WHEN IS A GAP NOT A GAP? LIGHT LEVELS AND LEAF AREA INDEX
IN BAMBOO-FILLED GAPS IN A CHILEAN RAIN FOREST

CUANDO UN CLARO NO ES UN CLARO?: NIVELES LUMINICOS E
INDICE DE AREA FOLIAR EN CLAROS OCUPADOS POR CHUSQUEA
QUILA, EN UN BOSQUE LLUVIOSO CHILENO

Christopher H. Lusk*

*Departamento de Botánica, Universidad de Concepción, Casilla 160-C, Concepción, Chile.

ABSTRACT

Bamboos of the genus Chusquea are aggressive colonisers of tree-fall gaps in the temperate rain forests of southern Chile. Chusquea thickets inhibit regeneration of tree species, suggesting that light levels beneath bamboo-filled gaps may be lower than beneath tall forest. Two LAI-2000 canopy analysers were used to compare diffuse light availability beneath five Chusquea quila thickets and five neighbouring tall forest stands, in a low altitude (È 400 m a.s.l.) old-growth temperate rain forest in Parque Nacional Puyehue (40º39'S). Leaf area indices (LAI) of these two vegetation phases are also compared. Average diffuse light levels beneath bamboo thickets (1.5 %) were only slightly lower than those beneath tall forest (1.7 %). Similarly, mean leaf area index of Chusquea thickets (6.1) was slightly higher than that calculated for tall forest stands (5.3). However, measurement of leaf area index with the LAI-2000 is likely to overestimate the actual photosynthetic surface area of bamboo thickets, due to retention of dead leaves by Chusquea. On the other hand, LAI of tall forest stands is underestimated, due to the omission of forest floor vegetation < 50 cm tall. The abundance of Chusquea thickets in old-growth forest, and their ability to retain sites by suppression of tree regeneration, suggests that a two-phase positive-feedback vegetation switch model is appropriate for the dynamics of these forests.

Keywords: Chusquea, diffuse light, forest dynamics, LAI-2000, positive feedback vegetation switch.

RESUMEN

Los bambús del género Chusquea son colonizadores agresivos de claros en los bosques lluviosos templados en el sur de Chile. Los matorrales de Chusquea, que se desarrollan tras la formación de los claros, suprimen la regeneración de las especies arbóreas, llevando a pensar que los niveles lumínicos bajo los bambú podrían ser inferiores a los que prevalecen bajo el bosque cerrado. Se usaron dos analizadores de doseles LAI-2000 para comparar disponibilidad de luz difusa bajo cinco matorrales de Chusquea quila y cinco rodales aledaños de bosque cerrado, en un bosque lluvioso antiguo ubicado ubicado a una elevación de È 400 m s.n.m. en el Parque Nacional Puyehue (40º39´S). Además se comparó el índice de área foliar de estos dos tipos de vegetación. El nivel promedio de la luz difusa bajo los matorrales de C. quila (1,5 %) fue levemente menor que el medido bajo el bosque cerrado (1,7 %). Asimismo, se midió mayor índice de área foliar para los bambús (6,1) comparado con el bosque cerrado (5,3). Sin embargo, las mediciones de índice de área foliar con el LAI-2000 probablemente sobreestiman la superficie asimilatoria efectiva de los matorrales de bambú, debido a la retención de hojas muertas por los culmos de C. quila. Por otra parte, el índice de área foliar del bosque es subestimado, debido a la omisión de la vegetación del piso (< 50 cm en altura). La abundancia de los matorrales de Chusquea spp. en los bosques antiguos, y su capacidad de retener los sitios mediante la supresión de la regeneración de los árboles, sugiere que un modelo bifásico de retroalimentación positiva es apropiado para la dinámica de estos bosques.

Palabras claves: Chusquea, dinámica forestal, LAI-2000, luz difusa.

INTRODUCTION

In most forests, canopy gaps created by tree deaths provide the most favourable sites for regeneration of canopy tree species (Pickett & White 1985). However, in some cases, intense competition from understorey plants or lianas can limit opportunities for establishment of tree seedlings in gaps (Hiura et al. 1996; Schnitzer et al. 2000). In extreme cases, reversion of gaps back to tall forest can be delayed for decades by vigorous growth of such plants (Schnitzer et al. 2000).

In the temperate forests of South America, bamboos of the genus Chusquea often form dense thickets in tree-fall gaps, especially on mesic low-altitude sites (Veblen 1982). Tree seedling densities beneath Chusquea thickets are often lower than beneath neighbouring tall forest stands (Veblen 1982; González 1999). Recruitment opportunities for tree species in gaps colonised by bamboos appear to largely restricted to elevated microsites on logs (Veblen et al. 1980a), and to brief periods after periodic synchronous flowering and death of the bamboos, at intervals of 15 to 25 years (Veblen 1982). It seems likely that bamboos often cycle through more than one generation in large gaps before eventually ceding to tall forest. Chusquea bamboos therefore appear to have a profound influence on the dynamics of South American temperate forests.

