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Colonization Strategies of Two Liana Species in a Tropical Dry Forest Canopy

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Colonization Strategies of Two Liana Species in a Tropical Dry Forest Canopy BIOTROPICA 39(3): 393–399 2007 10.1111/j.1744-7429.2007.00265.x Colonization Strategies of Two Liana Species in a Tropical Dry Forest Canopy Gerardo Avalos1,2,5, Stephen S. Mulkey3, Kaoru Kitajima3,4, and S. Joseph Wright4 1The School for Field Studies, Center for Sustainable Development Studies, 10 Federal St., Salem, Massachusetts 01970, U.S.A. 2Escuela de Biolog´ıa, Universidad de Costa Rica, Ciudad Universitaria "Rodrigo Facio" San Pedro, San Jose,´ Costa Rica 3Department of Botany, University of Florida, 220 Bartram Hall, P.O. Box 118526, Gainesville, Florida 32611-8526, U.S.A. 4Smithsonian Tropical Research Institute, Box 2072, Balboa, Ancon,´ Republic of Panama ABSTRACT Lianas impose intense resource competition for light in the upper forest canopy by displaying dense foliage on top of tree crowns. Using repeated access with a construction crane, we studied the patterns of canopy colonization of the lianas Combretum fruticosum and Bonamia trichantha in a Neotropical dry forest in Panama. Combretum fruticosum flushed leaves just before the rainy season, and its standing leaf area quickly reached a peak in the early rainy season (May–June). In contrast, B. trichantha built up foliage area continuously throughout the rainy season and reached a peak in the late rainy season (November). Both species displayed the majority of leaves in full sun on the canopy surface, but C. fruticosum displayed a greater proportion of leaves (26%) in more shaded microsites than B. trichantha (12%). Self-shading within patches of liana leaves within the uppermost 40–50 cm of the canopy reduced light levels measured with photodiodes placed directly on leaves to 4–9 percent of light levels received by sun leaves. Many leaves of C. fruticosum acclimated to shade within a month following the strongly synchronized leaf flushing and persisted in deep shade. In contrast, B. trichantha produced short-lived leaves opportunistically in the sunniest locations. Species differences in degree of shade acclimation were also evident in terms of structural (leaf mass per area, and leaf toughness) and physiological characters (nitrogen content, leaf life span, and light compensation point). Contrasting leaf phenologies reflect differences in light exploitation and canopy colonization strategies of these two liana species. Abstract in Spanish is available at http://www.blackwell-synergy.com/loi/btp Key words: Bonamia trichantha; Combretum fruticosum; light acclimation; Panama. LIANAS FORM A DISTINCTIVE STRUCTURAL ELEMENT OF TROPICAL physiology of liana leaves, even though such studies would provide FOREST CANOPIES and exhibit a variety of mechanisms of ascen- insight into canopy interactions between lianas and trees, as well as sion, growth patterns, physiological strategies, and morphologies among different liana species. (Schnitzer & Bongers 2002). Lianas can comprise 25 percent of Leaf phenology and shoot architecture influence the quality upright, understory stems (Putz 1984), contribute significantly of the light environment experienced by individual leaves through- to species diversity and productivity (Gentry & Dodson 1987, out their lifetime, and thus, are linked to species differences in Hegarty 1991), influence forest regeneration (Pinard & Putz 1993, leaf life span and leaf functional traits (Kikuzawa 1995, Kitajima Schnitzer et al. 2000, Phillips et al. 2005), and compete for water et al. 2005). Some plants continue shoot extension throughout the (Perez-Salicrup´ & Barker 2000) and light with host trees (Clark & growing season continuously producing new leaves on the sunniest Clark 1990). In a tropical dry forest, 30 percent of the canopy surface portion of the crown. In these species, leaves become increasingly surveyed under a canopy crane was occupied by liana foliage (Avalos shaded as they age, and photosynthetic rates decline rapidly as ni- & Mulkey 1999b). Lianas represent one of the most dynamic life trogen and other mobile nutrients are reallocated to new leaves (e.g., forms of tropical forests, often reproducing clonally and exploiting Hikosaka et al. 1994, Kitajima et al. 2002). Consequently, leaf life all forest layers from the canopy surface to the deepest soil strata span may be short in these species, because the potential of mature where roots are found (Holbrook & Putz 1996). Because lianas have leaves to acclimate to shade is morphologically constrained (Oguchi proportionally less support biomass than trees (Holbrook & Putz et al. 2003), and inefficient self-shaded leaves senesce as their net 1996), they should be better able to exploit heterogeneous canopy carbon balance approaches zero (Ackerly 1999). This strategy, found light conditions through flexible extension growth. Unfortunately, among many pioneers, opportunistically exploits the highest light most studies of lianas and their impact on forest regeneration are availability and allows rapid growth rates. The opposite strategy based on ground surveys, which are inherently limited. From