Amazonian biotic data and conservation decisions

'Department of Vertebrate Zoology, ?Department of Entomology, 3Department of Botany, 4ADP Office, 5Department of Entomology, 5,6Departmentof Anthropology, 'Systematic Entomology Laboratory, USDA, c/o Department of Entomology 8Division of Fishes, National Museum of Natural History, Smithsonian Institution, Wahington, DC

We evaluate the utility of museum collections for conservation decisions by comparing re- cently assembled data sets on various taxa to an Amazonian indicator taxon, primates. Our data include one group of amphibians, two groups each of fishes and flowering plants, and four groups of terrestrial . In contrast to many other Amazonian groups, the taxa analyzed here and the primate indicator group are well-known taxonomically (few to no known undescribed species, no nomenclatural problems). We apply a suite of statistical and graphical methods designed to detect undersampling bias and nonrandom geographic pat- terns in the data. Our results indicate that: I) Some of the taxa in our data set are adequately sampled at the species level, others are not; and 2) all geographic ranges appear to be undersampled, including those for the indicator group. Currently available data adequately determine species richness at the level of the Amazon basin for heliconias, the plant Talisia, heliconiine and ithomiine butterflies, certain fish genera from both large and small rivers, the frog genus Leptodactylus, birds, and primates. In contrast, present data are inad- equate for the genera Agra, Batesiana, Deinopis, and Hemiceras. We recommend that similar suites of analytical techniques be used routinely to assess the adequacy of data prior to their use in making conservation decisions. We conclude that museum data are adequate to use for conservation purposes for certain Amazonian taxonomic groups, which is an encouraging finding. For taxonomic groups with data that fail the adequacy tests, we recommend a bottom-up approach of analysis using expert evaluation of the available data.

A uhhdade de coleqdes de museu para densdes acerca da conservaqdo poucas ou nenhuma especze ndo-descrrta e sem problemas de nomen- ambzenral foz avalzada por mero da comparaqdo entre dados recenres clarura) Lim conjunro de merodos esransncos e graficos foz aplrcado de vanos raxa e um raron bem esrudado de pnmaras da Amazdnza 0s aos dados para derecrar desvros produzzdos por amostras znsuficrenres dados zncluem um grupo de anfibzos, dozs grupos de pezxes, dozs gru- e padrdes geograficos nZo-alearorzos 0s resulrados rndrcam que I) pos de planras fanerogamas, e quatro grupos de artropodes rerrestres Alguns dos raxa do nosso conjunro de dados sdo adequadamenre Ao conrrarro de murros ourros grupos amazdnzcos, os raxa analzsados amostrados em nrvel de especze, outros ndo, e 2) para rodos os grupos e o grupo de prrmaras sZo raxonomzcamenre bem entendrdos (com as dzstrzburqdes geogra$cas parecem rncompleras, znclusrve as do gru-

Correspondence to: W. Ronald Heyer, .hphibians and Reptiles, Smithsonian Institution. 20560-0162. Washington, DC E-mail: [email protected]

372 - Cihcia e Cufiura Journalof the BraziIianAssochtion for the Advancement of Science Volume 51 (516) SeptemberlDecember1999 po de referincia (prrmatas). 0s dados disponiveis no momento indi- tecnicas de analise sejam usados rotineiramente para avaliar a ade- cam adequadamente. em nivel da bacra do Amazonas, a riqueza de quaqsdo dos dados antes de se fazer uso dos mesmos em decisdes de especles de helicdnias, plantas do giriero Talisia, borboletas conservaqsdo, Conclur-se que para certos grupos taxonbmlcos da Ama- (Heliconirnae e Ithoniinae), alguns gineros de peixes tanto de grandes zdnra, as cole~desde museu ssdo adequadas para utilizar para fins de como de pequenos rios, anfibios do gPnero Leptodactyhs, possaros e conservaqsdo ambiental, o que e encorajadol: Para os grupos taxonbmi- primatas. Ao contrario, os dados disponiveis no momento nao ssdo cos que se mostrarem inadequados nos testes, recomenda-se uma ano- adequados para os gineros de rnsetos e aranhas Agra, Batesiana, lise detalhada e curdadosa da informaqsdo disponivel usando-se avalr- Deinopis, e Hemiceras. Recomenda-se que conjuntos semelhantes de aqbes de especiabstas dos grupos.

