Species abundance, distribution and diversity in ...

TAXON 59 (2) • April 2010: 592–597

Haripersaud & al. • Plant diversity and collecting in the Guianas

B I O D I V ER SI T Y AN D CO NSERVAT I O N

Species abundance, distribution and diversity in time and space after centuries of botanical collecting in the Guianas Padmattie Haripersaud,1 Hans ter Steege,1 Jean-Jacques de Granville,2 Hervé Chevillotte3 & Michel Hoff 4 1 Plant Ecology and Biodiversity, University of Utrecht, Sorbonnelaan 14–16, 3584 CA Utrecht, The Netherlands 2 Herbier de Guyane, Institut de Recherche pour le Développement, Cayenne, France 3 UMR OSEB (Organisation, Systématique et Evolution de la Biodiversité), MNHN-IRD, Paris, France 4 Université Louis Pasteur, Strasbourg, France Author for correspondence: Padmattie Haripersaud, [email protected] Abstract For centuries, botanists have collected plant specimens across the Guianas (Guyana, Suriname, French Guiana). In this paper, we describe the construction of a comprehensive angiosperm specimen database for the Guianas and examine: (1) the historical accumulation of species and specimens; (2) the pattern of geographical expansion of collecting efforts; (3) the distribution of specimen records among families, genera, species, growth forms and countries. The cleaned database contained 168,487 specimen records belonging to 7146 species. The specimen records showed uneven distribution among families, genera, species, growth forms and countries. Although there was some species overlap between and among countries, unique species were collected in each country. Despite the high collecting efforts, many areas still remain under-collected. Keywords botanists; collecting effort; French Guiana; Guyana; species; specimens; Suriname

INTRODUCTION Botanical knowledge of the Guianas (Guyana, Suriname, French Guiana) has accumulated over more than four centuries (Ek, 1990, 1991; Hoff, unpub.). However, the specimens from botanical expeditions are scattered over herbaria worldwide and it is only during the past two decades that information contained on specimen labels is becoming increasingly available in digital form. To our knowledge this is the first attempt to compile the digital data from primary sources to develop a comprehensive database for the Guianas, although previous studies have used information from the individual countries (e.g., Poncy & al., 1998, 1999; Funk & al., 1999, 2002; ter Steege & al., 2000). Here we describe the historical variation in the accumulation of specimen and species data and the pattern of expansion of the geographical area in which the specimens were collected. We then analyse how the specimen records in the database are distributed among families, genera, species, growth forms and countries.

MATERIALS AND METHODS Building a digital herbarium. — During the initial phases of the study, all participating herbaria of the Flora of the Guianas consortium were asked to contribute their digital specimen data. The angiosperm database of the Nationaal Herbarium Nederland, Utrecht branch (about 115,000 specimens) forms the backbone of this study. This herbarium no longer exists as a separate entity (Erkens & Baas, 2008) but all of the Guianas specimen labels were digitized just before the herbarium ceased to exist. This database was augmented with specimen data from 592

the herbarium of French Guiana (about 79,000 specimens; www. cayenne.ird.fr/aublet2), the New York Botanical Garden, the Missouri Botanical Garden, the Jenman Herbarium, the Jonah Boyan Herbarium of Guyana, Lands Bosbeheer and Bosbeheer Suriname of Suriname, and the Smithsonian Institution, Washington, D.C. (Kelloff & Funk, 1998; Clarke & al., 2001; Hollowell & al., 2000, 2003, 2004). There were many duplicate records (specimens with the same taxonomic identity, collection date, collector and number) in the database since many of the herbaria have a history of exchanging duplicates. These duplicate records were removed from the database. When there were conflicts in species identifications between duplicate specimens from different herbaria, the identification by the leading specialist was maintained. The species names, as shown on each label, were updated based on the Checklist of the Plants of the Guiana Shield (Hollowell & al., 2001; Funk & al., 2007) and the W³tropicos website (www.tropicos.org). The Angiosperm Phylogeny Group II system was used for the classification of families and genera (www.mobot.org./MOBOT/research/APweb). Only records identified to species level were retained in the database, and infra-specific information was not used. Records of introduced species were removed from the database because most of these species grow in populated areas whereas the focus of our study was on natural ecosystems of the Guianas. We used the W3tropicos website and the Checklist of the Plants of the Guiana Shield to determine whether species were introduced or occurring naturally. Information on latitude and longitude was taken from the labels when available. Locality information, retrieved from labels or field notes, was converted to spatial coordinates using national gazetteers. Records that lacked information on date of collecting, specimen identity and/or locality were removed from the database.

