Plant science in forest canopies – the first 30 years of advances and challenges (1980–2010)
Summary
As an emerging subdiscipline of forest biology, canopy science has undergone a transition from observational, ‘oh-wow’ exploration to a more hypothesis-driven, experimental arena for rigorous field biology. Although efforts to explore forest canopies have occurred for a century, the new tools to access the treetops during the past 30 yr facilitated not only widespread exploration but also new discoveries about the complexity and global effects of this so-called ‘eighth continent of the planet’. The forest canopy is the engine that fixes solar energy in carbohydrates to power interactions among forest components that, in turn, affect regional and global climate, biogeochemical cycling and ecosystem services. Climate change, biodiversity conservation, fresh water conservation, ecosystem productivity, and carbon sequestration represent important components of forest research that benefit from access to the canopy for rigorous study. Although some canopy variables can be observed or measured from the ground, vertical and horizontal variation in environmental conditions and processes within the canopy that determine canopy–atmosphere and canopy–forest floor interactions are best measured within the canopy. Canopy science has matured into a cutting-edge subset of forest research, and the treetops also serve as social and economic drivers for sustainable communities, fostering science education and ecotourism. This interdisciplinary context of forest canopy science has inspired innovative new approaches to environmental stewardship, involving diverse stakeholders.
I. Introduction
In Papua New Guinea, a tribe called the Korowai still lives in the treetops, erecting amazing aerial houses accessible by twig ladders. It is speculated that their unusual habit of community tree houses evolved as a mechanism to escape enemies on the forest floor, and provide a healthy environment above the dank, dark understory. Throughout human history, trees represented safe havens from danger, sites of spiritual connection, and an important source of food, medicines, materials, and productivity (reviewed in Lowman & Rinker, 2004). Although soil and streams provide important childhood ‘playgrounds’, tree houses remain a foremost recreational vestige of children and adults alike that inspires links between humans and the natural world (Lowman, 2009a; Louv, 2011). Many famous people have played in childhood tree houses – John Lennon (of the Beatles), Winston Churchill, the Roman Emperor Caligula, and Queen Victoria when she was a young princess. Recent medical findings indicate that children who play outdoors and learn about nature have better health and well-being (Louv, 2011).
In an evolutionary sense, humans descended from ancestors in the treetops. Recent findings about ancient hominoids in Ethiopia indicate that our ancestors inhabited forests (not savannahs as previously thought) (White et al., 2009). Why do the treetops continue to hold such spiritual as well as scientific importance for cultures around the world? And why have scientists only recently explored these heights for scientific discovery, given the fact that forestry is a relatively well-established discipline? Only in the past three decades have methods been developed that foster safe, versatile access to the treetops. And even more recently, with the advent of ecosystem services provided by forests gaining traction on the accounting ledgers of policy-makers, forest canopy research has gained attention as forest health links directly to human health (Perrings et al., 2010). Ecosystem services include fresh water yield, genetic libraries, carbon storage, energy production, medicines, food, shade, building materials, soil conservation, and spiritual/cultural heritage. Access to forest canopies has emerged as an important component of whole-forest research, especially with regard to climate change, biodiversity, and ecosystem service analyses (reviewed in Ozanne et al., 2003).
Forest ecosystems are composed of two fundamental subsystems: the forest floor/rhizosphere and the canopy. The canopy is composed of the foliated portion of the forest that represents the photosynthetic engine that captures solar energy and pulls water upward from the soil for exchange with the atmosphere, processes fundamental to sustainability of forest ecosystems and the services they provide. Because the forest floor is relatively easy to access, forest floor communities and processes related to decomposition, water infiltration, aggregate formation and nutrient turnover to roots or export have been studied in forests around the globe for at least two centuries (Coleman et al., 2004). By contrast, the canopy remained a virtual frontier as a result of limited access until relatively recently (Denison et al., 1972; Mitchell, 1982; Perry, 1986). Before the 1970s, canopy research was largely restricted to observations from the ground, from short trees or harvested sites, or from a point in the canopy that could be accessed with ladders (e.g. Beebe, 1949). With the advent of single-rope climbing techniques in the 1970s, followed by towers, balloons and cranes, canopy research in the past 30 yr has advanced by leaps and bounds in understanding of the diversity of canopy organisms and habitats and their effects on primary productivity as this affects local and regional climate and exchange of materials with the forest floor (e.g. Lerdau & Throop, 1999; Novotnýet al., 2003; Koch et al., 2004; Lowman & Rinker, 2004).
With their billions of green leaves, the treetops are epicenters of life and the basis of food chains around the planet. Forest canopies reputedly house c. 50% of the biodiversity of terrestrial ecosystems (reviewed in Wilson, 1992; May, 2010; Lowman et al., 2012). The combination of sun, fruits, flowers and year-round productivity in tropical rain forests provides ideal conditions for an enormous array of canopy inhabitants. Thousands of species of trees and vines produce a veritable salad bar for millions of insects that in turn are eaten by myriad reptiles, birds, and mammals (Lowman, 1999). Individual bromeliad tanks can house hundreds of residents, many unclassified for science (Lowman et al., 2006). This diversity of organisms is not without influence on the processes of primary productivity, evapotranspiration and exchange of materials among canopy, atmosphere and forest floor. For example, the forest canopy is the interface between 90% of Earth’s terrestrial biomass and the atmosphere (Ozanne et al., 2003) and regulates regional and global gradients in temperature, precipitation and airflow (Raupach et al., 1996; Finnigan, 2000; Foley et al., 2003; Juang et al., 2007; Janssen et al., 2008). Anthropogenic activities, as well as natural environmental changes, can alter both diversity and processes in forest canopies that affect regional and global climate, as well as critical ecosystem services. Increasingly, forest canopy scientists – along with coral reef ecologists, soil biologists, ice physicists, water chemists and others – have taken on the role of planetary physicians, working against a nearly impossible timeline to unravel the critical mysteries of how ecosystems function. With access into forest canopies, scientists have demystified some of their complex machinery, but many unanswered questions remain. Advances in forest canopy research during the past 30 yr and future questions comprise the topics of this review.
