The Ecology of Tropical Rain Forest Having solved many of the prob- lems of access, canopy biologists Canopies are now designing new sampling techniques and formulating hy- Margaret D. Lowman and Mark Moffett potheses. 'They face the difficulty of working in a large three-dimensional space. How are organisms detected With the advent 01 increasingly sophisti- Biological information about can- and sampled in such a hetero- cated techniques /or access, tropical lorest opies changed very little from geneous environment, where humans canopy research has burgeoned in the last Wallace's day until - exactly one are rendered less agile? In a lew years. Although an enormous amount hundred years later in 1978 - Don scenario similar to the expansion of of basic descriptive work remains to be Perry published a method of climb- coral reef fish ecology in the 1970s done, canopy research is now entering a ing into tropical tree canopies with the advent of SCUBA, canopy more advanced and ecological phase. using ropes and technical climbing biologists are developing sampling apparatus2. Although Perry was by protocols to account for the spatial, no- means the first researcher to temporal and substrate heterogen- Until recently, most of our knowl- climb into canopies, the use of single- eity of their en~ironment~,~. edge about forest ecosystems has rope technologies heralded a rapid The development of canopy been based on observations from expansion of canopy research in- research has been affected by sev- ground level. These ground-based volving a range of apparatus includ- eral spatial and temporal con- perceptions are summarized in a ing towers, walkways, platforms, straints of this habitat, including: comment by Alfred R. Wallace' cranes and dirigi bleP5. Having (I j differential use of this geometric Overhead, at a height, perhaps, overcome many of the logistic limi- space by canopy organisms; (2) het- of a hundred feet, is an almost tations of access into tall trees, we erogeneity of substrate; (3) varia- unbroken canopy of foliage can now do field work and bility in ages within the canopy formed by the meeting together of formulate hypotheses in an above- (e.g. soillplant communities accru- these great trees and their inter- ground heterogeneous three- ing in uneven layers on branches, lacing branches; and this canopy dimensiona! system. leaf cohorts between sun and is usually so dense that but an Historically, most ideas about shade regions), (4) variability in indistinct glimmer of the sky is to forest ecology were developed in microclimate of the atmosphere- be seen, and even the intense temperate regions. By contrast, canopy interface; (5) the high diver- tropical sunlight only penetrates most work on forest canopies has sity of organisms (many unnamed); to the ground subdued and bro- been pioneered in the tropics. The (6) development of protocols to ken up into scattered fragments . . . reasons for such sudden interest in quantify processes in the canopy it is a world in which man seems tropical canopy research are two- environment. Many aspects of an intruder, and where he feels fold. First, tropical tree canopies canopy research are so new that overwhelmed.. . are the most complex of any forest results are not yet published. type. Second, the threatened extinc- In this review, we highlight sev- Margaret Lowman is at the Selby Botanical Gardens, tion of tropical organisms (many of eral areas of research that have been Sarasota, FL 14216, USA; Mark Moffett is at the which live in the canopy) has pro- enhanced by canopy access. We Museum of Comparative Zoology, Harvard Uni- vided incentive to study them be- define three major types of canopy versity, Cambridge, MA 02118, USA. fore they disappear6 (but see Ref. 7). research, each of which requires

0 1993, Elsevier Science Publishers Ltd (UK) 0169-5347/931$06.00 TREE vol. 8, no. 3, March 7993

different logistics and experimental Branching patterns, in turn, are diversity of gliding animals in Asia design: studies of plants, studies of indirectly affected by the location has been attributed to the relative animals and studies of canopy of a tree. Berner, who is studying scarcity of lianas in this region, processes (e.g. photosynthesis, the interactions between branch which many animals use as 'high- herbivory and nutrient cycling). growth patterns, disturbance and ways' to cross from one crown to the plant community dynamicsi7,found nextz2. As crowns become more Sessile organisms: trees, vines, that trees on slopes produce more widely dispersed (particularly in epiphytes and epiphylls asymmetrical branch growth pat- windy regions), lianas themselves Studies of sessile organisms in terns as com~aredto trees on level have more difficulty extending lat- forest canopies pose fewer logistic ground, due to increased light influx erally from tree to tree2'. Vines may difficulties than other aspects of into tree crowns on hillsides. But comprise one quarter of all leaves canopy biology. The biggest ob- the steeD slo~esalso result in in the forest of Barro Colorado stacle is access to growing shoots more disiurbance and higher mor- Island, and one individual of and reproductive parts, many of tality for trees growing there. Entada monostachya has been which occur in the uppermost can- Similar differential tree growth and recorded to connect the