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Data analysis. — The specimen records in the database were collected between 1804 and 2004. To determine the number of specimens made by individual collectors, we constructed a frequency histogram with log2 counts of specimens plotted against percentage of collectors in each class. To examine the historical accumulation of species and specimens, specimen records were ordered according to year of collecting and cumulative number of records was plotted as a function of collecting year. The geographical pattern of collecting efforts was determined by dividing the Guianas in 5 × 5 arc-minutes grid cells and mapping the distribution of records for different cumulative 50-year periods (1804–1853, 1804–1903, 1804–1953 and 1804–2004). To examine the relative abundance of species records for each country, the logarithm of the relative abundance of each species was plotted as a function of the rank order of abundance. To examine the historical accumulation of singletons (species represented by single specimen records) in the database, we ordered the singletons according to year of collecting and counted how many were collected per year. To correct for sampling artefacts, we examined whether more singletons were collected in some areas than others. For this purpose the Guianas were divided in 1 × 1 degree grid cells and the number of singletons and species records counted per grid cell. We fitted a logarithmic regression through number of singletons plotted against number of specimens and calculated the residual for each data point in the graph. A large residual was interpreted as a high singleton/specimen ratio. To examine how records were distributed among growth forms in each country, we compared the percentage of records for each growth form on a country basis. Species composition overlap among countries was determined by calculating the percentages of shared and unique species. To examine the relationship between the number of specimen and the number of species records per grid cell, we counted the number of specimens and species records per 0.5 × 0.5 degree grid cells. We then plotted the number of specimen records against the number of species records. To calculate the efficiency of collecting we divided the data into time periods and subsequently divided the number of new species found by the number of specimens collected for each time period.

RESULTS AND DISCUSSION After removing records of duplicates and introduced species, the database contained a total of 190,398 specimen records. Of these, 168,487 contained information on specimen identity, collection date and locality and were used for analysis. Although this database does not contain records of all specimens collected in the Guianas, we feel it covers more than 85% of all angiosperm specimens collected in the area. As mentioned above, many of the herbaria focusing on the region have a history of exchanging duplicates. We therefore assume that, even though some herbaria are not fully digitized, we have effectively digitized most of the specimens collected in the area. The information content of the labels of very old