II. History of canopy access
Early foresters and naturalists based their ideas about forests on observations made at ground level (reviewed in Lowman, 2009a,b). Explorers such as Alfred R. Wallace and Charles Darwin wrote enthusiastically about the unbroken canopy overhead during the late 1800s, and ideas about forest canopies changed very little until almost 100 yr later when a steel tower was installed in Mpanga Forest Reserve, Uganda to monitor insect vectors of human diseases (Haddow et al., 1961). Several years later, Oxford University’s Operation Drake installed a canopy structure in the Asian tropics (Mitchell, 1982); ladders were used to study the chromosomal cytology of Himalayan trees (Mehra & Bawa, 1968); a canopy structure in Malaysia was tethered to tree crowns for phenological observations (Muul & Liat, 1970); and a few rigs were installed in Sulawasi forest canopies (Sutton, 2001). All of these early forays into the forest canopy were primarily for purposes of observation and exploration, without long-term viability.
The 1980s was hailed the ‘golden age of canopy access’ with the development of single rope techniques (SRTs) in the early 1970s (Denison et al., 1972), independently adapted from caving to treetops by Lowman (1984) in Australia and by Perry (1986) in Costa Rica (Fig. 1). Whereas SCUBA equipment in the 1950s heralded the age of exploration for coral reefs (reviewed in Sale, 2002), the versatile toolkit of ropes, harness, and climbing hardware enabled scientists to reach the mid-canopy with ease, safely suspended from a rope, to study the diversity of canopy organisms and their roles in the canopy (reviewed in Lowman & Rinker, 2004). SRT is ineffective, however, for reaching the uppermost canopy and the leafy perimeters of tree crowns, as ropes require looping over sturdy branches located close to the tree trunk. To overcome those shortcomings, new tools were designed to reach the perimeters and uppermost canopy. Ladders (Appanah & Chan, 1981), scaffolds (Mehra & Bawa, 1968), walkways (Lowman & Bouricius, 1995), canopy booms (P. Ashton, pers. comm.), hot air balloons (Hallé & Pascal, 1992), and construction cranes (Parker, 1995) all provided access to slightly different regions of the treetops, and hence enabled researchers to answer different questions.
Single rope techniques (SRTs) represented one of the first, and most affordable, canopy access techniques, as illustrated here by Indian graduate students training to study pollinators.
From their aerial perches, canopy scientists not only documented extraordinary biodiversity but also sounded the alarm about the consequences of deforestation and degradation for these veritable hotspots of life (e.g. Lowman & Selman, 1983). As a consequence, canopy access methods became important for education and ecotourism, as well as research. Canopy walkways for both research and ecotourism now span the globe, from Costa Rica to China (Fig. 2). The first two canopy walkways were constructed nearly simultaneously in 1985: one in Malaysia by Ilaar Muul anchored in tree crowns, and another in Queensland, Australia supported by telephone poles (see Lowman, 1999). The Australian model was an outcome of Lowman’s Earthwatch expeditions, which provided both safe access for her volunteers to collect herbivory data and a revenue stream for ecotourism. Five years later, North America’s first canopy walkway was constructed in the Hopkins Forest at Williams College, Massachusetts (Lowman & Bouricius, 1995; Lowman, 1999); and America’s first public canopy walkway was erected in Myakka River State Park, Florida in 2000 (Lowman et al., 2006; Lowman, 2009b). In addition to the popularity of canopy walkways around the world (http://www.canopyaccess.com), zip lines provide a thrill-ride through the canopy, further reinforcing the notion that forests – if conserved rather than cleared – provide local livelihoods (Lowman, 2009b).
Canopy walkways provided access to a team of scientists, students, or ecotourists, illustrated here in the Yunnan Province, China.
The French-designed hot-air balloon and inflatable raft, called ‘Radeau des Cimes,’ was designed to reach the uppermost canopy, and flown for expeditions in French Guinea, Gabon, and Cameroon; components were also deployed in Panama and Australia (Hallé & Pascal, 1990) (Fig. 3). This creative canopy access tool has inspired children and researchers world-wide (reviewed in Hallé & Pascal, 1990). Construction cranes represent the most recent tool for safe canopy access (reviewed in Mitchell et al., 2002). The first crane was erected in Panamanian seasonally dry forest by the Smithsonian Tropical Research Institute (Parker, 1995). Cranes were established in Australia, Switzerland, Germany, Japan, Indonesia, the USA, and Venezuela. For financial reasons, the US crane was recently shut down, and the Venezuela crane was decommissioned because of challenges related to its remote location near the Orinoco River.
The canopy raft and hot air balloon not only provided access to the uppermost canopy, but also served as a hook for inspiring children and citizens about science.
Essentially from 1980 to 1995, the toolkit for canopy access was developed by a handful of researchers around the world (reviewed in Lowman & Rinker, 2004). With each method facilitating access to specific regions of forest, and designed for different types of data collection, forest scientists could now conduct rigorous, whole-forest research on both mobile and sessile inhabitants, without restriction to the understory alone.
III. Consequences of whole-tree approaches to forest science
Canopy access tools allowed whole-forest approaches to research that truly changed scientific perspectives on forests, just as tools for soil research have expanded forest science below-ground. Before the advent of canopy biology, most scientists were restricted to studying those portions of the forest that could be viewed at ground level, a veritable tunnel from 0 to 2 m high, usually within arms’ reach and typically representing < 5% of a tall, mature forest. Not surprisingly, such limited observations often resulted in erroneous conclusions. Foremost of these new discoveries facilitated by canopy access were the findings about biodiversity of forests; spatial and temporal variability in herbivory among different heights in forest canopies; new findings about canopy cover and productivity inspired by above-canopy tools such as satellite imagery, especially useful for modeling; the variability of forest denizens, such as epiphytes, along elevational gradients; horizontal and vertical differences in leaf traits, including rates of photosynthesis, within forest canopies; spatial and temporal variation among canopy populations; long-term consequences of environmental changes for canopy biodiversity and processes; interactions between canopy and atmosphere that affect vertical and horizontal gradients in microclimate within the canopy and affect regional and global patterns of temperature and precipitation; and interactions between canopy and forest floor that drive water transport and biogeochemical cycling. Perhaps the most important benefit of safe access into forest canopies has been experimental manipulation of canopy architecture and diversity to test hypotheses concerning effects of these variables on primary production, carbon flux, and canopy–atmosphere and canopy–forest floor interactions (e.g. Dial & Roughgarden, 1995; Whelan, 2001; De Souza & Martins, 2005; Lindo & Winchester, 2007; Mooney, 2007; Richardson et al., 2010; Shiels et al., 2010).