crowns of opy. Some methods (e.g. raft5 and mortality occur around the margin 64 canopy trees2'. Indeed, to crane8) facilitate access to these of a tree gap, apparently prolong- describe vines as sessile is some- upper regions. Shade-tolerant ing the successional processI8. times inappropriate, because of plants such as bromeliads and The first comparisons between their fast growth, mobility and for- other epiphytes are often access- ground-level observations and di- aging behavior as they search for ible in the mid-canopy region. rect measurements of canopy lightZ4. Techniques other than Epiphytes and epiphylls colonize architecture are under way in climbing have been employed to branches and leaves, respectively, Panama8.The 'surface' of tropical for- study vines, such as the use of in moist canopy regions. Never- ests appears much more irregular winches in Australia to haul Calamus theless, their diversity, distribution and dynamic than most measure- down from the canopy and measure and abundance is not well docu- ments from the ground would indi- its growth25.We are only beginning mented', and data on growth, cate, and is more heterogeneous to understand the complex dy- recruitment and survival are few than in temperate forests, partly namics of tree and vine growth in (but see Refs 10, l l ). because of the larger number of relation to canopy processes. Trees are the major substrate of tree species. This has implications the canopy ecosystem, and tree for canopy-atmosphere interactions, Mobile organisms in canopies species - their architecture, limb and for population dynamics of Most studies of vertebrates have strength, surface chemistry and tex- organisms in the upper canopy. For been made from ground level - an ture - play fundamental roles in instance, precipitation reaching the adequate vantage point for diurnal shaping the canopy community. understory layers can vary several- mammals and some birds. But Tree architecture is far more varied fold depending on the angle of access into the canopy has led to the in the tropics than in the temper- incidence of rainfall1'. Canopy discovery of unexpectedly arboreal ate zones, and the patterns of topography affected the flux of proclivities in some rodents, whose reiteration of canopy branches and wind-blown insects in Puerto Rican behavior was not obvious from the their implications for canopy rain forest canopies, contributing ground. Malcolm used the peconha processes are not well understood to the regulation of Anolis lizard Indian method (strap between the in either regi~n'~,'~.Over time, as populations (R. Dial, PhD Thesis, feet) to look at edge effects on small canopy branches grow, the com- Stanford University, 1992). Other mammals in the canopy of lowland munities within them increase in environmental (e.g. light, sunflecks, forest near Manaus, Brazil2" He complexity. For example, patches of wind-below-crown level) and bio- found that species exhibit distinct leaves, heterogeneous in their age logical factors (e.g. density of vines, height preferences, and more mam- structure, foliage quality and distri- distribution of flowers, populations mals were arboreal than terrestrial. butionI4, attract different popu- of canopy leaves and subsequent In a Costa Rican cloud forest, lations of insects both within and organisms that inhabit them) are Langtimm also found stratified between tree crowns: herbivores affected by tree growth and canopy height preferences for different prefer shade leaves over sun architecture. species of small mammals2'. leave^'^,'^; and patches of canopy Crown shyness gaps between Ornithologists face the challenge vegetation (e.g. palms versus trees arise from dieback of the of trying to capture (as well as to vines) may host entirely different outermost branches due to wind- observe) birds in tree crowns. In populations of insectsI6. Similarly, shearingZ0 or shading of adjacent New Guinea, Bechler hoisted nets branching patterns affect the com- crowns2'. The amount of spacing up and down tall poles to quantify munities that form around them. between tree crowns may have birds of paradise in the canopy Branches that are steeply inclined profound effects on the dispersal (B. McP. Bechler, PhD thesis, Prince- have less accumulation of canopy of canopy organisms, providing ton University, 1983). More recently plants (and consequently canopy pathways for flying organisms both in Peru, Munn used a large sling- soils and insects) than branches between tree crowns and between shot to position aerial mist nets in that grow horizontally (S.W. Ingrarn, canopy layers, but inhibiting the emergent trees as high as MA Thesis, University of California horizontal passage of climbing ani- 40-60 m28.Bierregaard and Lovejoy at Santa Barbara, 1989). mals and plants. The unusual found that birds will increase the TREE vol. 8, no. 3, March 7993

