from this data set shouldbe of interest to more than just tropical biologists. Mostattempts to understand rarity in plants have come frombotanically well-known but drastically altered temper-ate landscapes such as the British Isles or California(e.g., Ratcliffe 1984, Rabinowitz et al. 1986, Quinn etal. 1994). Botanical exploration of our site in Peru isfar from complete, and the data presented below arepreliminary; the trade-off is that they come from alargely undisturbed region of the planet.
This is the first attempt to classify a wide range ofplant species under Rabinowitz’s (1981) scheme usingquantitative data at each step. Rabinowitz et al. (1986)classified a subset of the British flora but used surveyresponses, and not plot data, to estimate local abun-dance and habitat specificity. Similarly, the four-cate-gory classification scheme proposed for Asian tropicaltrees by Bawa and Ashton (1991) was founded on theauthors’ familiarity with the regional flora rather thanon specific data sets. The scarcity of Rabinowitz anal-yses is regrettable, but it should not reflect badly onher system. To our way of thinking, it remains one ofthe best ways to present multiscale species abundancedata in a comprehensible way.
Such data did not exist for tropical tree species untilvery recently. The best studies of Neotropical tree spe-cies distributions to date are those of Hubbell and Fos-ter (1986b), who reported local patterns from a 50-haplot in Panamanian moist forest, and of Gentry (1986)and others who have documented large-scale distri-butional patterns in Central and South America. Thispaper bridges those scales, providing a fuller pictureof how tree species are distributed in the richest forestson earth.
METHODS
Study site and data collection
We used data from 21 tree plots in lowland tropicalmoist forest in the Manu River basin, Manu NationalPark, southeastern Peru (118529 S, 718219 W). Rainfallat the site is highly seasonal, with most of the annual2000 mm falling during a November to May wet sea-son. Detailed descriptions of the climate, physical land-scape, and flora are given by Terborgh (1983, 1990)and Foster (1990).
The plots were established between 1975 and 1996by P. Nunez, J. Terborgh, Robin Foster, Alwyn Gentry,and many others. In each plot, all free-standing trees$10 cm dbh were mapped, measured for diameter at1.3-m height (avoiding trunk irregularities), and iden-tified, or collected if field identification was not pos-sible. Though initial field identifications were made bymany different botanists, subsequent recensuses ofmost plots by P. Nunez have made it possible to stan-dardize taxonomy. For the plots not recensused (i.e.,the four Pakitza plots), P. Nunez studied voucher spec-imens deposited in the Missouri Botanical Garden, theField Museum of Natural History, and Peruvian her-baria.
Plots range in size from 0.8675 to 2.5 ha, for a totalof 36.375 ha, and are distributed over an area of ;400km2 (40 3 10 km). Thus, while 36 ha is a large sizefor tropical tree inventories, the plots only cover 0.09%of the area we intend them to characterize. Plots aredistributed unequally in four different forest types: ter-ra firme or upland forest, mature floodplain forest, pri-mary successional floodplain forest, and swamp forest(see Fig. 1 for locations of plots and see the Appendixfor their sizes, stem numbers, species numbers, etc.).
These forest types are defined by the past and currentmeanderings of the Manu River. Terra firme forest isfound on the low hills bordering the river’s 6–8 kmwide meander belt and is never subject to flooding.Judging from satellite images, aerial photographs, andradar images of the study area, terra firme forest ac-counts for ;88% of all forest in the study area. Maturefloodplain forest covers much of the river’s meanderbelt and is very rarely flooded (twice in the last 25 yr).It occupies ;6% of all forest in the area. Primary suc-cessional floodplain forest refers to the primary suc-cession that occurs on sandy point bars laid down onthe inside bends of the river, and covers roughly 4%of the study area. Swamp forest represents the finalstage in the life of an old oxbow lake, when trees col-onize an elongate, seasonally flooded depression in themeander belt. Swamp forests are the smallest foresttype, accounting for only ;2% of the Manu landscape.