he world's museums contain over two billion speci- also assumes that speciation and distribution patterns of mens (l), the largest source of scientifically verifi- lesser known groups correlate well with the best known able evidence on the Earth's biota. To an alarming groups. Others make the same kind of assumption on a glo- extent these data are all we reliably know about the bal basis (10). For purposes of this paper, we refer to this as T the indicator taxa approach, and the purportedly well-un- distribution and abundance of most species. Although each specimen and its associated data are potentially useful for derstood species that serve as proxies for the entire biota as conservation (and comprise all the data we are likely to have indicator species, taxa, or groups. The indicator taxa ap- in the short-term for many groups), museum data are gener- proach shares with the first approach the notion that groups ally assumed to be biased in various ways, even if those covary, although it does not spec@ why. Even absent evi- biases are rarely quantified. Species lists are suspected to be dence of covariation, the indicator taxa approach may still incomplete because most groups are undersampled, but to be justified simply because the indicator taxa data, by defi- an unknown extent. Apparent species ranges may be both nition, are most complete and free from the biases discussed undersampled and biased by patchy, nonrandom collecting. above. Even if collected, species may remain undescribed, But how are such indicator taxa defined? What quanti- misidentified, erroneously synonymized, or inaccurately de- tative criteria might place taxa (or, more exactly, our knowl- limited fiom other closely related species. All these errors edge of taxa) along a continuum from lesser-known to indica- prevent production of the accurate maps on which sound tor status so that more than just human favorites such as conservation decisions depend. Such problems are legendarily primates, birds, and butterflies might support conservation severe in the Amazon basin (e.g. References 2,3,4), the focus decisions? of this paper. Evaluating the completeness of inventories, lists, distri- One way around these problems is to use a theory that bution maps, and the like, whether for the species of a local predicts speciation and distributional patterns for all organ- community or whole lineages at regional or global scales, isms in the region of interest in hopes that its predictions involves the same general statistical problem-stimating from yield a realistic picture not obvious fiom the raw data them- a sample the number of unknown classes in a statisticalpopu- selves. For example, the forest refugia model (5) hypoth- lation (I I). The question is, how complete is the sample? This esized historical processes that should have affected all bi- problem has been the focus of increasing theoretical and em- otic distributions in Amazonia. During peak glaciation pirical research with encouraging results (12-24). cycles, the climate in most of the Amazon basin is thought We have been working with the neotropical lowland biota to have been cooler and drier. The predicted consequence and are interested in methods of objectively evaluating spe- was that the rain forest contracted to islands of habitat, or cies-level distributional data for use in making conservation refugia, within which differentiation of the isolated taxa took decisions. We are particularly concerned with assessing sam- place. Based originally on bird data, the model predicted pling completeness for areas where most of the biota is still that the conservation of these refugia would be particularly poorly understood, such as Amazonia. For such areas, even effective in conserving the forest-associated biota. How- rough, heuristic methods that help to evaluate knowledge of ever, refugia predicted fiom distributional data of other taxa would be useful. groups did not coincide convincingly with the bird-predicted In this paper we use statistical and graphical criteria to refugia (6,7). Since the forest refugia hypothesis, other evaluate the data assembled during our taxonomic revision- equally plausible hypotheses have been invoked to account ary work on ten Amazonian groups of vertebrates, plants, for the historical and recent distributions of the Amazonian and arthropods; we compare the results to those obtained biota (e.g. Reference 8). None of them are so convincing from Amazonian primates, a well-known indicator taxon. If that conservation decisions should be exclusively based data on species richness (total number of species) are ad- upon them. equate for conservation purposes at the scale of the entire A more common circumvention uses just those few Amazon basin for the indicator taxon, and any of our data are groups for which distributional data are thought to be rela- comparable, then our data should also be considered in con- tively complete and relatively unbiased to set priorities servation decisions. Our analyses indicate that at fher scales (biodiversity indicator species as defined in Reference 9). (e.g. detailed distribution maps of small areas), even indicator For Amazonia, primates, birds, and certain butterflies are taxa data may be inadequate. Faced with the reality of having generally considered to meet these criteria. Like general theo- partial data to make local conservation decisions in Amazonia, ries about lineage diversification in the basin, this approach we propose a protocol for resolving this dilemma.

Volume 51(516) SeptemberIDecember 1999 Cibncia e Cultura Journal of the Brazilian Association for the Advancement of Science- 373 A precise definition of "Amazonia" is to some extent from 348 specimens were included in the data set (34-40). arbitrary. For this study we defined Amazonia as the combi- Agra extends from southern Texas to northern Argentina, nation of the "Dominio equatorial amaz6nico" and the and is estimated to contain more than 2,000 species, 464 of "Dominio Roraima-Guianense" on Ab' Saber's (25) map. We which are described. It is the largest known monophyletic included any species with a sigdicant portion of its distribu- generic-level lineage among predatory . Possibly due tion (> incidental) within Amazonia and below 350 m. Some of to undersampling, very few species are known to have exten- these Amazonian species are truly rare in collections (i.e. few sive ranges. Even where canopy fogging has been used in records in total are known for a species), but others are rare the western Amazon basin for more than two decades at nine only within Amazonia (i.e. many more records for the species scattered localities, most Agra species are known from single outside Amazonia exist). In order to assess the impact of our localities, implying high species turnover or beta diversity. definition of Amazonia, we also recorded all extra-Amazonian Batesiana-Geballusa-Gouleta (Carabidae, Bembidiini), localities for the species in the dataset. a monophyletic lineage of three closely related genera, con- tains 65 species, of which 26 occur in Amazonia. Members of this lineage are associated with tree trunks, lianas, branches, The taxa and twigs, either standing or decaying on the forest floor. Co- occurrence of as many as eight species at a site is common in We selected taxonomically well-understood groups (usually the western Amazon basin. Distributional data were extracted genera) from our own ongoing systematic revisions, based on fiom 1,990 specimens. collections fiom the entire geographic range of the taxon. It is Hemzceras (: ) is a large group worth emphasizing that our taxa are well understood taxonomi- of conspicuous, exclusively neotropical , containing cally but are poorly to moderately sampled geographically. 230 species. Amazonia to date has 106 species of Hemiceras. Data were assembled for three genera of plants: Species can be either widespread or restricted and, for an Phenakospermum (Zingiberales, Strelitziaceae), a mo- , are commonly collected. Hemiceras have been reared notypic neotropical genus, is an arborescent herb widespread upon Leguminosae, the most important neotropical tree fam- in Amazonia (26). These distinctive palm-like plants grow to ily, especially fiom Inga (41). Distribubonal data were extracted over ten meters in height and occur in transitional habitats fiom 2,250 specimens. between tall rain forests and open areas of savanna and Deinopis is a poorly known pantropical spider genus. cerrado (27). Data are fiom 27 specimens. Six of the 15 neotropical species are undescribed. Deinopis Heliconia (Zingiberales, Heliconiaceae) contains ap- are stick mimics by day and web-spinning sit-and-wait preda- proximately 225 species, of which 95% occur from Central tors by night. They are among the largest of web-spinning Mexico to northern Argentina (28). These often large herba- spiders, but appear to be comparatively rare both in nature ceous plants are a conspicuous component of the flora of and in collections, and are certainly mcult to collect. The lowland primary and secondary tropical forests. Thirty two six Amazonian Deinopis species are represented by only 69 species (including two undescribed taxa) known from specimens from 55 localities. Amazonia are included in this analysis (29,30,3 1,32), taken Data were assembled for Amazonian representatives of from 822 specimens. Although most of these species are re- one genus of frogs, two groups of fishes (one typical of large stricted to this biogeographic area, the main distributions of rivers, the other of small river systems), and 37 species of several species occur elsewhere in the Neotropics. Amazo- platynine monkeys. nian Heliconia are relatively well-known taxonomically (3 1,33). Leptodactylus is a neotropical frog genus with 14 well- Talisia (Sapindaceae) in the Amazon contains 36 spe- defined species occurring in the Amazon basin. Data were cies, all of which are included in our analysis, based on 4 11 extracted from Heyer (42,43,44), supplemented by museum specimens. These species occur within the Amazon basin, data obtained after the respective revisions were published. with a few extending into surrounding non-Amazonian low- A few other species of Leptodactylus occur in Amazonia, but lands. Talisia are monocaulous shrubs to large trees mostly neither their species limits nor distributions are well defined of nonflooded lowland forest (< 500 m elevation), but also at present (e.g., L. didymus and L. mystaceus are diagnosable occur in seasonally flooded varzea forests. They are scat- only by advertisement calls and have poorly understood dis- tered throughout the forest, never dominating the habitats in tributional limits) (45). The 14 Leptodactylus species occur which they occur. About 70% of the taxa used for this analy- collectively in forests and open habitats. They are often com- sis are taxonomically well understood, but 30% are incom- mon and easy to collect; their distributions are among the pletely known from fragmentary collections. Twelve taxa are best understood for frogs in Amazonia. Data extracted from currently known from more than ten collections, while the revisions are based on examination of more than 5,600 indi- vast majority (30 species) are known from less than eight viduals. collections; seven are known from one collection only. Steindachnerina and Cyphocharax (Curimatidae) Data were assembled for Amazonian representatives of (46,47),Boulengerella (Ctenoluciidae) (48), and Caenotropus six arthropod taxa: Four genera, one genus, and (Chilodontidae)(49), are four fish genera characteristic of large one spider genus. rivers. Thirty-three species of Steindachnerina and Agra (Carabidae, Lebiini) to date contains 101 species Cyphocharax are hstributed within the Amazon basin, but with ranges withAmazonia. Distributional data extracted some range beyond the basin. These detritivorous curimatids