Forest canopy access significantly advanced and, in some cases, changed our perceptions about many aspects of forest ecology, and also increased the accuracy of information related to forest processes and biodiversity. Quite simply, biologists could not accurately measure forest dynamics or their interactions with the atmosphere and global climate without gaining access to the upper reaches of the trees. Access to whole trees, instead of just understory, led to discovery of millions of new species, changing our perception of global biodiversity (Winchester, 2006). In large part, this diversity of canopy organisms reflects the diversity of canopy habitats and microclimatic conditions within the canopy, which can only be measured within the canopy (Andrade & Nobel, 1997; Dial et al., 2004; Cardelús & Chazdon, 2005; Cervantes et al., 2005; Sillett & Van Pelt, 2007). Access to the canopy of the tallest trees in the world was necessary for measurement of leaf water potential at various heights in giant redwoods, Sequoia sempervirens, in order to ascertain that maximum tree height, based on hydraulic conductivity, was 120–130 m (Koch et al., 2004).
Distribution of foliage and foliage properties are primary aspects of forest structure that affect requirements for water and nutrients and rates of photosynthesis, evapotranspiration, net gas exchange, and interception of precipitation, particulates and aerosols (Gutschick, 1984; Ellsworth & Reich, 1993; Harley et al., 1996; Dominy et al., 2003; Fyllas et al., 2009; Asner & Martin, 2011). Canopy foliage is composed of different tree species, which differ in size, shape and various chemical components, and different configurations and chemical composition within trees, based on availability of light, water and nutrients, as well as foliage of associated epiphytes (Ellsworth & Reich, 1993; Dominy et al., 2003; Fyllas et al., 2009; Asner & Martin, 2011).
Obvious differences in foliage distribution arise from variation in leaf size, shape, thickness and within-branch density among tree species, for example, between conifers, with dense needle-shaped foliage, and broad-leaved angiosperms; among broad-leaved species with simple vs compound leaves; and between deciduous trees, with foliage only during the growing season, and evergreens, which retain foliage year-round and often for several years. Foliage size, shape, thickness and density represent important tradeoffs among photosynthetic efficiency, energy and nutrient investment, and ease of replacement (Gutschick & Wiegel, 1988; Gutschick, 1999). Deciduous trees typically retrieve nutrients, especially nitrogen, before senescence (Marschner, 1995), resulting in different qualities of litterfall contributing to canopy–forest floor interaction.
The arrangement of leaves along the three-dimensional branch architecture also varies among tree species and reflects specific adaptations to optimize photosynthetic efficiency. Trees with long-lived leaves that can maintain photosynthesis under diffuse light may retain leaves along branches (e.g. Douglas-fir, Pseudotsuga menziesii (Mirb.) Franco), whereas trees with short-lived leaves or leaves that require full sun may retain only a cluster of leaves at the exposed ends of branches (e.g. Cecropia spp.). Leaf distribution and photosynthetic efficiency also reflect leaf angle relative to branch angle and direction of sunlight and the arrangement of tree crowns of various species in three-dimensional canopy space. Some crowns have denser foliage (higher leaf area index) than do others.
Relying on canopy access, Hietz & Hietz-Seifert (1995a,b) and Cardelús (2007) tackled the challenges of sampling epiphytes, creating standardized techniques with respect to temporal variability: short, intermediate and long-term sampling. Cardelús’ short-term method involves a rapid technique to quantify species richness, and includes standardizing the number of branches as well as the area/branch sampling space. Species counts (presence/absence) per branch were analyzed using sample based rarefaction curves to determine if species saturation is reached (Cardelús et al., 2006). Intermediate sampling methodology involved more extensive canopy data collection to include not only number of epiphytes but also abundance of each species along branch transects or within plots within a three-dimensional canopy space (Cardelús, 2007). Long-term sampling protocols involve methods for measuring species richness, abundance and distribution, as well as demography, whereby researchers return to permanent vertical transects in the canopy marked with permanent tags or flagging tape (e.g. Zotz, 2005).
Canopy access also facilitated more quantified and accurate estimates of arthropod diversity and distribution in whole forests (Basset et al., 2007). The Biodiversity of Soil and Canopy Athropods (IBISCA) is an international research protocol developed by an international team of entomologists in response to the lack of large data sets on the diversity and distribution of arthropods at multiple scales in tropical forests (Leponce et al., 2010). The IBISCA protocol includes multi-scale, multi-taxa, multi-methods, and many researchers and volunteers to collect and process the voluminous collections. IBISCA has set a new ‘industry standard’ of international collaboration and exhaustive baseline data for several tropical sites, with many specimens still under investigation and classification (Basset et al., 2007). IBISCA has illustrated the importance of canopy sampling as well as seeking cost-efficient cataloguing and processing of biodiversity samples, still major hurdles for biodiversity inventories of whole forests. The jury is still out on the exact number of species on our planet (ranging from as low as 10 million to as high as 100 million), but access into whole forests inspired the significantly higher estimates of global species composition (May, 2010).
In the scientific literature published before canopy access, herbivory was usually measured by simplified methods of sampling leaves from understory to mid-canopy. Most estimates indicated c. 5–8% leaf area eaten, based on leaves collected at a point in time (aka, a snapshot), often from low-hanging branches or picked up from the forest floor (e.g. Bray & Gorham, 1964; Odum & Ruiz-Reyes, 1970; Schowalter et al., 1981; Landsberg & Ohmart, 1989). In 1979, Lowman not only used SRTs to monitor whole-tree herbivory, but she also executed monthly monitoring observations to record the amount defoliated from individual leaves over their entire life span. This whole-tree approach led to a two- or three-fold increase in estimates of the amount of foliage consumed by herbivores (mostly arthropods in the case of Australian rain forests) (Lowman, 1984, 1985). Similar corrections were made for Australian dry forests (Lowman & Heatwole, 1992), and neotropical forest canopies (Lowman, 2009b). Measuring whole-forest herbivory not only required canopy access for accuracy, but also relied upon careful attention to vertical changes in temporal and spatial factors including individual leaves, branches, height above ground, crowns, forest stands, and types of forest (Lowman, 1985).