These four habitats cannot be ordered along a regulargradient of environmental attributes but are distin-guished by gross differences in age, soil type, lightenvironment, and flooding frequency, and they formremarkably discrete patches on the Manu landscape.The plots in primary successional forests do followlinear age gradients in succession, as inferred bychanges in forest structure, but they do not includemature floodplain forest.
Classification
We classified each species occurring in the plots intoone of Rabinowitz’s ‘‘seven forms of rarity.’’ Rabino-witz’s system of classifying rare plant species is thebest-known of many (see Gaston [1994] for a review).Under her scheme, every species is classified as: (1)
December 1999 2653TREE SPECIES DISTRIBUTIONS IN AMAZONIA
FIG. 1. A stretch of the Manu River in the vicinity of the Cocha Cashu Biological Station, Madre de Dios, Peru. Thelocations of tree plots mentioned in the text are given by numbers, which also indicate how many plots were sampled ateach site. The inset shows the location of the study site in South America.
FIG. 2. Rabinowitz’s classification scheme for rare species (adapted from Rabinowitz [1981] with permission from JohnWiley and Sons Limited).
abundant somewhere or scarce everywhere, (2) re-stricted to a single habitat type or not, and (3) geo-graphically widespread or restricted. Of the eight re-sulting combinations, seven describe different ways aplant species can be rare; the eighth describes a uni-versally common species (Fig. 2).
In its strictest sense, Rabinowitz’s method requiresfixing arbitrary definitions of ‘‘abundant,’’ ‘‘scarce,’’‘‘restricted,’’ ‘‘widespread,’’ ‘‘broad,’’ and ‘‘narrow,’’resulting in an eight-celled, 2 3 2 3 2 matrix. Althoughwe did choose arbitrary thresholds to define geographicrange as ‘‘large’’ or ‘‘small,’’ habitat specificity as
‘‘wide’’ or ‘‘narrow,’’ and local population size as‘‘large’’ or ‘‘small,’’ as explained below, we also reportthe range and variation of the latter two variables.
Local abundance
Because the Rabinowitz scheme asks whether spe-cies are abundant anywhere, a species’ local abundancewas defined by the highest stem density it reached atany single site in the network of plots. Species whosemaximum local abundance was #1 individual/ha werescored as locally scarce everywhere. Species with max-imum local abundances of .1 individual/ha were
2654 Ecology, Vol. 80, No. 8NIGEL C. A. PITMAN ET AL.
scored as locally abundant somewhere. We did not useHubbell and Foster’s (1986b) similar threshold for rar-ity in tropical trees (,1 individual/ha) for two reasons.First, their data set includes stems much smaller thanours. Second, several of the Manu plots are #1 ha inextent, so that even the rarest stems in those plots wouldnot have qualified as locally rare under their threshold.
Habitat specificity
We defined narrowly restricted species as those thatoccurred in one forest type and no other, and wide-spread species as those that occurred in more than oneforest type. Deciding whether a species was restrictedor widespread required that the species be representedby some minimum number of individuals. We selectedtwo arbitrary thresholds based on the number of plotsa species occurred in, in order to evaluate how theresults changed as more information became availableabout species. Analysis was restricted first to the 462species occurring in two or more plots, and then to the365 species occurring in three or more plots.
Geographic range
Information on the Peruvian ranges of named specieswas taken from Brako and Zarucchi’s (1993) checklistof Peruvian plants. Like all data sets of Amazonianphytogeography this one is preliminary, in some casesreflecting artifacts of collection intensity or taxonomicconfusion more faithfully than the actual ranges of spe-cies (Gentry 1992). Because much of Peru remainsbotanically unexplored and range extensions are com-mon, using the checklist biased us towards scoring spe-cies ranges as small.
We defined small-ranged species as those that havenever been collected outside the Peruvian departmentof Madre de Dios, and large-ranged species as thosethat have. The rationale is that the size of the depart-ment of Madre de Dios, 78 415 km2, fits the most widelyused criterion of tropical plant species endemism, 50–75 000 km2 (Gentry 1986, 1992). All species listed inBrako and Zarucchi (1993) as occurring exclusively inMadre de Dios were rechecked in other sources, andspecies found to occur outside Peru were scored ashaving large ranges.