374 CMciae CuItura Journal of the Brazilian Ass~~~~air~onfor the Advancement of Science Volume 51(516) SeptemberiDecember 1999 inhabit dikerse habitats in lowlands and lower elevations. Each distinct combination of latitude and longitude in the Amazonian Boulengerella comprises five species of large data was considered a dtstinct locality. Multiple collections predatory characiforms, again typical of large rivers. or specimens of the same species (or subspecies, in some Caenotropus is a lineage of herbivorous and spongeeating cases) with the same coordinates represent repeat collections fishes. The data for these three groups are among the most from the same locality. The data set was thus a list of all thorough for any broadly distributed Amazonian fishes. Data observed localities for all taxa. From these data we calculated: are based on 785 specimens of Boulengerella, 1,620 of a) The total species richness at a locality (again, to the near- Caenotropus, 4,10 1 of Cyphocharmc, and 1,221 of Steznda- est minute); b) the number of unique collecting localities chnerzna. (which might include various taxa); and c) the total number of Nannostomus (Lebiasinidae, Nannostomina) is a genus dtstinct records (two species from the same locality represent of small river fishes with 15 well delimited species in the Ama- two records). zon basin, six of which range either into the Rio Orinoco ba- As noted above, we included the extra-Amazonian lo- sin andlor into the Guianas. Data are based on 1,706 speci- calities for a species if part of its range fell in the Amazon mens. Distributional data are from published (50-55), and some basin, in order to assess the effect of our definition of the previously unpublished records. Most Nannostomus species Amazon. The graphical criteria we wish to apply (19) require inhabit lowland forests, often slow moving blackwater or that point data be grouped in samples or quadrats. We chose clearwater streams. Some species occur in lowland savannas onedegree on a side (latitude or longitude) cells as sample and at least two can also be found in slow moving whitewater units. One degree at the equator of either latitude or longi- channels along the Rio Amazonas. Data are adequate to in- tude is roughly 111 km.As we have defined it, Ab'Saber's clude 7 species from the lebiasinid tribes Lebiasinini and Amazonzan morphoclimatzc domain (25) contains all or part I'yrrhulinini. One species of Lebiasinini occurs in the Ama- of 472 grid cells. If a grid straddled the domain boundary, all zon basin along the eastern base of the Andes in Ecuador localities within the grid were included in the dataset. and Peru. The F'yrrhulinini are widely distributed throughout We used Estimates, version 5.0.1 (19) to assess the de- the Amazon with some species extending beyond the basin. gree of undersampling and spatial aggregation (clumped col- All species in the group are small, primarily insectivorous lecting effort) in the data. This program computes randomized fishes occuning mainly in quiet backwater portions of small species accumulation curves, and reports the mean of various forest streams in clear or blackwaters. A few inhabit lakes, statistics based on those curves. It includes a variety of spe- close to shore, and swamps and small streams in savanna cies richness estimators and graphical techniques to detect areas. Data for Lebiasinini and Pynhulinini are based on 3,3 18 patchiness in data. For each estimator Pielou's (66,67) pooled specimens. quadrat method is used to depict graphically the behavior of The final data set for thls study includes neotropical the estimators and indicator of patchiness as sample size in- primates, thus pennimng direct comparison of the above taxa creases (20). In the ideal case of a complete inventory, the with an indicator group. Data from 37 primate species based observed species accumulation curve climbs asymptotically on at least 4,500 specimens collected in 2,055 localities in to the mespecies richness in the area being sampled, but the Central and South America were extracted primarily from estimators asymptote much sooner than the observed curve. Hershkotitz's revisions (5664). Estimates includes richness estimators based either on The distributional data were assembled in final fashion relative abundance or incidence. Abundance-based estima- on 27 June 1995. Few new locality records or taxonomic re- tors require relative abundance of species withn and between finements have appeared since then, and these do not mate- samples. Incidence-based estimators require just presence1 rially affect our results or conclusions. absence of taxa within quadrats or samples. While the num- ber of times a species has been found at a particular locality is often viewed as a measure of its relative abundance, accurate Analysis measures of relative abundance are notoriously difficult to obtain and are more likely to be biased than incidence data For mapping and other geographic purposes we chose the (68,69). We prefer to be conservative and treat the data as a Plate Caree projection as a base map for three reasons. First, matrix of presencelabsence scores of species by Amazonian it minimizes distortion in the equatorial region. Second, it cor- localities. Therefore we used the incidence-based Chao2 es- relates precisely with the maps in Cartesian space produced timator (13,20) and incidence-based coverage estimator ICE by statistical programs. Third, it pennits later grid- or raster- (13,16) to estimate species richness and to assess based analyses of the area. The coastlines, rivers and politi- undersampling bias. Both estimators augment the negatively cal borders were derived from the Digital Chart of the World, biased observed richness by a factor that depends on the generalized to a scale of 1:25,000,000 using the MundoCart presence of and distribution within samples of "rare" taxa. By program (65). defimtion, when all species in an inventory have been ob- To produce point maps of species or taxa we used mu- served multiple times (i.e. are not "rare"), the inventory is seum locality data to determine longitude and latitude to the complete. Conversely, inventories replete with "rare" species nearest minute, and converted these values to decimal de- underestimate true richness. For the Chao2 estimator, "rare" grees as used by the ArcDnfo GIs program. A minute of ei- species are those observed in only one or two samples; once ther latitude or longitude at the equator is roughly 1.8 km. all species are known from two samples or more, the estimate