the is to produce leaves in a seasonal flush, which results in quick ground, it could be difficult to distinguish liana and tree leaves, and self-shading of many leaves even before they become fully mature. liana stem density does not necessarily correlate with liana leaf area Consequently, crowns of species following this strategy consist of displayed on top of the canopy. Limited accessibility to the forest both sun and shade acclimated leaves that persist for a prolonged canopy has historically constrained in situ studies of phenology and time, often throughout the growing season. Such species produce a greater crown leaf area index (Canham et al. 1994, Montgomery Received 31 October 2005; revision accepted 28 June 2006. & Chazdon 2001, Kitajima et al. 2005), exerting strong resource 5 Corresponding author; e-mail: avalos@fieldstudies.org competition for light by casting denser shade below. Both strategies C 2007 The Author(s) 393 Journal compilation C 2007 by The Association for Tropical Biology and Conservation 394 Avalos, Mulkey, Kitajima, and Wright have been found among tree species (Kikuzawa 1995, Kitajima et al. essary. While our samples most likely included multiple individuals, 2005). However, we are unaware of published studies on the phe- and we traced them down to the ground whenever possible, actual nological and physiological diversity of leaves among liana species. genet identity could have been lost due to mechanical or herbivory This type of functional diversity must be ultimately linked to their damage. strategies of light competition with each other, and with their host canopy trees. LIGHT GRADIENT WITHIN LIANA PATCHES.—Daily variation in pho- Here, we report the patterns of canopy colonization, leaf dis- tosynthetic flux density (PFD) was measured with GaAsP photodi- tribution, leaf phenology, and gas exchange properties of two lianas ode (G1118, Hamamatsu, Japan) positioned in the middle of the Combretum fruticosum (Loefl.) Stuntz (Combretaceae) and Bonamia adaxial surface of individual leaves subsampled in both sun and trichantha Hallier f. (Convolvulaceae). These are the two most com- shade microsites. The photodiodes were calibrated against a quan- mon lianas in the area accessed by the canopy crane at Parque Nat- tum light sensor (Li-190SA, Li-COR, Lincoln, Nebraska, U.S.A.) ural Metropolitano, Panama (Avalos & Mulkey 1999b). The two under open-sky conditions. Total daily PFD was calculated from species differ in seasonality of leaf production and patterns of mi- 5 min averages for PFD sampled every 5 sec and recorded with crohabitat use, providing an opportunity to explore how their leaf LI-1000 data loggers. Care was taken to maintain the natural leaf phenology may be linked to their light exploitation strategies, leaf angle and orientation during the measurements. For typical leaf distribution under sun and shade microhabitats within the canopy, and solar angles, cosine-error correction for these sensors would shade acclimation potential, and leaf life span. Our ultimate goal is have little effect on estimated total daily PFD (Pearcy et al. 1990). to examine how these functional leaf traits determine the ability of The LI-1000 dataloggers were left in the field for five consecutive lianas to cast shade and compete for light with host trees. days, and were moved to different patches of the two species every 2 wk, resulting in a total of 18 and 19 d for sun and shade leaves of C. fruticosum, and 16 d each for sun and shade leaves of B. METHODS trichantha between June 21 and July 24, 1994. Data collected by sensors found in inappropriate positions, or fallen off the leaf, were STUDY SITE.—The study was conducted in the Parque Natural discarded. Metropolitano, near Panama City, Panama (8◦59 N, 79◦33 W, elevation 150 m). This 265-ha site is covered with a 100- to 150-yr DISTRIBUTION OF FOLIAGE UNDER SUN AND SHADE CONDITIONS.— old stand of tropical dry forest with a canopy height of 30–40 m. In the early rainy season (July 1994), we measured the proportion The majority of annual rainfall (mean = 1800 mm, ACP 2002) of leaves displayed under distinctive sun and shade microenviron- occurs during the rainy season from May through mid-December. ments within the patches of C. fruticosum and B. trichantha using a The upper canopy of this forest was approached from above with a dismountable plastic cubic frame (40 × 40 × 40 cm) constructed 42-m tall construction crane. The forest under the crane is domi- with PVC pipes. This cube was first placed to include sun leaves nated by long-lived species that can persist in mature stands, such as within 40 cm of the canopy surface. All leaves inside the cube in Anacardium excelsum (Anacardiaceae) and Luehea seemannii (Tili- this topmost position were counted and designated as sun leaves. aceae), as well as the early successional species Castilla elastica and The cube was then disassembled, except for the bottom square, and Cecropia longipes (Moraceae). Crown architecture, foliage distribu- reassembled using the former bottom square as the new top square tion, and light utilization patterns of the seven most common tree to count all leaves enclosed within the next 40 cm of the canopy.
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