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A Protocol for Rapid and Representative Sampling of Vascular and Non Selbyana 24(1): 105-1 1 1. 2003. Institute of Plant Sciences, University of Gottingen, Untere Karspiile 2, 37073 Gottingen, Germany . The Evergreen State College, Olympia, WA 98505, USA Institute of Plant Sciences, University of Gottingen, Untere Karspiile 2, 37073 Gottingen, Germany. Botanical Institute, University of Greifswald, Grimmerstr. 88, 17487 Greifswald, Germany. NICOLENOSKE Botanical Garden and Botanical Museum, Free University of Berlin, Konigin-Luise-Str. 6-8, 14191 Berlin, Germany. ABSTRACT. A protocol for rapid and representative sampling of vascular and non-vascular epiphytes (ex- cluding epiphylls) is presented for one hectare of tropical rain forest, including montane forest. We estimate that the inventory and morphospecies recognition (excluding species identification) can be camed out in approximately 2 weeks by a team of six persons, three specialists (one each for vascular plants, bryophytes, and lichens) and three field assistants. Key words: Cloud forest, epiphytes, minimum sample size, non-vascular epiphytes, sampling, species diversity, tropical rain forest The value of epiphytes also is exemplified by their usefulness as ecological indicators of cli- The enormous diversity of epiphytes, both mate and forest types (Benzing 1990, Frahm & vascular plants (e.g., orchids, bromeliads, aroids, Gradstein 1990, Nadkarni & Solano 2002). Non- ferns) and non-vascular plants (mosses, liver- vascular epiphytes and "atmospheric" vascular worts, lichens), is one of the most striking char- epiphytes are indicators of microclimate and en- acteristics of tropical wet lowland and montane vironmental quality, as their growth forms and forests. This feature distinguishes these forests physiology make them sensitive to changes in from most temperate forests (Catling & Lefko- the environment (Benzing 1990, Bates & Farmer vitch 1989, Cornelissen & ter Steege 1989, Gen- 1992, Nash 1996, Shaw & Goffinet 2000). Non- try & Dodson 1987, Nadkarni et al. 2001, Nied- vascular plants lack the protective cuticle that er et al. 1999). Epiphytes play a key role in eco- vascular plants have, which allows the free en- system-level interactions in tropical wet forests, trance of solutions, gases, and minerals to the especially in the processes that affect the water living cells of the plants. balance and nutrient cycles of the forest (Coxson As they often live high up in the canopy, epi- & Nadkarni 1995). They are a major source of phytes frequently have been overlooked or un- food and habitat for birds, mammals, amphibi- ans, and reptiles, and offer shelter to a variety derstudied in rain forest studies, because of dif- of invertebrates and microorganisms (Remsen & ficulties of access. These limitations have been Parker 1984, Nadkarni & Matelson 1989). largely overcome by the development of tech- niques for access into the canopy (Mitchell 1982, Lowman & Nadkarni 1995, Mitchell et al. * Corresponding author. 2002). Although many vascular epiphytes may 106 SELBYANA Volume 24(1) 2003 be spotted and identified from some distance, 240 1 Est inventories based solely on observations from the ground will be incomplete and biased, as many small species growing in the canopy can- not be detected from the forest floor. Unless freshly logged trees are available, inventory of the canopy must be conducted with access from tree-climbing, cranes, or balloons. Documenting the diversity of epiphytes re- quires uniform, repeatable sampling methods. Haphazard collecting gives a rough impression number of plots of the species richness of a forest, but it does not provide robust data for comparing biodiver- FIGURE1. Species accumulation curves and esti- sity of different habitats. Historically several mated total number of species (Est) of vascular epi- methods have been used (McCune 1990, Shaw phytes in three 1 ha plots in a montane forest of Bo- & Bergstrom 1997, Nieder & Zotz 1998), but livia (after Kriimer 2003), using the MMMeans rich- ness estimator (Colwell & Coddington 1995). In each they have not been widely accepted by the can- hectare plot, up to eight trees were sampled, as was a opy research community. The need for standard- 20 X 20-m plot around each sampled tree. ized sampling of tropical epiphytes was dis- cussed at the Second International Workshop on Tropical Canopy Research of the European Sci- 200 1, Flores-Palacios & Garcia-Franco 200 1, ence Foundation held at Ulm in 1995. The pa- Rauer & Rudolph 2001). Recent studies indicate pers that came out of that meeting (Gradstein et that the MMS of vascular epiphytes is relatively al. 1996) were a first step toward developing a small. About 80% of the total estimated number uniform method for epiphyte sampling. of vascular epiphyte species in 1 ha of Bolivian In this paper, we present a standard protocol montane forests was tallied by sampling eight for vascular and non-vascular epiphyte sampling trees and a 20 X 20 m plot around each tree in tropical wet forests, including montane for- (Kromer 2003) (FIGURE1). About half of the ests. These