Volume 51(516) SeptemberIDecember 1999 Ciencia e Cultura Journal of the Brazilian Association for the Advancement of Science 375 will equal the observed richness. The ICE estimator is more then recalculates the species accumulation curve. Any ag- complex and uses more information than just ones and twos, gregated pattern in the data, real or artifactual, is destroyed, but the logc is basically the same. We used Estimates, ver- which thus yields a "null" curve based on random placement. sion 5 .O. 1's default values for number of randomizations and If the empirical curve (mean of randomized accumulation cutoff values for coverage-based estimators (50 and 10, re- curves without reassignment of specimens) differs substan- spectively). tially from the Coleman curve, then aggregated occurrences Although these richness estimators are nonparametric, of species in particular andlor adjacent samples affects the they do assume random sampling. Unfortunately their sensi- shape of the accumulation curve, which in turn will affect tivity to departures from random sampling has not yet been estimates of species richness based on it. Conversely, if the studied, particularly as regards species accumulation curves empirical and Coleman curves are nearly the same, then ag- and the like. Given the well-known difficulties in accessing gregation in the data is less of a problem for statistics that the more remote regions in the Amazon basin, the random depend on the empirical curve. We used Coleman curves to sampling assumption is unlikely to be valid, even for the pri- detect spatial aggregation in the data for all studied groups, mate data. In practice it is diflicult to distinguish between real including primates. We also calculated the Poisson index of and amfactual spatial aggregation in data, because biologi- dispersion to test for spatial aggregation (71), although, as cal populations and species ranges are, in fact, very often noted above, this cannot distinguish between real and arti- spatially aggregated. This, of course, makes a truly random factual aggregation. sample (equal probability of sampling each individual) diffi- In summary, primates are an indicator taxon in the sense cult, if not impossible, to achieve (68,69,70,71). Furthermore, that they are generally considered to be well-known taxo- biologists in general, much less museum collections, do not nomically and wellcollected throughout the Amazon basin. usually track evidence of absence, whlch is thus difficult to The above criteria provide a means to evaluate objectively distinguish from absence of evidence. Much sampling effort data of this sort for application to conse~ationdecisions. in the Amazon has not been recorded (see below, however). When applied to the primate indicator taxon data, these sta- It does seem likely that museum data on rarer species is rela- tisticallgraphical approaches provide a standard against tively less biased than for more common species, because which data on candidate groups can be compared. collectors tend to skip common and concentrate on rare or unusual taxa. Museum collections do represent the sum total The total data set contains 6,27 1 records, representing of a huge number of statistically independent events that 422 distinct taxa among 3,930 unique localities. Ofthese, 4,455 vary in all kinds of ways. Perhaps a more practical question is records (2,618 unique) are within the 472 Amazonian one- how to measure the effects of spatial aggregation on species degree grid cells (Table 1). accumulation curves and estimates of species richness, rather Our individual data sets vary considerably in terms of than to what extent it is real or amfactual. number of species included, number of localities known for Estimates 5.0.1 includes techniques to assess graphi- the species involved, and the number of species known from cally the degree of spatial aggregation in data. A Coleman a single locality in Amazonia (Table 1). As such, they are curve (17,18) randomly reassigns specimens to samples, and broadly representative of Amazonian biotic data.

Table 1 - Characterization of Amazonian species/distributional data broken down by taxonomic groupings.