As a result of access into canopies of 800-yr-old, 70-m-tall conifers on Vancouver Island, Canada, Winchester (2006) discovered that perched soils harbored a diverse assemblage of oribatid mites adapted to their arboreal environment and largely distinct from the more familiar assemblages of oribatids associated with litter decomposition on the forest floor. Similarly, Erwin’s initial fogging surveys of neotropical trees led to his extrapolation that there may be over 30 million species on the planet, not the 1–2 million as was previously estimated (Erwin, 1982).
Although not part of the within-canopy access toolkit, remote sensing was an important development that advanced canopy research. Aerial photography pioneered the notion of quantifying volume of timber, conditions of forest stands, and even the shapes of individual crowns (e.g. Aldrich & Drooz, 1967). More recently, satellite imagery, such as provided by Lidar and digital photography, can facilitate mapping of tree crowns, diversity of stands, discrimination of tree crowns and lianas, and even distribution of populations over entire regions (Castro-Esau et al., 2004; Sánchez-Azofeifa & Castro-Esau, 2006; Kalacska et al., 2007; Palace et al., 2008). With larger budgets, multi-sensor airborne sensor platforms such as Lidar can provide information about canopy structure (Asner et al., 2008), condition (Carter & Knapp, 2001) and chemical composition of forest canopies (Asner & Vitousek, 2005). Combined with some degree of ground-confirmation and intensive data collection in the understory, these images enable a detailed analysis of the whole forest, although these technologies remain beyond the reach of most individual researchers at this point in time.
IV. Canopy communities – their inhabitants, environment, and processes
1. Canopy communities
Canopy access in the 1980s led to discoveries of communities of microorganisms, epiphytes and animals that mirror the diversity of canopy habitats and resources. These organisms can also modify canopy structure and canopy interaction with the atmosphere and forest floor. Various lichens, mosses, etc. form epiphytic mats (Nadkarni, 1984; Yanoviak et al., 2007) on branches and boles. Epiphytes represent a major component of the photosynthetic and water-holding capacity of the canopy (Fig. 4) (Pypker et al., 2005; Sillett & Van Pelt, 2007; Díaz et al., 2010). Epiphytes also accumulate arboreal soil and litter and support development of the distinct communities associated with the arboreal soil/litter environment (Yanoviak et al., 2007). Perched soils represent important reservoirs for seeds (seed bank) that may facilitate regeneration (Nadkarni & Haber, 2009). Some epiphytes, such as the birdnest ferns of tropical forests, reach large size on crotches or large branches that have sufficient soil accumulation and are capable of supporting fern weights up to 200 kg fresh weight apiece (Ellwood et al., 2002). Increased weight of large epiphytes following heavy rains may cause breakage of smaller branches. These plants greatly increase habitat area for canopy fauna (Richardson et al., 2000; Ellwood et al., 2002) and for interception of airborne moisture and nutrients (see the last paragraph of section IV. 2).
Distribution of epiphyte size classes in canopies of two emergent trees (a and b) in temperate old-growth rain forest in Chile. From Díaz et al. (2010) with permission from Elsevier.
Plant parasites and endophytes are important components of forest canopies (Carroll, 1988; Shaw et al., 2005). Parasites include those growing externally (e.g. mistletoes, fungi, and strangler figs) as well as those growing internally, often indistinguishable from endophytes (Moffett, 2000). Both groups affect canopy condition by removing nutrients, providing additional resources, and contributing chemicals that aid in defense of the host plant (Carroll, 1988).
Canopy animals represent a diverse and important component of canopy communities. Invertebrates and birds are diverse and functionally important treetop components in both temperate and tropical forests, whereas amphibians, reptiles and mammals are more diverse and important in tropical forests. Although invertebrate diversity mirrors tree species diversity and environmental conditions (e.g. Erwin, 1982; Novotnýet al., 2002, 2006; Gering et al., 2007), most tree crowns host dozens to hundreds of species that represent specialized and generalized herbivores (including folivorous and sap-sucking species), detritivores, predators and parasites (Schowalter & Ganio, 2003). The small size and heterothermy of these organisms make them particularly sensitive to vertical gradients of temperature and relative humidity, as well as variation in resources. Many species (e.g. aphids, scale insects and leaf miners) are small enough to live within individual leaves or within the boundary layer of plant surfaces that have relatively constant temperature and moisture conditions. Even smaller, tardigrades may be common in forest canopies, but very few surveys exist (see Miller, 2004).
Some animal groups are associated exclusively with specific canopy habitats. Epiphyte mats and accumulated soil host rich assemblages of specialized arthropods (Yanoviak et al., 2007). Other arthropods occupy the aquatic environments of treeholes (Yanoviak, 1999) or epiphytes (Richardson et al., 2000). Vertebrates may live and nest in forest canopies (e.g. tree frogs, birds, squirrels and monkeys), whereas some species forage in tree canopies (e.g. snakes, hunting cats, and bats) (Reagan & Waide, 1996; Kays & Allison, 2001; Malcolm, 2004). Increasingly, canopy dwellers show sensitivity to changes in landscape composition, especially forest fragmentation that interrupts large-scale movement among suitable habitat patches (Whelan, 2001; Anzures-Dadda & Manson, 2007; Arriaga-Weiss et al., 2008; Baker & Olubode, 2008; Stouffer et al., 2009).
Interactions among species affect community structure and consequences for canopy processes. For example, predaceous birds vs ants alter canopy herbivore abundances in different ways that affect canopy productivity (Fig. 5) (Marquis & Whelan, 1994; Terborgh et al., 2001; Mooney, 2007). Animals may form or modify structures in canopies as a result of nest-building or other activities. Woodpeckers and other birds excavate cavities in branches and boles that can be used by other animals or eventually fill with water or debris to provide new habitats. Bees, ants and termites construct arboreal nests from sediments and/or organic matter, thereby increasing the complexity of canopy structure.
Effects of bird and/or ant exclusion on total herbivore density and composition (pie charts) in ponderosa pine, Pinus ponderosa Douglas ex Lawson, canopies. Herbivore densities (means ± SE) are for six post-treatment months. Means with different letters differ significantly (P < 0.05). The interaction between bird and ant effects was significant (P = 0.03). From Mooney (2007) with permission from the Ecological Society of America.