specimens (e.g., Aublet, Schomburgk) is often inadequate and could therefore not be used in our study. Moreover, identifications of these old specimens may be unreliable when not checked by specialists. Finally, most herbaria have a backlog of specimens and it takes a long time before specimen information becomes electronically available. Therefore, information on collections made after 2004 was incomplete and not taken into consideration. We believe, however, that additional specimens from the study period (1804–2004) or newer specimens will not essentially alter the results of this study. The specimens were made by 560 collectors (Fig. S1 in the Electronic Supplement to this article). Some collectors spent most of their careers collecting in the region and 40 (about 7%) gathered more than 1000 specimens. However, the majority collected fewer specimens and 232 (about 42%) made 10 or less specimens. Historical development of the specimen data. — The oldest known specimen of the Guianas was collected by A. Chastelein in Suriname in 1661 (Ek, 1991), and the oldest known botanical explorations in Guyana and French Guiana date back to the eighteenth century (Ek, 1990; Hoff, unpub.). However, there is not much locality information for specimens collected during the seventeenth and eighteenth centuries. The number of specimen records in the database (1804– 2004) increased gradually between 1804 and 1953 and then very rapidly until 2004 (Fig. 1). The geographical area in which the specimens were collected expanded from 1804 to 2004 and some areas, especially those closer to cities and research institutions, were repeatedly collected. Between 1804 and 1853 1107 (15%) species were collected, despite the low number of the specimens (1728 or 1%). There were two main peaks in species accumulation during this time period. The first peak occurred in 1837 due to the collecting efforts by F.L. Splitberger in Suriname, mainly in the vicinity of Paramaribo and the plantations. The second peak was due to the collecting efforts of R.H. Schomburgk in the following year, during his survey of the boundaries of British Guiana (now Guyana) (Ek, 1990). The low number of records from before 1854 is due not only to low collecting effort but also because information contained on many older specimen labels was illegible, inadequate, or unavailable digitally. The largest number of specimens were made in Suriname and least in French Guiana. The database contains only 18 specimens collected in French Guiana before 1854. The main reason is that we did not have access to the specimens of the National Herbarium of Paris (P), where most of these historical specimens are stored, because digital data were not available. But, also, botanical research in French Guiana at that time mainly focused on useful plants for food and medicine, and forestry botany was not a priority (Hoff, unpub.). Cartographers, appointed in the period between 1767 and 1876 to demarcate the boundaries of French Guiana, did some botanical collecting (mostly lower plants) as a side activity. For the period up to 1903, the database contained 7979 (5%) specimens and 2503 (35%) species records (Fig. 1); the geographical area covered by collectors has increased (Fig. 2). Most of the specimen records between 1854 and 1903 are from 593


Guyana and the least from French Guiana. The main peaks in species accumulation during this period (especially 1879 to 1887) are due to the collecting efforts of G.S. Jenman in various geographical areas in Guyana. Another peak occurred in 1903 due to the collecting effort of G.M. Versteeg along the Gonini River in Suriname. French Guiana continued to be poorly collected. The most important contributors to the botanical knowledge of French Guiana were P.A. Sagot and E.M. Mélinon but their activities were restricted to the coast as the interior was considered unsafe for travel and collecting following the discovery of gold (Hoff, unpub.). For the period up to 1953, the database contained 39,666 (24%) specimens and 4658 (65%) species records. There were four main peaks in species accumulation during this time period. The first peak is due to the collecting efforts of botanists collecting under the ‘Boschwezen’ number series, mainly in the Zanderij, Sectie O, Brownsberg areas and along the Nickerie Guyana Species

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Fig. . The historical accumulation of number of angiosperm specimens and species collected in Guyana, Suriname and French Guiana. Species and specimens ordered according to year of collecting and cumulative number of specimens or species plotted as a function of the year of collecting.