RESULTS
Tree plots
The 21 plots surveyed contained a total of 19 252stems $10 cm dbh. All but 377 stems have been iden-tified to family and placed in one of 829 species ormorphospecies. Almost a third of all species and mor-phospecies (31%) are represented by a single individualand nearly half (45%) occur in only one plot. We dis-carded four species because they were treelets that onlyoccasionally exceeded the diameter cutoff, producingan artifactual signal of rarity: Vernonia patens (Aster-aceae), Tessaria integrifolia (Asteraceae), Styloceras
brokawii (Buxaceae), and Solanum sessile (Solanace-ae). Thus questions about local abundance could beanswered for 825 total taxa: 588 (71%) determined tospecies, and 237 (29%) determined to morphospecies.Questions about habitat specificity could be answeredfor the 462 species that occurred in more than one plot.Questions about geographic range could be answeredfor 506 species. All three questions could be answeredfor 381 species, or just under half of the total.
Geographic range
Of the 506 species for which geographic range sizeinformation exists, not one occurs exclusively in thedepartment of Madre de Dios. The nineteen specieslisted in Brako and Zarucchi (1993) as only occurringin Madre de Dios were all found to occur outside ofPeru.
Habitat specificity
Fifteen to twenty-six percent of all species werefound to be restricted to a single forest type, dependingon the threshold used (Fig. 3). Of the 462 species oc-curring in more than one plot, 26% occurred in a singleforest type, while 17% were found in all four foresttypes. Of the 365 species occurring in more than twoplots, 15% occurred in a single forest type and 22%occurred in all four. Under both thresholds, the greatmajority of species restricted to a single forest typewere restricted to terra firme forest (73 and 76%, re-spectively).
Local population size
The maximum local densities of species ranged from0.4 to 217 stems/ha (Laetia corymbulosa [Flacourti-aceae] in swamp forest at Pakitza). While a few largevalues inflated the mean maximum density to 5.2 stems/ha, the median was much lower: half of all speciesoccurred in some plot at a density of .1.5 stems/ha(Fig. 4).
Rabinowitz classification
We present two different Rabinowitz matrices cor-responding to the two different subsets of the data usedfor the habitat specificity test: one for species occurringin more than one plot, and another for species occurringin more than two plots (topmost and middle matricesin Fig. 5, respectively). The most common categoryunder both thresholds was that of ‘‘common’’ plantspecies, i.e., those with large geographic ranges, oc-curring in more than one habitat, and having large localpopulation sizes somewhere in tropical America. Themost common form of ‘‘rarity’’ in our data set was thatof large geographic range, marked habitat preference,and large local population sizes somewhere.
Defining local scarcity less conservatively (i.e., rais-ing the threshold of #1 stem per hectare) would clearlyhave the effect of moving many species downward inthe matrices in Fig. 5. A similar effect would result if
December 1999 2655TREE SPECIES DISTRIBUTIONS IN AMAZONIA
FIG. 3. Patterns of habitat specialization observed in two subsets of Manu tree species. The diagram on the left refersto the 462 species and morphospecies that occur in two or more plots; that on the right to the 365 that occur in three ormore. In each case the left-hand columns show the proportion of species occurring in one, two, three, or four forest types,and the right-hand columns show the proportion of specialists occurring in each of four forest types.
FIG. 4. Distribution of maximum localabundances observed for 825 Manu tree species.Integers on the x-axis refer to a range of values(e.g., ‘‘2’’ indicates abundances between 2.00and 2.99 stems/ha).
the species excluded from the analysis because theyoccurred in a single plot were included. Even if all 825species were included, however, the majority of species(57%) would still be categorized as locally abundantsomewhere. In all such shuffling, large geographicranges and weak habitat specificity remain constant.