Mean Maximum Total Total Total unique # Of species # Of species Total Total records records unique Amazonian Amazonian known from known from Taxon species records per species any species localities records localities one record onegrid cell

Arthropods Agra 101 155 1.5 9 85 148 85 7 0 7 1 Bates~anagroup 26 116 4.5 28 54 115 5 3 7 7 Delnop~s 6 37 6.2 12 36 12 12 1 1 Hem~ceras 106 888 8.4 37 319 374 8 1 2 2 22

Vertebrates Leptodacrylus 14 942 67.3 202 756 6 15 455 1 1 Primates 37 2002 54.1 189 1372 1537 980 1 1

Large river fshes 41 719 17.5 64 489 628 414 ' 1 1 Small river fishes 22 262 11.9 33 234 251 223 1 2

------Plants Tahsra 36 3 19 8.9 6 2 275 234 191 5 6 Zingiberales 33 83 1 25.2 58 643 541 403 1 1

Grand total 422 627 1 11.8 202 3930 4455 2618 110 112

376 CSnciae CuIhrra Journalof the Brazilian Association for the Advancement of Science Volume 51 (516) SeptemberIDecember 1999 As expected, primalcs are known from many more locali- ample; of all Laxa treated here. the carabid genus ilgra prob- ties than any other taxon (2,002 in all, 1,537 in Anatonia). The ably has the most species, and is relatively the most nexl most collected tasa are knon~nfrom about half as niany undersampled. The set of curves in Figurc 2A has a number localities (Table 1). The collecting intensity for primates is of characteristics that confirm this impression. First, thc em- high (54.1 localities per species). Despite only hallas Inany pirical species accuunulation cumre (Sobs) is nearly linear. Sec- localitics as for primates, the lrog genus Leptodaclylzis has ond; the gap between it and either richncss estimate (ICE ,and been collccled more intensely (67.3 localities per spccies (Table Chao2) is so large that evcn the richncss estimators, which 1)). All primate species but o~ucare known from two or more amempt to correct for undersampling bias, are probably still, localitics; but this is also true of six out of the ten other g~oups at best: lowcr bound estimates. Thrd, the cuuves lor uniques in the data set. By these mcasuues the primate data are no1 and duplicates (species occurring in just one or two samples markedly different from some ol the other groups included (19). respectively) increasc monotonically. The vast majority here. of reasonably pristine spccies ranges include at lcast two Amazonia is unevenly sampled. When nonprimate locali- distinct museum localitics (i.e., latitudes or longitudes differ- ties are plotted for all 385 tasa, the historical impact of primary ing by one degrce or more); so this is, again, good evidence access to Amazonia by major rivers is obvious (Fig. 1). Bota- of undersampling. The abundance of "rare" species (uniques nists do seem to have made a greater elfort to collect behveen and duplicates) in the samplc suggests that many morc spe- major rivers. cies of Ag/,a await discovery, and that thc ranges of thc kilolvn species are probably grossly undereslimated. In contrast the primates. zingibers (Phenalospe/.nninz arid UndersampIing bias Helicor~ia),thc frog genus LeptodacQlzw, and large river fishes sl~olvsigns olbeing relatively well-known (Figure 2E,G,I,K). Statistical and graphical tesls for undersampling bias con- Thc richness estimates and the observed species curve es- form to our a priori, inkutive expectations (Fig. 2). For es- sentially coincide and arc nearly flat by the end of the sample.

Figure 1. Locallties of :?oilprimate taxa in iirnazonia (.sqztai.esj all fishes: (ti-iai~gles)all plants, (cii.cles) amphibiails, (stai..s) all aitkropods

Volume 51 (516) SepternberlDecernber 1999 Ciencia e Cultura Journal of the Brazilian Association for the Advancement of Science 377 350 - 8) Batesiana-Gouleta

- Duplicates

0 10 20 30 40 50 0 10 20 30

Ej Large River Fishes F) Small River Fishes

I) Zingibers

Number of Grid Cells

Figure 2. Species rrchness eshmators and patchiness indicators for 64) species of the canopy beetle genus Agra. (B) specres of terrestrral beetles of the Bntesiana group, (q moths of the genus Hemiceras, (Dj spiders of the genus Deinopis. (E) specres of large river fishes, (F) species of small river fishes, (G) species of the frog genus Leptodactylus, (H) species of the plant genus Talisia. (0 Zingiberales based on localrtres of specres delrmited ruithrn Amazonra, (J) all Amazonian and extra-Amazonran localities for Zrngrberaies that occur in Amazonia. (K) prrmates

378 CiSncla e Cultura Journal ofthe Brazilian Association for the Advancement ofScience Volume 51(516) SeptemberIDecember 1999 . .~nvivonwent and ~iodive~sitp..

C) Hemiceras

Number of Grid Cells based on localrlres delrn~rtedwrthin Arnazonia. (L) all flmazonlan and extra-Amazonran localrtres that occur in Amazonra. Sobs = en~prrical species accrirnzilation curve; ICE - coverage estimator of Chao and J.ee (14); Chao2 - incidence-based esfimator of Chao (13); Cole - Colemci??curve, a patchiness rnd~catnr,of Colen~crn(I 7); uniqzies = nlimher of specres occzri,ring in just one grid cell; dziplicates = nuniber of specres occur,ring in just hvo grid cells.