size of their territories vertically to temporal variability, as well as epiphytes47,and consider epiphytes compensate for forest fragmen- artefacts of sampling, make studies a vital component of canopy com- tati~n~~.Using single-rope tech- of canopy arthropods difficult, and munities. Many epiphytes are rare niques, Nadkarni and Matelson the volume of data collected re- or endangered, and with the documented 193 species of birds quires many years to analyse. destruction of their tropical forest using epiphytes in tree crown^'^. environment, research on them (as Reptiles and amphibians in tree Processes in forest canopies well as other canopy organisms) is canopies have been studied in In forest trees, reproductive urgently needed. Epiphytes were Puerto Rico. Reagan" developed biology is predominantly a canopy recently the subject of an inter- sampling techniques to monitor phenomenon. The surprising im- national sympo~iurn~~,but their Anolis lizard populations in tree portance of thrips in the pollination population biology and life canopies. Dial (PhD Thesis, of dipterocarps was discovered histories are still poorly known. Stanford University, 1992) per- using a boom for canopy acced9 Other processes, such as photo- formed some of the first exper- (Fig. I). The staggered pattern of synthesis, have been reviewed for imental studies on populations of dipterocarp flowering and fruiting vinesZ0 but less extensively for lizards in tree canopies; he ex- requires insect pollinators that other canopy foliage (but see Ref. cluded lizards from tree crowns and can rapidly increase in numbers 8) The interaction of most canopy found a marked increase in abun- to accommodate the intermittent processes - in particular, large- dance of insects, their food source. flowering periods40. Comparisons of scale canopy dynamics - is not Studies of invertebrates in tropi- levels of allozyme diversity be- yet understood. Much of the cal forest canopies have perhaps tween high- and low density popu- groundwork, however, has been created more controversy than any lations of tree species show that completed to facilitate the extra- other aspect of canopy research. low-density populations have less polation of small-scale studies to Early studies by Erwid2 in tropical allozyme genetic diversity, yet main- larger-scale community population forest canopies raised the estimates tain higher levels than would be dynamics (e.g. from leaf to canopy, of the total number of species on found in most temperate plants4'. from organisms to populations, Earth from one million to 30 million Perhaps this can be attributed from flower to entire crown), and within a decade; however, this to long-distance pollinators for from short-term observations to high figure has recently been many tropical canopy trees, and long-term phenomena (e.g. from questioned3'. Fogging experiments further canopy investigations are seedling mortality to recruitment by Erwin in Brazil produced 1080 required. Fruit-dispersal syndromes patterns in tree crowns, from beetle species in four lowland rain- involving vertebrates have been measurements of light levels to forest canopies, and 83% of the studied in forest canopy in gap dynamics and photosynthesis, species were restricted to only one Borneo42,although most work was from litterfall patterns to nutrient forest type34.Sampling small flying conducted with binocular^^^, and - cycling processes). organisms with statistical repro- like pollination studies - require ducibility is difficult, and Erwin's many hours of observation. Prospects methods have taken many years to Measurements of herbivory and Canopy research has emerged as developJ5. the heterogeneity of both foliage a new dimension to our study of Since the first canopy fogging quality and herbivore distribution ecosystems. In the tropical rain in Brazil, forests in several other have been enhanced by canopy forests, where canopies are more regions have been similarly as- access. In earlier studies, where complex than any other forest type, sessed for insect diversity, including defoliation was sampled only by modern techniques of access have Borneo36, Vene~uela'~and Aus- harvesting lower-canopy leaves, made it possible to address hy- tralia38. The enormous spatial and both the extent and the patchiness potheses concerning biodiversity of herbivory was ~nderestimated~~.and community ecology in the Herbivores consume significantly canopy. less foliage in the upper crowns The next decade will be critical, (sun leaves) as compared to the as attempts to document the bio- lower crowns (shade leaves), but diversity and ecology of rain forest young leaves (especially in the canopies accelerate before habitat shade) are often completely con- fragmentation and deforestation ~umed~~.Differences in recorded take their toll. We advocate paral- herbivory levels can arise from lel studies of temperate versus artefacts of sampling46, although tropical canopies, and aquatic canopy access has increased the (e.g. coral reefs) versus terrestrial accuracy of results44. ecosystems, all of which will illumi- Access to tree crowns has stimu- nate the mechanisms for differ- lated interest in canopy nutrient ences in species diversity and Fig. I.Malaysian scientist S Appanah in a canopy boom cycling, particularly with reference community structure. at Pasoh Forest, Malaysia. The boom can be moved to epiphytes9. Nadkarni and Matel- readily and here is used to reach fruits of a dipterocarp son have documented the im- tree. This method has wonderful potential but is seldom References mentioned in the literature. Photo supplied by Mark portance of wind-blown fine I Wallace, A.R. (1 8781 Tropical Nature, Moffett. litter in providing nutrients for Macrnillan TREE vol. 8, no. 3, March 1993

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