Nonindependence of variables
The number of forest types a species occurred in waspositively correlated with its maximum local abun-dance (Spearman’s r 5 0.59, P , 0.0001). Maximumlocal abundance was also positively correlated with the
number of Peruvian departments a species was reportedfrom (Spearman’s r 5 0.14, P , 0.01). There was nocorrelation between number of departments and num-ber of habitats. While the data did not meet the as-sumptions of normality, parametric tests gave similarresults.
DISCUSSION
Overview
Most tree species found in the plots at Manu appearto occur over large areas of the Peruvian Amazon, arenot restricted to a single forest type, and can be found
2656 Ecology, Vol. 80, No. 8NIGEL C. A. PITMAN ET AL.
FIG. 5. Rabinowitz classifications for two subsets of Manu tree species and, for comparison, those for a data set of Britishplant species. The topmost matrix refers to the subset of 381 Manu species occurring in two or more plots; the middle matrixrefers to the 314 Manu species occurring in three or more plots; the lowermost matrix refers to 160 plant species native tothe British Isles (British data from Rabinowitz et al. [1986]). The percentage of species in each category is given.
somewhere in relative abundance. In this section wediscuss how reliable these generalizations are forManu, and explore how relevant they may be to upperAmazonian forests in general. Extrapolating resultsfrom a partially sampled area of 400 km2 to a poorlyexplored forest of .106 km2 is surely an undesirableway to do ecology. Nonetheless, the size of the dataset and the consistency of the patterns at Manu en-couraged us to think big.
Geographic range
That most species appear to have large geographicranges is not a new observation for the Manu flora,whose species-level affinity with other Neotropical for-ests, even ones as distant as Barro Colorado Island inPanama, led Gentry (1990) to characterize the regionas ‘‘not very distinctive floristically’’ (Foster and Bro-kaw 1982, Foster 1990). Manu’s low rates of endemismlend support to Gentry’s (1992) characterization of nar-row endemism in Neotropical plant species as a phe-nomenon largely restricted to Caribbean islands, val-leys and hilltops along mountain ranges, and isolatedpatches of unusual edaphic conditions. It seems in-creasingly clear that this sort of endemism should nolonger be interpreted as evidence of refugia where spe-
cies persisted during colder or drier paleoclimates (Haf-fer 1969, Prance 1982, Salo 1987, Nelson et al. 1990,Colinvaux 1993, Bush 1994).
Considering how poorly explored upper Amazoniais, these data suggest that most tree species in upperAmazonia are cosmopolitan, ranging throughout thebroad crescent of forest at the eastern base of the An-des, from the Colombian to the Bolivian lowlands. Atleast 69% of the named species occurring in the Manuplots, for instance, have also been collected in Ecua-dor’s Amazonian lowlands, ;1500 km away, eventhough Amazonian Ecuador has been very patchily ex-plored by botanists (R. Foster et al., unpublished plantlist). Other authors have found similarly low levels ofendemism in upper Amazonian plant communities(Balslev [1988] for Amazonian Ecuador; and Young[1996] for the Peruvian department of San Martin).Perhaps this is to be expected, due to the relativelysimilar climatic and edaphic conditions throughout up-per Amazonia, deriving from the Andean orogeny. Iftrue, it will mean that ‘‘Rapoport’s rule,’’ which positsa decrease in the latitudinal range size of species withdecreasing latitude, is very weak at low latitudes forSouth American trees (Stevens 1989, 1992).
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Habitat specificity
Fifteen to twenty-six percent of the tree species inthe plots at Manu occur in only one forest type. Wethink that the lower figure is much closer to the truth,and that it may still be too high. The reason is thatsampling more area or more stems consistently turnsup species previously thought of as restricted growingoutside of their supposed habitat. Even so, the analysiswe present here is much too rough to settle persistentquestions about levels of habitat specialization in Am-azonian plants (e.g., Gentry 1986, 1988, 1990, 1992,Salo et al. 1986, Balslev et al. 1987, Prance 1994). Amore rigorous approach in preparation makes use of anull model to compare observed distributions of theindividuals of each species in different forest types withthe distributions expected if individuals were scatteredamong plots at random (though not entirely at random:a negative-binomial distribution helps model the localclumpiness of tropical tree distributions). We presentthe simpler test here for two reasons: first, because theresults of the two approaches have so far been verysimilar, and second, because the null model approachis sufficiently complex and problematic to require agreat deal of additional explanation.