Volume 51 (516) SeptemberIDecember 1999 Ciincia e Cultura Journal of the Brazilian Association for the Advancement of Science 379 In fact, these Amazonian groups are arguably oversampled by collecting effort (number of localitieslgrid cell). In sum- as far as a rough estimate of the species richness is con- mary; the vertebrate and plant data probably reflect biologi- cerned. The behaviors of the "rare" species curves (uniques cal reality much more faithfully than the arthropod data. Pri- and duplicates) are typical of putatively complete invento- mates are well-known and well-collected, but our plant and ries. Early on, the uniques curve rises faster than the dupli- vertebrate groups are known nearly as well. In contrast the cates curve. Additional sampling eventually converts uniques patterns shown by poorly known and undercollected groups into duplicates, and duplicates into triples or higher frequen- (arthropods) differ in consistent, sensible ways. Patterns cies. The uniques curve thus declines faster than the dupli- shown by such taxa may not be spurious, but they should be cates curves and may even cross it, but both tend towards used carefully and critically. zero when no species remain to be discovered and almost all species are known from two or more localities. The other tam in the study fell between these two extremes. Among Spatial aggregation arthropods, the Batesiana group and Hemiceras (Fig. 2B,C) seem much better known than Agra (note the dfierent Y-axis When tested using classical statistical techruques (Poisson scales). The curves for Deinopis illustrate the very earliest index of dispersion I), collections for all of these Amazonian stages in knowledge of a taxon, when sample data are so tax& either separately or together are highly clumped (p < 0.000). sparse that statistics based on accumulation curves vary This result is not surprising, but it is dficult to spec@ how widely. much is due to biased sampling versus biological reality. The The cunles for zingibers and primates illustrate how a Coleman curves (which provide a picture of the data as if strict geographic definition of Amazonia can distort interpre- individuals were distributed and had been sampled at ran- tation of biological patterns. Zingibers are fairly well collected dom) in all cases closely follow the obsenred (Sobs) curves (25.2 localities per species; 403 Amazonian localities for 33 (Fig. 2). Because Estimates repeatedly randomizes sample species), but the observed and estimator curves (Fig. 21) are order as it computes statistics (here 50 times), it provides a still rising by the end of the sample, and the uniques curve is standard deviation for each statistic as each sample is added level rather than declining. Primates (Fig. 2K) show the same to the curve. If hvice the standard deviation of the Coleman symptoms. If all extra-Amazonian records are added, how- curve is taken as a rough confidence interval, in all cases the ever, the curves show the typical signature of nearly com- observed cunles fall within these limits. Hence, the estimator plete inventories (Fig. 2J, L). Some Heliconia and primate curves for species richness seem little affected. despite the species are primarily non-Amazonian taxa, at least as we de- obvious spatial aggregation in the data (Fig. 1). fine it, though they do occur in Amazonia. When records The Coleman curves do show evidence of patchiness, outside "Amazonia" and above 350 m are deleted, these spe- however. even if the effect is slight. For all the plant and cies are artifactually rare; additional random sampling in vertebrate data (except large river fishes) the observed curves Amazonia would be quite unlikely to encounter them. Limit- fall below the Coleman curves. This is because the relatively ing the analysis to just Amazonian records distorts the re- rare species occur in disproportionately few samples (i.e. are sults for these taxa in a characteristic and logical way. aggregated). When randomly dispersed among samples in While apparently not as complete as the primate, large the Coleman curves. the probability of encountering these river fishes, Leptodactylus, and

fifths of the variation in local Figure 3. Pior of number- qf species (exclr!drng primares) agarnsr unique localrrre~for one degree per-grid cell richness can be elplained grid cell5 rorrhin krnazonra Indivrdtrai symbols may r-epreserir more than one data pornt.

380 Ciincia e Cultura Journal of the Brazilian Association for the Advancement of Science Volume 51 (516) SeptemberIDecember 1999 species earlier in the accumulation increases so that the accumplation curves for "rare" species. These quantitative Coleman curve tends to rise a bit faster than the observed criteria can be used to judge the quality of other taxonomic curves. inventories, and thus to rank taxa along a continuum of knowl- Spatial aggregation does affect estimates of species edge. For the groups considered here, zingibers: the frog ge- ranges however. Taxonomically undersampled groups are in- nus Leptodactylus, and the fish genera typical of large rivers evitably undersampled geographically. The detailed ranges seem about as well known as primates. The same criteria indi- for all species analyzed herein are unknown. Some of the cate that the arthropod taxa analyzed here are much less well- groups included here included common species, which al- known, although among those the Batesiana group of cara- most certainly occur in many more grid cells than Figure l bids and the noctuid genus Hemiceras are better known than shows. About one fourth of the Amazonian grid cells (1 13 of the others. The sapindaceous genus Talisia, and fish genera 472) contain no localities for any of the groups investigated typical of small rivers are intermediate. The statistical estima- here. This is due to lack of sampling within those grid cells, tor results are best for the data sets with the most localities not lack of species within them. These results suggest that per species and worst for the data sets with the fewest locali- for the grid cells that have been sampled, patchiness of col- ties per species. lections seems not to be a severe problem. However, the pres- The initial concern that collecting records for the Ama- ence of unsampled gnd cells does pose problems in under- zon basin are so biased geographically as to invalidate the standing individual species distributions and contributes to sort of analysis attempted here is mitigated by the close agree- geographic undersampling for all of our individual data sets. ment between observed curves and the Coleman curves from which all traces of aggregation have been removed. While it is possible that the Amazon still harbors new species of hese results show that museum collection data (or other groups as well sampled as primates, the percentage of new Tsuch inventory data) can be analyzed quantitatively to species should be small. At a more general level, the Amazon gauge the relative completeness of taxonomic inventories. basin has been and remains one of the largest and most inac- As expected for the indicator group of primates. the curves cessible land areas in the world. Museum collection data in suggest that nearly all Amazonian primate species are known. other areas should be much less patchy, and thus the meth- Evidence for this is the asymptotic behavior of the species ods used here to assess indicator status should work even accumulationand richness estimation curves, their near equal- better if applied elsewhere. Of course the analyses used here ity when all data are included, and the prdctable behavior of depend on new statistical techniques which themselves re-

Figure 4. 'Map ofneorro- prcal lowland prrmate colleclrng srtes.