2. Canopy–atmosphere interaction
Forest canopies provide a large surface area of branches and foliage for interception of solar heat, precipitation and airflow. Canopy height, canopy cover and vegetation type determine how much shade is provided and precipitation and wind are intercepted before reaching the forest floor (Monteith, 1973; Gutschick, 1999; Juang et al., 2007). Photosynthesis by the forest canopy is the process that stores energy fixed from atmospheric carbon dioxide in carbohydrates and drives whole-forest functions, as well as ecosystem services valued by humans. Respiration reverses this process as the energy of stored carbohydrates is released to perform the various metabolic functions of trees and the community of organisms in the canopy. Fluxes of these and other biogenic gases affect carbon storage and distribution in the canopy and, in turn, influence atmospheric conditions regionally and globally (Lerdau & Throop, 1999; Turner et al., 2005, 2007; Misson et al., 2007).
Taller, denser canopies ameliorate solar heating and significantly reduce temperatures within and below the canopy (Fig. 6) (Foley et al., 2003; Madigosky, 2004; Juang et al., 2007). The forest canopy absorbs solar energy and reflects light and heat, lowering albedo and reducing surface temperatures (Gash & Shuttleworth, 1991; Lewis, 1998; Foley et al., 2003). Albedo is inversely related to canopy height and ‘roughness’ (the degree of unevenness in canopy surface), declining from 0.25 for canopies < 1 m in height to 0.10 for canopies > 30 m height, and reaches lowest values in tropical forests with very uneven canopy surface (Monteith, 1973). Canopy roughness also generates turbulence in airflow (Fig. 7) (Raupach et al., 1996; Finnigan, 2000; Cassiani et al., 2008; Su et al., 2008), thereby contributing to surface cooling by wind (sensible heat loss), evapotranspiration (latent heat loss), and rise of moist air to altitudes at which condensation and precipitation occur (Meher-Homji, 1991; Foley et al., 2003). At night, the canopy absorbs reradiated infrared energy from the ground, maintaining warmer nocturnal temperatures, compared with canopy gaps or deforested sites.
Effects of forest canopies on climatic variables. From Foley et al. (2003) with permission from the Ecological Society of America.
Diagrammatic representation of two extremes in air flow over an edge between forest and clearing. At low foliage density or wind speed, relatively unimpeded air flow is described by an exit flow model (top). At higher foliage density or wind speed, impedance by the canopy is described by a back-facing step (BFS) flow model with a recirculation zone in the clearing where sinking airflow strikes the surface and another recirculation zone at the edge where the back-flow contacts the tall forest canopy. h, canopy height; uyt, streamwise velociety; z, boundary layer height. From Cassiani et al. (2008) with permission from Springer.
Canopies intercept fog or rising clouds, augmenting annual precipitation (Brauman et al., 2010). Deeper and denser canopies intercept more precipitation than do shorter and sparser canopies. Epiphytes increase water interception and storage (Pypker et al., 2006). Dry deposition of particulate materials and nutrients often is a substantial proportion of total atmospheric inputs to forest canopies (Lovett & Lindberg, 1993). Interception of precipitation channels and stores water and dissolved nutrients in canopy reservoirs (such as tree holes and phytotelmata), and reduces the volume and impact of water reaching the forest floor, thereby reducing erosion and facilitating infiltration and storage in litter and soil.
Evapotranspiration contributes to canopy cooling and to convection-generated condensation above the canopy, thereby increasing local precipitation (Fig. 6) (Meher-Homji, 1991; Foley et al., 2003; Juang et al., 2007). Evapotranspiration increases relative humidity above the canopy and coupled with strong advective moisture flux, especially in the tropics, promotes local cloud formation (Trenberth, 1999). Furthermore, volatile chemicals emitted from canopy foliage can serve as precipitation nuclei (Facchini et al., 1999). Canopy removal over large areas, that is, deforestation, has been associated with declining local and regional precipitation (Meher-Homji, 1991; Janssen et al., 2008) as a result of positive feedback between reduced canopy cover, increased albedo and regional drying.
Forest canopies intercept airflow, reducing wind speed, creating turbulence (as described in the second paragraph of this section) and acquiring particles and aerosols from the air. Reduced airflow affects canopy gradients in temperature, relative humidity and, consequently, evapotranspiration rate. Dry deposition of particles (adsorption) and absorption of aerosols provide sediment and material that enhance canopy function (soil development and nutrient input) or stress plants and interfere with canopy function (pollutants). For example, Solberg et al. (2009) reported that European forests, especially pine and spruce forests, have shown greater-than-predicted growth rates over the past 15 yr, explained largely by a fertilization effect of atmospheric nitrogen deposition.
Forest canopies generate a number of volatile organic compounds (VOCs) that influence atmospheric chemistry, especially oxidative potential (Guenther et al., 1996; Heald et al., 2009; Lelieveld et al., 2008). The most abundant VOCs are isoprene and monoterpenes (Lerdau et al., 1997). Tropical forests are the largest source of isoprene (Lerdau & Throop, 1999; Lelieveld et al., 2008). Isoprene biosynthesis and emission rates are related to light intensity, temperature and foliar nitrogen availability, whereas monoterpene biosynthesis and emission rates appear to be controlled primarily by temperature (Harley et al., 1996, 1997; Lerdau et al., 1997; Pressley et al., 2006; Heald et al., 2009). Methanol and acetone also are emitted by many plant species. Canopy foliage and their animal residents emit additional volatile compounds (e.g. plant signaling and defensive compounds and animal pheromones) that have relatively little effect on atmospheric conditions, but are critical to regulating species interactions (Cardé & Baker, 1984; Murlis et al., 1992).
A major effect of these compounds is their light-sensitive oxidation into hydroxyl radicals, ozone, and carbon monoxide (Lerdau et al., 1997; Lelieveld et al., 2008; Heald et al., 2009). Carbon monoxide, in particular, influences the oxidizing capacity of the atmosphere and is involved in photochemical reactions that increase atmospheric ozone concentration. However, isoprene also functions to increase the longevity of methane in the atmosphere, thereby indirectly contributing to global warming (Lerdau et al., 1997; Lerdau & Throop, 1999; Heald et al., 2009). Background isoprene emission by forests appears to be in balance with atmospheric oxidative capacity and may function to maintain atmospheric conditions conducive to forest production, but deforestation and conversion to agricultural or urban uses is likely to disrupt this balance (Lelieveld et al., 2008).