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River in Suriname. The second peak occurred in 1937 due to the collecting effort of N.Y. Sandwith around the Mazaruni Station and of A.C. Smith collecting around the Kuyuwini landing and in the Rupununi area of Guyana. In the same year, H.E. Rombouts collected specimens along the Marowyne, Lawa and Litani rivers, causing a large increase of the number of new species in Suriname. A third peak occurred in 1938 due to the collecting effort of A.C. Smith in the Rupununi area and the Kanuku and Iramaikpang Mountains areas and in the same year due to the effort of botanists collecting under the ‘Forest Department’ number series around the Moraballi Creek area and around Mazaruni Station in Guyana. The last peak in this period occurred in 1944 due to the collecting effort of B. Maguire in several geographical areas of Suriname and the Forest Department along many tributaries of the Essequibo River in Guyana. In the period 1954 to 2004 collecting strategies changed from enriching species lists of individual collectors to enlarging the species lists of target geographical areas. A large number of specimens in the database are from this period. There were three major peaks in species accumulation: a first peak in 1963 due to the collecting efforts of B. Maguire and others in the Wilhelmina Mountains of Suriname; a second peak in 1987 due to the efforts of J.J. Pipoly particularly in the Ayanganna Mountains and M.J. Jansen-Jacobs in the Rupununi area of Guyana; an a third peak in 1989 due to collecting efforts of J.W. Hahn in the Paramakatoi area, L.J. Gillespie in the Kaieteur and Kanuku Mountains area, M.J. Jansen-Jacobs in the Gunn’s Strip area in Guyana, and J.-J. de Granville in the Monts Atachi Bacca area in French Guiana. During this period large scale forestry inventories were carried out in all three countries and permanent research centres were set up. Of 2485 new species that were added to the database during this time period, 1060 were first collected in French Guiana, 960 in Guyana and 501 in Suriname. A rich flora with over  species of flowering plants. — The specimens in the database are distributed unevenly among 183 families, 1525 genera and 7146 species (Table S1 in the Electronic Supplement). The best represented families are Fabaceae, Rubiaceae, Melastomataceae, Poaceae and Cyperaceae. The ten most specimen-rich families account for 71,101 (about 42%) specimens and 3045 (43%) species; twelve families are represented by just one or two specimens. French Guiana had the largest number of species represented in high abundances (Fig. S2 in the Electronic Supplement): 65 species were collected in French Guiana with more than 100 specimens per species vs. only seven and five species in Guyana and Suriname, respectively. More species were represented by one specimen in Guyana (1295 or 24% of all species) than in Suriname (801 or 20%) and French Guiana (655 or 15%). The singletons in the database were collected throughout the collecting period and from all over the Guianas (Fig. 3). The oldest singleton in our database was collected in 1827 and most were from after the 1980s (Fig. S3 in the Electronic Supplement). The number of singletons in the database is likely to be related to low collecting efforts or under-collecting and not necessarily to species rarity. After correcting for sampling

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Specimens

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Fig. . Number of specimens and species collected in the Guianas over 50-year periods (1804–1853, 1804–1903, 1804–1953, 1804–2004). Area divided in 5 × 5 arc-minutes resolution and number of species and specimens counted per grid cell.

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intensity, we found that nine 1-degree grid cells showed an unusually high number of singletons compared to the number of specimens collected (Fig. 3): Saül (French Guiana), five sites in Pakaraima (Guyana) and three sites in the Rupununi Savannah area (Guyana). We suggest that the high number of singletons in Guyana is probably due to the greater impact of the Guayanan Flora in Guyana than in the other two countries.

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Most specimens are trees. — The specimen records were not equally distributed among climbers, epiphytes, herbs, palms, shrubs and trees (Fig. 4). More trees were represented in the database than other growth forms. Palms are the least represented and this is probably due to the physical difficulties associated with collecting these plants. Also, when compared to other growth forms, palms are represented by relatively fewer species in the Guianas (Funk & al., 2007). There were no substantial differences in the distribution of growth form specimens between countries. Variation in species composition among the Guianas. — The number of species collected was highest in Guyana and lowest in Suriname (Figs. 1 and 5). Although some species were common to all three countries, many species were unique to one country (Fig. 5). A total of 2520 (or 35%) of the species were collected in all three countries. Guyana and Suriname show the highest similarity in collected species and French Guiana and Guyana the least. About 25% of the species in the database were unique to Guyana while a lower number of unique species (6% and 11%, respectively) were collected in Suriname and French Guiana (Fig. 5). Unique species are not necessarily represented by few specimens in the database as the number of specimens the unique species ranges between 1 and 72 (average 4). Geographical distribution of specimens. — To maximize the chances of detecting new species for the Guianas, botanical expeditions tend to focus on new or under-collected areas in the Guianas. As a result, the geographical area in which the specimens were collected gradually expanded from 1804 to 2004 (Fig. 2). Also some areas, especially those that are close to cities or research stations, were revisited. As a result, the number of specimens collected per 5 arc-minutes grid cell (about 10 × 10 km) ranged between 0 and 7131 by the end of 2004, and the number of species between 0 and 1693. Species number was strongly determined by the number of specimens collected (Fig. S4 in the Electronic Supplement). In all, only 1504 out of 5345 grid cells (or 28.1%) have been sampled, showing the incompleteness of our knowledge of the geographical distribution of species within the Guianas. Addition rate of new species is slowing. — The addition of new species to the historical curve was initially very rapid when new species were constantly being discovered (Fig. 1). However, towards the end of the 20th century the rate of addition of new species slowed down considerably. This is probably because most of the species occurring in areas in the Guianas visited by botanists had already been collected. By 1995 the rate of addition of new species for the Guianas was reduced to 1.4 for every 100 specimens collected (Fig. S5 in the Electronic Supplement). Since most of the Guianas still remains undercollected, targeting areas with different habitats from those already sampled might increase the rate of addition of new species. Moreover, collecting at different times of the year might also yield new species. Most botanical expeditions were carried out during the dry season when many species are known to be flowering or fruiting. Collecting during other periods might yield species with a different phenology pattern. Many species, however, are rare in nature (Hubbell, 2001) or inconspicuous, and we have to accept that many of these may never be found.