While most species are not restricted to a given hab-itat, a majority do show some preference for certainhabitats, i.e., their abundances are higher in some foresttypes than in others. Thus by saying that a species isnot restricted to a single forest type we are not sayingthat its stems occur with equal likelihood everywhereon the landscape. What simple analyses like this onesuggest is that the habitat preferences of Amazonianplants are a matter of degree, and not as strict as sug-gested by earlier researchers. This complicates ideasabout what the habitat heterogeneity in the basin meansfor the speciation and coexistence of tree species, sincehabitat patches are unlikely to serve as isolated ‘‘is-lands’’ of suitable habitat (Salo et al. 1986, Tuomistoet al. 1995).
Fifteen percent is a much lower number than we hadexpected, given the ideas, widely held in the literature,that habitat specialization, or beta diversity, is extraor-dinarily strong in Amazonian tree communities (Camp-bell et al. 1986, Balslev et al. 1987, Gentry 1988,Prance 1994, Ruokolainen et al. 1995). In fact, betadiversity at Manu seems to be exceedingly weak. Manyearlier workers appear to have arrived at artificiallyhigh figures for beta diversity because the areas of for-est they sampled were not large enough to distinguishactual turnover of species between habitats from arti-factual turnover due to insufficient sampling.
Another possibility is that beta diversity is muchhigher in lower Amazonia (i.e., Brazil) than it is inupper Amazonia, due to the much more pronouncedenvironmental differences between flooded and un-flooded habitats as one travels eastward in the basin.Edaphic differences between the floodplain forest and
terra firme forest at Manu pale in comparison to thosebetween the same forest types in Brazil, where flood-plain forests are under water for a large portion of theyear and adjacent terra firme grows on old and highlyweathered soils. Thus it would make sense if beta di-versity were higher downstream than it is upstream,though this has yet to be tested.
Local population size
That 253 of the 829 species and morphospecies re-corded in the plots were represented by a single indi-vidual is a good illustration of the scale of the samplingproblems faced by tropical tree ecologists, even witha data set of .19 000 stems. Because the plots wesampled are too small to give a clear idea of localpopulation sizes, or of maximum local abundances, itis very difficult to judge how much of the observedpattern is representative of true community-wide spe-cies abundances, and how much is the result of insuf-ficient sampling. Are the 253 ‘‘singleton’’ species ac-tually rare, or did the 21 plots happen to fall in areaswhere they are poorly represented?
The answer to that question might shed light on theforces maintaining tropical tree diversity in nature. Ifcommunity drift sensu Hubbell and Foster (1986a) isthe dominant force structuring tropical tree commu-nities, one might expect species abundances to fluctuatestrongly at intermediate spatial scales within a foresttype. On the other hand, if fine-tuned biotic interactionscontrol the composition of communities, then speciesabundances should be roughly equivalent from site tosite. At least for one of the forest types in Manu, maturefloodplain forests, important aspects of species com-position and community structure are predictable atintermediate spatial scales (Terborgh et al. 1996).
Only a minority of the species recorded in the plotswere locally rare by our definition. Although our def-inition of rare is less conservative than the only otherdefinition we know of (Hubbell and Foster 1986b), theresult should not be misconstrued as a challenge to theview that tropical tree species are locally scarce. Any-one who has done field work in tropical forests cantestify that tropical tree species are locally scarce. Infact, calculating species densities for the entire areacovered by the plots (36.375 ha) demonstrated that 88%of species had ,1 individual/ha overall. The point isthat a majority of tree species occur at some localityin the Manu forest at densities higher than our thresholddefining rarity. If sampling were carried out throughoutthe ranges of these species, it seems inevitable thatevery species would follow suit. This result seems tobe only a consequence of the clumped local distribu-tions of tropical trees (e.g., Hubbell 1979).