Associated canopy organisms can affect these canopy–atmosphere interactions in a number of ways. Epiphytes can contribute to canopy moderation of forest microclimate. Stuntz et al. (2002) found that epiphytes significantly reduced midday temperatures and evaporative drying in the surrounding canopy, even compared with branches within the same tree that were devoid of epiphytes. Classen et al. (2005) demonstrated that herbivory by both sap-sucking and folivorous insects reduced foliage density enough to reduce crown shading and interception of precipitation and affect temperature and relative humidity around treated trees enough to affect ecosystem processes (Fig. 8).
Effect of herbivory by scale insects, Matsucoccus acalyptus, on soil moisture (a) and temperature (b) in a piñon-juniper (Pinus edulis Engelmann/Juniperus monosperma Engelmann) woodland in northern Arizona during August 1999–June 2002. Treatments included trees that were susceptible or resistant to the scale or susceptible but with scales removed. Different letters indicate significant differences, using contrasts. From Classen et al. (2005) with permission from the Soil Science Society of America.
3. Canopy–forest floor interactions
Forest canopies significantly affect, and are affected by, conditions on the forest floor. Forest canopies intercept sunlight, reflecting heat and shading the forest floor, thereby reducing albedo and cooling the canopy and forest floor (Gash & Shuttleworth, 1991; Foley et al., 2003; Janssen et al., 2008). This insulating effect increases with canopy cover and canopy depth. The temperature at the forest floor under dense, complex canopies typically remains 2–4°C cooler than at the top of the canopy, with the difference between canopy surface and forest floor reaching a maximum of 10–12°C at midday when ambient temperature peaks and disappearing at night (Parker, 1995; Foley et al., 2003; Madigosky, 2004). Litter falling from the canopy (see the sixth paragraph of this section) further insulates the soil surface from temperature extremes. As a result of this canopy cooling effect, temperatures at the forest floor are relatively constant diurnally and seasonally, providing stable conditions for a variety of organisms and processes.
Canopy opening as a result of disturbance, herbivory or deforestation reduces this shading effect (Classen et al., 2005; see Fig. 8). Solar exposure can raise soil surface temperatures to 45°C during midday (Seastedt & Crossley, 1981), creating adverse conditions for many forest floor organisms that control decomposition and soil fertility (Amaranthus & Perry, 1987) and increasing evaporative loss of water. Furthermore, the effects of such soil warming can extend as much as 200 m into undisturbed forest, creating a horizontal gradient in forest floor temperature (Chen et al., 1995). Loss of vegetation cover can initiate a positive feedback between evaporation and reduced precipitation that leads to further vegetation loss (Janssen et al., 2008).
The canopy also intercepts and modifies precipitation, determining evapotranspiration rate (see the fourth paragraph of section IV. 2), throughfall and stemflow chemistry, droplet impact on the forest floor, and erosion (Foley et al., 2003; Pypker et al., 2005; Brauman et al., 2010). Precipitation percolates through canopies with variable impacts to the forest floor (Ruangpanit, 1985; Meher-Homji, 1991). Interception rates increase with increasing canopy surface area and decreasing precipitation volume (Brauman et al., 2010). Throughfall and stemflow show chemical enhancement, relative to raw precipitation, as a result of acquisition of nutrients from material adhered to or leached from foliage and branches during downward flow from the canopy. Foliage fragmentation resulting from herbivory or storm damage increases leaching from open edges of leaves (Kimmins, 1972; Seastedt et al., 1983; Schowalter et al., 1991). Increased nutrient content of throughfall increases flux of nutrients from canopy to forest floor. Water reaching the forest floor in excess of soil storage capacity leaches into streams and is exported from the forest.
Plants require water and nutrients for photosynthesis and canopy growth, and path-length resistance limits the height to which water can be drawn through capillaries, restricting maximum canopy height to 120–130 m (Koch et al., 2004). If soil water becomes limiting, xylem cells cavitate, and the plant exhibits symptoms of drought stress (Mattson & Haack, 1987; Trumble et al., 1993). Some bark beetles detect and use cell cavitation as a cue to water-stressed plants that are less able to produce defensive compounds and thereby become more suitable hosts (Mattson & Haack, 1987). If water limitation is severe, portions of the canopy die, leading to lateral branching, reiteration of trunks arising from the main trunk (Sillett & Van Pelt, 2007), and/or development of platforms that contribute unique habitats for various organisms.
Relative humidity at the forest floor typically is higher than at the top of the canopy, as a result of lower temperature and airflow, with the gradient particularly pronounced at midday (Parker, 1995; Madigosky, 2004). High relative humidity and low airflow minimize direct evaporation of soil moisture. However, when disturbance opens the canopy, soil exposure and warming increase the rate of evaporation and can lead to soil desiccation and/or flooding (Classen et al., 2005; see Fig. 8). Counteracting this trend is the reduced interception of precipitation and uptake of soil water by the opened canopy, increasing soil moisture.
Biomass and nutrients are transferred from the canopy to the forest floor through several pathways. Carbohydrates produced in the canopy move downward through the phloem and are used for metabolic activity throughout the plant or are stored in woody tissues and roots. Allocation of net primary production to below-ground plant parts is often 50% or more in forests (Coleman et al., 2004). Furthermore, 20–50% more carbon enters the rhizosphere from root exudates and exfoliates than is measured in root biomass at the end of the growing season (Coleman et al., 2004). Root exudates support a variety of associated organisms, particularly nitrogen-fixing bacteria and mycorrhizal fungi that are critical to adequate uptake of water and nutrients by roots. Exudates also contribute to soil aggregate formation, a process that increases soil nutrient retention (Coleman et al., 2004). Canopy materials rain to the forest floor as litterfall, affecting whole-forest dynamics. The degree of canopy shading and amount of throughfall govern litter temperature and moisture, two factors that control decomposition and respiration rates (Meentemeyer, 1978; Whitford et al., 1981; Seastedt, 1984; Prescott, 2002). Decomposition rate also is a function of litter quality, as determined by tree species and litter material, for example, foliage vs wood (Prescott, 2002; Fonte & Schowalter, 2004).