Volume 51 (516) SeptemberIDecember 1999 Ci&nciae Cultura Journal of the Brazilian Association forthe Advancement of Scienceo 381 quire more testing before their strengths and weaknesses are In summary, conservation decisions in Amamnia should really understood, in particular their robustness when as- be based on more than one or two well-known and collected sumptions are strained or violated. (indicator) taxa, because the data for a number of other taxa are just as good, at least at the level of the entire Amazon basin. In addition to birds, heliconiine and ithomiine butter- Amazonian indicator groups flies, and primates, we can use several fish genera from large rivers, Leptodactylus, heliconias, probably aquatic beetles Amazonian bird, heliconiineand ithomiine butterfly, and pri- (74), scarab beetles (75), tiger beetles (76), mosquitoes mate data are generally considered more robust than data for (77,78,79), lizards (80,8 l), the plant familes Chrysobahaceae other Amazonian groups and one might argue that these (see references in Reference 4), Lecythdaceae (see references groups should be used preferentially to make conservation in Reference 4), and Palmae (82). The data for certain fish rkommendations. Two critical aspects contribute to the util- genera from small rivers and the plant genus Talisia can be ity of Qstributional data for making scientifically based infer- used with some caution. By contrast, taxa such as Agra and ences: I) The species-level must be accurate; and Deinopis are too seriously undersampled taxonomically and 2) geographic distributions must be correct. geographically over the entire basin to support conservation Amazonian birds, heliconiine and ithomiine butterflies, decisions, at least on their own. An additional point is that and primates are well-known taxonomically. The suggestion the graphical methods of analysis demonstrated here can be that distributions for these groups are equally well under- applied at any geographic scale to test for adequate taxo- stood is doubtful, however. Raymond A Paynter Jr and asso- nomic sampling and the effect of spatially aggregated samples ciates have recently published a series of ornithological gaz- on patterns in species richness. etteers for Latin America. Their maps of collecting localities We emphasize that the most simcant finding of this show that Amazonian bird locality data are as dominated by paper is that there are several taxonomic groups with ad- river access as ours. For example, Brazilian Amazonian col- equate museum-associated data to use for species richness lecting localities are sparse (72) and, as expected, most of analyses at the level of the Amazon basin. Species richness those are near the major rivers. The butterfly data are similar, is an important piece of information in making informed con- except that the road transect from southeast Brazil to Porto servation decisions. There are many groups in Amazonia that Velho has been well-sampled (73). The primate data are mar- remain undersampled, as is true also for other relatively un- ginally better than our nonprimate data, but again with es- known geographic areas. In the following section, we dis- sentially all collecting localities restricted to the major rivers cuss how incomplete data can be used to make conservation (Fig. 4). The richness estimator and the Coleman cwve re- decisions. sults for primates (Fig. 2K,L) are similar to those for Leptodactylus and Zingiberales (Fig. 2G,I,J), and large river fishes (Fig. 2E). Taxonomically the latter groups are just as Local Amazonian conservation well-known as any of the indicator taxa. Historically rivers provided about the only access within Increasing ecosystem degradation or loss within the Ama- Amazonia. As a result, all Amazonian taxa suffer from geo- zon basin means that conservation will be applied at increas- graphic undersampling. Only recently has it been practical to ingly finer scales, whereas problems of geographic undersam- consider alternatives, and thus to ask if the classical strategy pling worsen at finer and finer geographic scales in Amazonia. via rivers is an adequate way to sample Amazonian biota. To formulate local conservation recommendations in the ab- The rivers do provide a vast network overlaid on the entire sence of adequate geographic data, we recommend a proto- basin. Therefore, adeqizite sampling (as illustrated above) of col that follows the philosophy laid out by Shrader-Frechette taxa throughout Amazonia via the rivers may nevertheless and McCoy (83). They argue that topdown, theoretically provide reasonably complete pictures of species richness. inspired solutions to ecologically based conservation prob- This conjecture presumes that the effect of rivers diminishes lems have not worked, and in many cases should not be ex- rapidly with distance for most taxa - that is, all major kosys- pected to work. Rather, the bottom-up case study approach tem types in Amazonia occur within walking distance of ac- has been much more successful and is likely to be more pro- cessible riverbanks. With satellite imagery it should be pos- ductive. We recommend that localized conservation decisions sible to determine how many, if any, ecosystem types be- for Amazonian areas be made on a case-bycase basis, with tween rivers (which might harbor new species) do not also knowledgeable experts evaluating the available data. A sci- occur along them. entific rationale for this approach can be shown with frog and Other robustly sampled groups certainly exist. Some of primate examples. them are adequately understood taxonomically and are thus Suppose that a discrete area (1,000 - 10,000 km?) within ready to be used. Others, such as bufonid and hylid frogs are Amazonia is being evaluated for possible protection and that probably adequately sampled, but poor taxonomic understand- the distributional data for frogs are incomplete (nearly al- ing diminishes their utility in this context. Focussed research ways the case at present). Almost any list of frog species to bring such groups to an acceptable taxonomic understand- from such an area could erroneously suggest high levels of ing would be a very cost-effective way to improve the scien- endemism, because frogs as a whole, unlike Leptodactylus, tific knowledge base of Amazonian conservation. are still poorly sampled. However, an expert Amazonian her-