Regional population size
One paradoxical result of these data is that tree spe-cies considered to be rare in Manu may be very abun-dant at large spatial scales. In other words, absolute
2658 Ecology, Vol. 80, No. 8NIGEL C. A. PITMAN ET AL.
population sizes of many locally scarce tropical treespecies in the Amazon basin may be very high. Con-sider a rough calculation to estimate how many adultindividuals of the rarest species encountered in theManu plots might occur in the department of Madrede Dios. The rarest species in the plots occurred at adensity of 1 stem/36.375 ha. Assuming that 90% ofMadre de Dios’s 78 415 km2 are covered by forest, andthat species densities are consistent enough across thedepartment to allow for reasonable extrapolation, onearrives at a figure of 200 000 adult stems in Madre deDios. When smaller stems are included, the total reach-es .106 individuals, and when one extrapolates to theremainder of upper Amazonia, the total becomes a tre-mendously large number.
The answer provides some perspective on how trop-ical tree species are rare (i.e., they are not rare in theway that black-footed ferrets are rare). The weakestlink of the extrapolation exercise is our understandingof how variable the densities of tree species are overthe large areas they occupy. Do species occur at roughlyconstant densities throughout Peru, or do they vanishentirely or dominate communities in some location oftheir ranges? Do species that occur exclusively in ma-ture floodplain forest at Manu also specialize in suchforests elsewhere in Amazonia, or are they found indifferent forest types altogether? Are generalists inManu generalists wherever they occur in the Amazonbasin?
Peruvian rarity and British rarity
We compared our results to those of a study of 160plant species native to the British Isles (Rabinowitz etal. 1986) and found a fundamental agreement under-lying the apparent differences between the two (see Fig.5). There are two major differences. First, 15% of theBritish plants sampled have small geographic ranges,while none of the Peruvian trees sampled do. Second,wide-ranging, abundant specialists were the most com-mon species among the British data set, whereas wide-ranging, abundant generalists were most common inthe Peruvian.
The differences appear to have simple explanations.The higher proportion of narrow endemics in the Brit-ish data set, for instance, is probably explained bothby much more extensive sampling in the British Isles,under which narrow endemics are more likely to bediscovered, and by the inclusion in the British data setof herbaceous species, which tend to have smaller geo-graphic ranges than trees. The high frequency of wide-ranging, abundant specialists in the British data set wasexplained by Rabinowitz et al. (1986) as a result of thepredominance of coastal species in the British flora.
Those differences obscure a fundamental similarity.In both data sets .75% of taxa fall into the same twocategories (see Fig. 5): the two boxes with large geo-graphic ranges and large population sizes. Consideringhow different the study sites are, we find the similarity
remarkable. The British Isles have a depauperate tem-perate flora, were buried under glaciers 18 000 yr ago,and have supported a dense human population in recenthistory. In contrast, lowland Peruvian forests have adiverse tropical flora that may have been affected bypaleoclimatic variation but not by catastrophic glaci-ation, and show no evidence of ever having supportedlarge human populations.
Then again, perhaps the results are not so surprising.Positive relationships between a species’ local abun-dance, the number of habitats it occurs in, and the sizeof its geographic range have been documented world-wide for a variety of taxa, and appear to be somethingmore than an artifact of sampling (McNaughton andWolf 1970, Hanski 1982, Brown 1984, 1995, Hubbelland Foster 1986b, Gaston and Lawton 1990; but seeGaston 1994). Given the consistency of the correlation,Rabinowitz (1981) was probably right in speculatingthat some of the seven forms of rarity are universallymore frequent in nature than others.
Limitations of the data and of the method
How representative of the entire data set were thetwo subsets of species we were able to analyze underthe Rabinowitz method? What degree of bias was in-troduced by excluding (1) species that lacked taxo-nomic identification, and (2) species that were repre-sented by fewer than some minimum number of indi-viduals?