Canopy organisms can substantially affect canopy–forest floor interactions. Epiphytes added 140 kg per tree in a temperate rain forest in Chile (Díaz et al., 2010) and added additional mass when filled with water. Breakage of over-weighted branches during storms is common. A number of insects have life cycles that are divided between canopy and forest floor habitats. Some folivores feed on canopy resources during immature stages and pupate on the forest floor (e.g. Selman & Lowman, 1984; Miller & Wagner, 1984). Others feed on below-ground tissues during immature stages but emerge and affect canopy structure as adults, for example, cicadas, which can cause substantial twig and foliage loss during oviposition in twigs. Insect outbreaks add substantial amounts of relatively nutrient-rich animal tissues, fecal material, and green foliage fragments, as well as nutrient-enhanced throughfall to the forest floor (Grace, 1986; Hollinger, 1986; Frost & Hunter, 2004, 2007, 2008). These materials stimulate decomposition and mineralization on the forest floor (Fig. 9) (Seastedt & Tate, 1981; Schowalter & Crossley, 1983; Schowalter et al., 1991, 2011; Frost & Hunter, 2004, 2007, 2008; Fonte & Schowalter, 2005). Roosting birds and bats can break branches and add feces that enrich soils below rookeries. Some forest-floor animals (e.g. elephants) can reach and substantially influence canopy structure and function up to 4–5 m height, and canopy detritivores contribute to decomposition in situ before material reaches the forest floor (Fagan et al., 2006; Lindo & Winchester, 2007; Cardelús, 2010).
Soil NH4-N concentrations with (diamonds) or without (triangles) added insect frass, as estimated by ion-exchange resin bags. Data are means ± 1 SE (n = 60). RM indicates that data were analyzed as nonparametric repeated measures. From Frost & Hunter (2004) with permission from the Ecological Society of America.
V. The role of forest canopies in providing ecosystem services
Many canopy processes provide essential ecosystem services on which human beings depend for survival. Forest ecosystem services are linked directly to the canopy by photosynthesis. In addition, canopy cover and interception of precipitation percolating through the canopy directly affect water flux and storage in the forest floor. In Guanxi, China seven surrounding regions paid Jinxiu County for water and soil conservation provided from its forests. Despite a lack of scientific literacy or extensive data sets, these people realized that forests mitigate floods, conserve fresh water, augment soil quality, and provide socio-economic benefits by ameliorating any hydrological extremes. Similarly, countries are increasingly aware that forest canopies regulate Earth’s climate by controlling greenhouse gas exchange such as carbon dioxide. Forest ecosystems store approximately four times more carbon than found in the atmosphere, whereas tropical deforestation caused almost one-quarter of the globe’s total greenhouse gas emissions in the 1990s (reviewed in Conte et al., 2011). Models to predict whole-forest changes require information about forest canopies, as well as understory and below-ground components.
In the Amazon, plants produce chemical defenses against insect attack, and these chemicals, in turn, are sources of medicines, used by indigenous people as well as by pharmaceutical companies (Helson et al., 2009). Other important ecosystem services include foods, construction materials, genetic libraries, gas exchange, carbon storage, fresh water conservation and circulation, and productivity as the basis of many food chains (reviewed in Lowman, 2009a; Schowalter, 2012; White et al., 2010). Both timber and nontimber forest products play a key role in the economy of many countries, and require careful management to ensure sustainability (Nelson et al., 2011).
These are some of the many reasons why we should worry about modifying or destroying tropical (or other) forests. When these providers of global services are altered, the changes that occur may have repercussions on a global scale (Lewis et al., 2009). Conservation of tropical forests, including their diverse and productive canopy regions, is a relatively straightforward proposition; and the effects of reducing, modifying, and removing forests are not only well understood, but hundreds of scientific studies have measured and modeled the consequences of deforestation (reviewed in Laurance & Peres, 2006). Despite the direct links between ecosystem services and healthy forests (e.g. Vittor et al., 2006), new solutions are required – hence the notions of recruiting diverse stakeholders to the decision-making table, or utilizing innovative conservation ‘hooks’ as described in the next section.
VI. Using canopy science as a ‘hook’ to inspire forest conservation
Since researchers first ascended in the 1970s into the upper reaches of forest and expanded their research into whole forests, millions of hectares of tropical rain forests have disappeared, along with thousands of undiscovered species. Similar loss has occurred in temperate forests, some with happy endings via reforestation, but often without the integrity and complexity of the original canopies. Changes in forest cover affect regional and global climate (Raupach et al., 1996; Finnigan, 2000; Foley et al., 2003; Juang et al., 2007; Janssen et al., 2008). Loss of forest canopies and consequences for ecosystem services are critical issues for subsequent generations. The next decade is critical. New ways to inspire forest conservation are urgently needed, in order to retain forest canopies as essential components of healthy ecosystems that in turn translate into sound economics.
One ‘low-hanging fruit’ is the maintenance of ecosystem services in secondary, or restored forests. While they may not have the complexity of primary forests, secondary forests nonetheless can support diverse floras and faunas (Chazdon, 2008; Dent & Wright, 2009) including native seed sources, pollinators, sustainable harvests, and productivity that in turn drives other ecosystem services, such as water quality (Uriarte et al., 2011; Yackulic et al., 2011). Farmers represent an emerging group of stakeholders working to restore secondary forest canopies. Eighteen countries in Africa are currently engaged in trials of fertilizer trees as part of a new agroforestry movement, ‘evergreen agriculture’ (Garrity et al., 2010). Canopy foliage provides shade and litterfall nutrients for crops grown beneath. During her lifetime, Wangari Matthai oversaw the planting of millions of trees in her home country of Kenya.
These African countries may learn from the experience of Australia, which suffered widespread social and economic problems when forest diebacks ravaged rural landscapes in the late 20th Century (Lowman & Heatwole, 1992). In this case, over-clearing for sheep and cattle grazing, plus the accompanying loss of insectivorous birds, led to outbreaks of herbivorous beetles that defoliated and ultimately destroyed the remaining trees and their canopies. A program called ‘a billion trees by 2000’ was initiated, one farm at a time (Heatwole & Lowman, 1987). In Brazilian Amazonia, human modifications have led to significant increases in the fire regimes of secondary and disturbed forests, sometimes as much as 42% higher fire frequency (Aragao & Shimabukuro, 2010). Restoring degraded forests may require the suppression of some human activities, and even outright government intervention for successful restoration of healthy canopies.
Despite cautious optimism about the ecosystem services provided by secondary forests, the conservation of primary forests has become an increasing priority for most countries. Conventional stakeholders of many tropical forests are large government and conservation nongovernmental organizations, but the increasing decline of forests necessitates wider engagement by diverse stakeholders (reviewed in Lowman, 2009a). Use of forest canopies for cultural or ecotourism ventures may offer some reversal of regional deforestation: canopies provide an important cultural value, recreational activities that link to economic benefits, and a unique ‘hook’ that may inspire conservation of the whole forest.