382 * CEmk e Cuhra Journal of theBniziIianAssociatiion for the Advancement of Science Volume 51 (W6)September/December 1999 petologist should be able to make some reasonable infer- western portion of the range, S. m. niger, has been collected ences from a species list and associated information. For ex- at only 19 of 75 localities within its putative range. The prob- ample, it should be obvious whether night collecting occurred, ability, p, of collecting it at a randomly selected site is then 191 and how thoroughly forest habitats had been sampled (ver- 75, or0.25. Theprobabilityofnot collectingit is 1 -p, or0.75. sus open river edge habitats etc). The frog fauna is reason- The latter value is the probability of not finding this species ably well-known at roughly eight to ten scattered localities at a locality within its western range, even though it occurs across Amazonia (most of these coincide with the highest there. In the onedegree wide strip west of the rio Xingu, species richness gnd cells identified in a companion paper primates have been collected at seven localities. The prob- (84) (see Fig. 1). Comparison of the target area list with the ability of not finding this tarnarin west of the Xingy even if it nearest completely censused site should indicate ifthe target were to occur there, is thus (1 - p)" = 0.75' = 0.13. The rio site is really different or unusual, or ifthe differences are due Xingu may be a barrier for this species, but the evidence is to undersampling. About 18 widespread frog species occur not compelling. throughout Amazonia. Complete inventories at any site should The bottom-up approach to conservation using expert probably contain all 18 species. Knowledge of the collectors evaluation of many independent cases has an important limi- and the weather conditions can help to assess the quality of tation. Different Amazonian groups show different biotic pat- the list. Transects through alternate regions can provide in- terns. Therefore, the more taxonomic groups (and experts) formation on appropriate breeding habitats under suitable that contribute to the analysis, the more robust the conserva- climatic conditions. Zimmerman and Bierregaard (85) have tion recommendations are likely to be (see also References shown that elements of the Amazonian forest frog fauna de- 86,87, for non-Amazonian examples demonstrating that the pend on patchily distributed breeding habitats that are readily distributional data for one taxon does not predict patterns in recognizable by humans. Finally, even if available data are other groups). Taxonomic expertise on Amazonian groups is misleading or unreliable, a knowledgeable herpetologist, given very limited. Given the amount of time and resources it would the available data, should be able to specify what fieldwork take to improve the Amazonian distributional database ver- will most quickly provide the data required to make recom- sus training more experts to evaluate the available data, one mendations. short-term solution seems to lie in training more experts. A knowledgeable specialist can also use a probabilistic In conclusion, we suggest that species and geographic approach to assess distributional limits and lacunae using undersampling can be detected graphically, and that such taxon-specific locality data. For example, the origmal primate assessment should be routinely applied whenever the scien- data set fkom which the Amazonia taxa data were extracted for tific data underpinning conservation decisions might suffer this study includes 140 subspecies and 5 1 species from 2,100 from such problems. Further, we suggest that to rely on a few localities in Central and South America. For each species socalled indicator taxa is both scientifically indefensible and throughout its expected range we counted the number of lo- unnecessary. We iden* several taxonomic groups that have calities where it was collected and where it was not collected, as robust data as Amazonian indicator taxa. Data from all of but where other species of primates occur. From these counts, these groups should be used to make conservation decisions we calculated the frequency of sites @) at which each spe- in Amazonia. Finally, we suggest that even when data are cies was collected within its range. Thus, the probability that imperfect, as they are likely to be at more local scales, several it would not be collected at such a site is (1 - p). These prob- critical approaches can still assess the quality of species lists abilities can then be applied to an area in which a species is and maps in order to optimize the allocation of scarce conser- apparently absent to infer whether the absence is real or due vation resources. to undersampling. If the number of collecting sites is (n), then the probability that the species occurs there but has not yet been collected is (1 - p)". References and notes This approach assumes that collecting effort has been approximately the same in all areas. If some sites were inten- 1. Duckworth WD, HH Genoways, CL Rose 1993 Preserving na- sively collected and others casually, the computed probabili- ture science collections: Chronicle of our environmental heri- tage. National Institute for the Conservation of Cultural Prop- ties will be biased. However, ths bias can be measured by erty, Washington, DC comparing the number of specimens collected per site in vari- 2. Nelson BW, CAC Ferreira, MF da Silva, ML Kawasaki 1990 ous areas. Also, known associations between primate spe- Endemism centres, refugia and botanical collection density in Brazilian Amazonia. Nature 345: 71 4-7 16 cies can reveal bias due to differential collecting effort in two 3. Heyer WR 1988 On frog distribution patterns East of the areas. For example, if squirrel monkeys (Sarmrrr) and spider Andes, p 245-273. In Proceedings of a workshop on neotropical monkeys (Ateles) were collected with equal frequency in both distributron patterns held 12-16 January 1987. PE Vanzolini, areas, then it is likely that the habitats do not differ greatly. WR Heyer eds, Academia Brasileira de Ciencias, Rio de Janeiro 4. Williams PH, GT Prance, CJ Humphries. KS Edwards 1996 Prom- Speclalist expertise is required to recognize and evaluate these ise and problems in applying quantitative complementary areas assumptions adequately. for representing the diversity of some neotropical plants (fami- In the case of the tamarin, Sagurnus mrdas, Hershkovitz lies Dichapetalaceae, Lecythidaceae, Caryocaraceae, Chrysobala- naceae and Proteacea). Biol J Linnean Soc 58: 125-157 (58) shows the Rio Xingu as the western boundary of the 5. Haffer J 1969 Speciation in Amazonian forest birds. Science range of this species. Is the Xingu really the western edge of 165: 131-137 the range of this tamarin? The subspecies that lives in the 6. Brown KS Jr 1987 Conclusions, synthesis, and alternative hy-

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71. Ludwig JA, JF Reynolds ' 1988 Statistical ecology. Wiley indicator taxa and effects of habitat modification in tropical Interscience, NY forest. Nature 391: 72-76 72. Paynter RA Jr, MA Traylor Jr 1991 Ornithological gazetteer of 88. Acknowledgements: This investigation is a product of the Neo- Brazil: M-Z, bibliography. Harvard University, Cambridge tropical Lowlands Research Program (RP Vari, Principal Investi- 73. Broy KS Jr 1987 Biogeography and evolution of neotropical gator), supported by the Smithsonian Institution's International butterflies, p 66-104. In Biogeography and Quaternary history Environmental Sciences Program and National Museum of Natu- in tropical America. TC Whitmore, GT Prance eds, Oxford mono- ral History (NMNH) in cooperation and collaboration with col- graphs on biogeography, Clarendon Press, Oxford leagues and institutions throughout the neotropical lowlands. Fig- 74. Spangler PJ 1990 A revision of the neotropical aquatic beetle ures 1 and 2 were prepared by eorge L Venable, Senior Scientific genus Stegolmis (Coleoptera: Elmidae). Smithsonian Contrib Illustrator, NMNH. We thank the Smithsonian Institution for Zool 502: 1-52 long-term financial support of our basic research, which has made 75. Halffter G, ME Favila 1993 The Scarabaeinae (Insecta: Co- this sort of product possible. We also thank our many colleagues leoptera) an group for analysing, inventorying and moni- and host institutions in Latin America for their support.

Volume 51 (516) Septembermecember1999 CSncia e Cuttufa Journal of the BrazIIian Association for the Advancement of Science* 385