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ACKNOWLEDGEMENTS We thank all of the herbaria and botanists who contributed to the database. Secondly, we thank the Netherlands Organisation for Scientific Research (NWO) for funding the Ph.D. project of P. Haripersaud and the digitization the herbarium specimens of the Guianas. Special thanks are due to Marinus Werger and Heinjo During for their useful comments on the manuscript.

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Funk, V.A., Zermoglio, M.F & Nasir, N. 1999. Testing the use of specimen collection data and GIS in biodiversity exploration and conservation decision making in Guyana. Biodiv. Cons. 8: 727–751. Hollowell, T., Berry, P., Funk, V.A. & Kelloff, C.L. 2001. Preliminary checklist of the plants of the Guiana Shield (Venezuela: Amazonas, Bolívar, Delta Amacuro; Guyana; Surinam; French Guiana). Washington, D.C.: Smithsonian Institution. Hollowell, T., Funk, V.A., Kelloff, C.L. & Gharbarran, G. 2000. Smithsonian plant collections, Guyana: 1986–1987, John J. Pipoly III. Biological Biodiversity of the Guianas Program, no. 43. Washington, D.C.: Smithsonian Institution. Hollowell, T., Gillespie, L.J., Funk, V.A. & Kelloff, C.L. 2003. Smithsonian plant collections, Guyana: 1989–1991, Lynn J. Gillespie. Contr. U.S. Natl. Herb. 44: 1–104. Hollowell, T., McDowell, T., Funk, V.A. Kelloff, C.L. & Gopaul, D. 2004. Smithsonian plant collections, Guyana: 1990–1991, Tim McDowell. Contr. U.S. Natl. Herb. 50: 1–150. Hubbell, S.P. 2001. The Unified Neutral Theory of Biodiversity and Biogeography. Princeton: Princeton Univ. Press. Kelloff, C.L. &. Funk, V.A. 1998. Preliminary checklist of the plants of Kaieteur National Park, Guyana. Biological Diversity of the Guianas Program, no. 28. Washington, D.C.: Smithsonian Institution. Poncy, O., Hoff, M. & Bordenave, B. 1999. Y-a-t-il des plantes menacées en Guyane française? Bull. Soc. Bot. Centre-Ouest 19: 145–170. Poncy, O., Hoff, M. & Brulard, J.F. 1998. La connaissance actuelle de la flore de Guyane peut-elle étayer les projets de conservation? JATBA Rev. d’Ethnobiol. 40: 373–398, ter Steege, H., Jansen-Jacobs, M. & Datadin, V. 2000. Can botanical collections assist in a National Protected Area Strategy in Guyana? Biodiv. Cons. 9: 215–240.

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