Religious leaders represent an important, yet under-utilized, group of stakeholders in forest conservation. Sustainable land use practices and religious stewardship share similar conservation values (reviewed in Verschuuren et al., 2010). One notable case is the Coptic or Christian Orthodox church in Ethiopia, where churchyards protect the last remaining tracts of native forests (Wassie-Eshete, 2007; Wassie et al., 2009; Lowman, 2011) (Fig. 10). These church forest patches provide sanctuary for native trees and other biodiversity, soil and fresh water conservation, pollinators, and a vital cultural and spiritual heritage (Bossert et al., 2006). Religious leaders are currently working with conservation biologists to educate local people about the ecosystem services of these remaining church forests, in particular the links between forests and fresh water, insect pollinators, honey, and shade (Lowman, 2011). Northeastern Ethiopia has lost over 95% of its forest cover, so the partnership between religion and science has the capacity to save the remaining 5% (Bongers et al., 2006).
Coptic Orthodox priests are stewards of northeastern Ethiopia’s last remaining forest patches, which provide essential ecosystem services to local communities.
A final example of diverse stakeholders fostering forest conservation involves ecotourism as a source of sustainable income. When canopy researchers share their canopy access tools, the outcome can provide an economic incentive for local communities to conserve their forests rather than harvest them. In many tropical regions, the payments derived from harvest operations usually exceed the economic benefits of leaving the forest intact (Novotný, 2010); but the harvest revenues represent tempting, short-term profits. Ecotourism operations – involving canopy walkways, bird watching, education-based nature tours, spas and holistic medicine – can lead to sustainable income streams for local communities. Currently, over 20 canopy walkways operate in tropical forests around the world, serving research as well as ecotourism (http://www.canopyaccess.com). Walkways range in cost from US $100 to US $3000 m−1 to construct, but they provide educational opportunities to teach visitors about forest conservation, in addition to sustainable income (Lowman, 2009b). In the Sucasari tributary of the Rio Napo in Peru, the world’s longest canopy walkway provides employment for > 100 local families, as well as education for thousands of visitors each year (Lowman, 2009b) (Fig. 11). Similar success stories exist for walkways in Western Samoa, Ecuador, and Gabon. At many sites, the benefits are less transparent, simply because Western accounting measures are not employed; but the conservation success is evident (Lowman, 2009b). In other cases, social media have leveraged diverse forest conservation stakeholders, including rock bands, clothing companies, school children, and Hollywood (see http://www.treefoundation.org).
The world’s longest canopy walkway, near the Sucasari tributary of the Rio Napo, Peru, provides employment for over 100 local families through ecotourism.
VII. Conclusions –‘black boxes’ in canopy science that remain
Currently, over half of the world’s forests have been cleared, burned or harvested. In some countries such as Ethiopia and Madagascar, < 5% of the original forests remains, while 95% remains in Surinam and Guyana. This disparate approach to forest conservation, coupled with our knowledge that forests represent a critical global resource, indicates that treetops are at significant risk over the next few decades.
In addition to the over-arching conservation priorities, forest canopies represent a hot-spot for cutting-edge research. Canopy science still needs improved scaling of data from leaf to crown to canopy from local to global scales; demystifying of critical pathways that link transport of water and nutrients to and from the canopy via roots, branches, and bole; improved remote-sensing capabilities to distinguish effects of natural vs anthropogenic stressors on canopy health; expanded research on effects of interactions among canopy biodiversity and processes including herbivory, throughfall, net primary productivity (NPP), canopy–atmosphere interactions, and canopy–forest floor interactions; and an expanded network of towers and sensors to verify on site data from remote sensing. Unanswered questions to be addressed by future research include:
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How many species exist in tropical forest canopies, and what complex interactions of species are currently threatened by deforestation?
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What specific interactions between canopy biodiversity and processes serve as critical drivers for forest health? What is the prognosis for the continued health of these interactions?
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What factors accelerate forest canopy restoration? How will events such as insect outbreaks and warming temperatures impact the health of existing forests?
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How do canopies respond to climate change and what factors might buffer them from irreversible degradation?
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What types of forest canopies are at greatest risk from environmental changes, and how can we ameliorate their degradation? What are accurate assessments of forest canopy loss in different geographical regions?
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Can we predict how canopy processes affect ecosystem services such as water filtration and fresh water conservation, pollination, and food supplies, and the consequences of canopy removal, in various regions? Can metrics be created to allow accurate accounting of these values by local and regional governments?
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How do forest canopies affect human health?
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How can we educate the public, especially policy-makers, about the importance of conserving forest canopies and their inhabitants?
Acknowledgements
For one of us (M.L.), research in forest canopies was inspired by walking in the footsteps of Tansley as an MSc student in ecology at the University of Aberdeen, Scotland. In the classroom, Dr Charles Gimmingham spoke in glowing terms about Tansley’s work, and our MSc class ventured into the heathlands to see first-hand some of the vegetation representing Tansley’s legacy. My advisor, Peter Ashton, helped me construct a scaffold adjacent to stands of Scottish birch trees, to compare the understory versus canopy phenology of Betula species along elevational gradients. This was my inaugural canopy access experience, although those metal scaffolds were amazingly cold due to the frigid spring temperatures of Aberdeenshire. I went from chilly Scotland to the humid tropics of Queensland, Australia where the trees were too tall for scaffolding. In a moment of creative inspiration, I determined that the same equipment used by the Sydney University Spelunking club to descend into a cave might also propel me up into the tree canopy. For the other of us (T.S.), interest in canopy research was born from PhD research on effects of canopy fauna on biogeochemical cycling, under the direction of Dr Dac Crossley, who pioneered the use of branch bagging to assess canopy arthropod abundance and effect on canopy processes during the International Biological Programme. Since then, I have had the privilege of conducting canopy research in a variety of boreal, temperate and tropical forest ecosystems and evaluating the effects of natural and anthropogenic disturbances on canopy communities and processes. This paper is published with approval of the Director of the Louisiana Agricultural Experiment Station, as manuscript number 2012-234-6705. For these moments of inspiration (combined with the proverbial 99% perspiration), both of us are grateful to our global ‘family’ of canopy scientists, who shared risks to explore and seek to understand the eighth continent of the world: forest canopies.