methods were prepared in the frame- vascular epiphyte species of a 4000 km2 region work of the Global Canopy Programme (GCP), in Mexico was found in 0.5 ha of forest (Hietz following the recommendations of the GCP & Hietz-Seifert 1995a); and ca. 50% of the spe- workshop held in Gottingen, Germany, on 24- cies of the valley of Sehuencas, Bolivia, oc- 25 February 2002 (Secoy 2002). The protocol is curred in less than 0.1 ha (Ibisch 1996). Eng- designed for Rapid and Representative Analysis wald (1999) recorded ca. 50% of the species of of Epiphyte Diversity (RRED-analysis) within a 0.1 ha of montane forest in La Carbonera, Ve- I-ha plot of forest. It is largely based on the nezuela, in 0.01 ha. research experiences of the authors in tropical The MMS of bryophytes is significantly America (Bolivia, Colombia, Costa Rica, Ecua- smaller than that of vascular plants. Sampling of dor, French Guiana, Guyana, and Panama). 3-5 trees yielded 75-80% of total bryophyte di- RRED-analysis pertains to the inventory of versity of a tropical forest stand (Gradstein vascular and non-vascular epiphytes of 1 ha of 1992, 1996, Acebey et al. 2003). The MMS of homogeneous forest. It is carried out by a team lichens, however, is larger than that of bryo. of six persons, three specialists (one each for phytes (Sipman 1996, Komposch & Hafellne~ vascular plants, bryophytes, and lichens) and 2000) and may be similar to that of vascula three field assistants. The protocol for non-vas- epiphytes. cular epiphytes focuses on corticolous, bark-in- Based on the available information on spe. habiting epiphytes. For sampling of epiphyllous cies-area relationships, we propose to samplr species, see Liicking and Liicking (1996). eight mature canopy trees within a 1-ha plot oj forest for RRED-analysis for vascular epiphyte! and lichens, along with five trees for bryophytes We also recommend sampling the epiphyte di Sampling Design and Tree Selection versity on treelets and shrubs in a 20 X 20 n area around each selected tree (see below). Thl Species-accumulation curves, based on the completeness of the sampling may be checkec number of epiphyte species recorded against the by means of species-accumulation curves and, number of trees sampled, provide information species-richness estimator (Colwell & Codding on minimum sample size (MSS) (Gradstein ton 1995) (FIGURES1, 2). Herzog and his col 1992, Wolf 1993, Hietz & Wolf 1996, Shaw & leagues tested the accuracy of different richnes Bergstrom 1997, Annaselvam & Parthasarathy estimators, including ACE, ICE, Chaol, Chao, GRADSTEIN ET AL.: SAMPLING EPIPHYTE DIVERSITY ORCH PTER Est Est 0 0 + number of plots FIGURE2. Species accumulation curves and estimated total number of species (Est) of orchids (ORCH) and ferns (PTER) on eight trees (diamond), on shrubs and treelets in eight 20 X 20-m understory plots (square), and on the trees, shrubs, and treelets taken together (circle) in a montane forest of Bolivia (after Kromer 2003). MMMeans, and MMRuns, in a study of species Sampling of Trees richness of tropical bird communities and found that the most accurate estimation of total species Representative sampling of the epiphyte di- richness was obtained by using the MMMeans versity of tropical rain forests requires sampling of whole trees, from the base to the outer can- richness estimator (for details, see Colwell 1997, opy. Trees may be ascended using the single Herzog et al. 2002). rope technique (SRT) (Perry 1978). Ground- Trees in close vicinity of each other tend to based inventory (GBI), using binoculars and have a similar epiphyte flora resulting from the sampling of fallen branches, is inadequate to as- clumped distribution of many epiphyte species sess the diversity of the epiphyte communities (Hietz & Hietz-Seifert 1995b, Sipman 1996, (Gradstein 1992, Flores-Palacios & Garcia-Fran- Engwald 1999, Nieder et al. 2000). Thus trees co 2001). Using SRT, Kromer (2003) recorded standing well apart (separated by at least 25 m) more species of vascular epiphytes-including and with crowns not overlapping should be se- three times as many orchids-in one 20 X 20 m lected for species richness estimates. Trees at plot of mountain forest than did Sugden and forest margins should be avoided because of po- Robins (1979) in fourteen 10 X I0 m plots using tential microclimatic edge effects. To maximize GBI. In a Mexican oak forest, 20% more species the information on species richness, preferably were found using STR than by using GBI (Flo- the oldest or largest trees (with the largest res Palacios & Garcia-Franco 2001). Sampling trunks) should be selected. These trees are usu- of the forest canopy by SRT is particularly im- ally richest in epiphyte species because of their portant for assessment of orchid (FIGURE2) and large and highly diversified crowns; they also non-vascular epiphyte diversity. About 50% of have been available for establishment by epi- the bryophyte species of the rain forest may be phytes during the longest period of time (Hietz restricted to the canopy (Gradstein 1992, Grad- & Hietz-Seifert 1995a, Shaw & Bergstrom 1997, stein et al.
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