The only variable for which substantial new data willbecome available as currently unidentified plants aregiven names is that of geographic range size. We thinkvery few of those will be confirmed as endemic toMadre de Dios. Only a tiny proportion of tree speciesknown from Manu are thought to be local endemics,if any at all (R. Foster, personal communication). Well-studied groups there contain few endemics. Of the 34species of Bignoniaceae that Gentry (1985) recordedat Cocha Cashu, for instance, none are endemic; the12 arborescent palm species occurring in the plots areall wide ranging in Amazonia (Henderson et al. 1995).Given how much of western Amazonia remains to bevisited by botanists, patterns of endemism in the regioncan only grow weaker.
While some of the unidentified specimens are un-described species, and may be undescribed preciselybecause they are endemic and thus poorly representedin herbaria, that is a small proportion of the taxa re-maining to be identified: for many years Manu has beenone of the best-collected sites in western Amazonia.The fact that many morphospecies remain unidentifiedto date has much more to do with the reluctance oftaxonomic specialists to identify sterile specimens thanit does with the taxonomic novelty of the specimens.Many of the currently unidentified species are in generathat are notoriously variable in vegetative characters(Neea, Inga, etc.), and our experience has been thatnew determinations mostly refer previously unidenti-
December 1999 2659TREE SPECIES DISTRIBUTIONS IN AMAZONIA
fied specimens to species already present in the dataset.
Excluding species represented by fewer than someminimum number of individuals introduces a muchmore appreciable bias in the results, especially withregard to local abundance. Maximum local abundancesreported in the first two matrices of Fig. 5 are notrepresentative of maximum local abundances in the en-tire data set, because the scarcest species were excludedfrom analysis.
This appears to be an inescapable consequence ofthe Rabinowitz method when it is used with purelyquantitative data. The problem is most acute in highlydiverse plant communities, where a large proportion ofthe species are represented by a very small number ofindividuals. The only solution is to sample more stems,thereby reducing the number of species to be excluded.
Ecology and conservation
Deciphering the ecological processes behind the pat-terns described above will require carefully designedfield experiments. In the meantime, the general im-pression is one of species that are broadly tolerant ofa range of nutrient and moisture levels, whose largegeographic ranges and lack of habitat specializationsuggest broad ecological niches rather than finely par-titioned ones. On the other hand, the apparent weaknessof niche-partitioning along nutrient and moisture axesshould not preclude marked specialization along otheraxes, like phenology, pollinator and disperser sym-bioses, or growth form.
The sort of rarity we report on here is far from theworst-case scenario of tropical conservation, i.e., pre-venting extinction among thousands of species, eachof which is locally rare, restricted to a single habitat,and confined to a small geographic area. Nonetheless,the scarcity of tropical tree species at small scalesmakes it clearer than ever that preserving them in theirnative forests will require very large protected areas(Hubbell and Foster 1986b).
ACKNOWLEDGMENTS
We thank the General Direction of Forestry and Wildlife(DGFF, now INRENA) of the Peruvian Ministry of Agricul-ture, and the administration of the Manu National Park, forpermission to conduct the research in the Manu BiosphereReserve. We are grateful to the many people who have helpedestablish and census tree plots in the forests of Madre deDios. This manuscript benefited from the comments of D.Livingstone, H. Tuomisto, K. Ruokolainen, D. A. Clark, M.Huston, the lab group of J. Clark, and an anonymous reviewer.Terborgh gratefully acknowledges financial support fromDuke University and the MacArthur Foundation. Pitmanthanks the Department of Botany at Duke University for fi-nancial support.
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APPENDIX
Distinguishing characteristics of 21 tree plots in Manu National Park, Madre de Dios, Peru.
118529 S 718219 W128039 S 718109 W118589 S 718139 W118529 S 718219 W
20.812511.6875
611693741310
157110
6188
51.231.928.723.1
9.65.05.35.4
86462332
23826
1122
Total swamp 5.5 3048 252 195.8 39 3
Grand Totals 36.375 19 252 825 1403.1 370 119
† Number of species occurring in no other plot.‡ Number of species defined as restricted to a single forest type, using the .2 plot threshold (see text for explanation).
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