Dense thickets of Chusquea can attain a standing biomass as high as 150 t ha-¹, and an annual production of > 10 t ha^-1 (Veblen et al. 1980b). The scarcity of regeneration beneath such thickets suggest that the bamboos may cause greater light extinction than tall forest, presumably reflecting higher leaf area indices. However, to date there are no data on light levels beneath Chusquea stands, or leaf area index of bamboo thickets. In this short communication, I compare leaf area index and diffuse light availability beneath canopy gaps colonised by Chusquea quila Kunth and beneath neighbouring closed canopies, in a low-elevation evergreen rain forest in south-central Chile.

METHODS

Study area

The study was carried out in low-altitude (350 - 400 m a.s.l.) Valdivian rainforest in the Anticura sector of Parque Nacional Puyehue (40º39'S, 72º11'W). The forest canopy, 25 to 35 m in height, is dominated by the broadleaved evergreens Laureliopsis philippiana (Looser) Schodde, Aextoxicon punctatum R. et P. and

Eucryphia cordifolia Cav. with occasional emergent Nothofagus dombeyi (Mirb.) Oerst. up to 45 m tall.

Instrumentation

Diffuse light availability and leaf area index (LAI) were measured using a pair of LAI-2000 canopy analyzers (Li-COR, Lincoln, Nebraska). One instrument was used to take measurements within the forest, while the other was placed at the centre of a clearing of about 120 m diameter, providing clearance of the 148º field of view percieved by the sensors, and programmed to take readings at 60 sec intervals. Integration of data from the two instruments enabled estimation of % diffuse non-intercepted irradiance in the visible range, at sites within the forest. As the LAI-2000 operates only with diffuse light, measurements were carried out on overcast days, or in late afternoon, when the solar disc was outside the field of view. Recent work has confirmed that % diffuse irradiance measured with the LAI-2000 is a good surrogate of spatial variation in mean daily photosynthetic photon flux density (Machado & Reich 1999) within a climatically homogeneous area.

The LAI-2000 estimates leaf area index (m² per m² land surface) on the basis of the gap fraction present in the 148º field of view, assuming that foliage elements are randomly distributed in the canopy, and randomly oriented with respect to azimuth (Welles & Norman 1991).

Sampling

Five large gaps caused by multiple tree falls were chosen subjectively, all at least 30 m wide on the shortest axis. All gaps contained dense stands of Chusquea quila > 2m tall, with scattered tree sapling and shrubs occasionally overtopping the bamboo. Measurements with the LAI-2000 showed that diffuse light availability above the bamboo was generally > 35 % of that in the 2-ha clearing.

A line transect was run across each gap, and measurements taken at random intervals. A total of 10 to 12 points was sampled in each gap. At each point, measurements were made at a height of 50 cm above ground, as low as is feasible with the LAI-2000. Light attenuation by herbaceous vegetation in the understorey was therefore not measured. This means that leaf area index is underestimated for tall forest, because of the omission of the ground layer. Within 50m of each gap, measurements were also made on a similar transect of 10 to 12 points laid out under tall forest with closed canopy.

For analysis, each pair of transects (Chusquea thicket + tall forest vegetation phases) was treated as a block. Data analysis was carried out using JMP Statistical Software (SAS Institute, Cary, NC).

Table 1. ANOVA to test for effects of site and vegetation phase on understorey diffuse light levels (%) and leaf area index.

Tabla 1. ANDEVA para evaluar los efectos de sitio y de tipo de vegetación sobre la penetración de luz difusa al piso (%), y el índice de área foliar.

Dependent variable	Whole model		Source of variation
			Site		Phase		Interaction
	r2	P	F-ratio	P	F-ratio	P	F-ratio	P
Diffuse light	0.13	0.82	0.09	0.78	0.69	0.44	0.15	0.71
LAI	0.46	0.26	0.01	0.91	4.86	0.07	0.27	0.62

RESULTS

Diffuse light levels were slightly lower beneath C. quila thickets than in tall forest understoreys (Fig. 1). However ANOVA showed no significant effect of vegetation phase, nor any evidence that site-to-site variation had any significant influence on understorey light levels, nor evidence of interaction between site and vegetation phase (Table 1).

Leaf area index of C. quila thickets was on average slightly higher than that of tall forest stands (Fig. 2). ANOVA showed that site-to-site variation had no significant influence on LAI (Table 1). There was a marginally significantly effect of vegetation phase (P = 0.07), and no evidence of interaction between site and vegetation phase.

DISCUSSION

Leaf area indices and forest understorey light levels reported here are similar to those documented for other temperate forests (Schulze et al. 1994; MacDonald & Norton 1992; Hollinger 1987). However, the percentage of diffuse light reaching the understorey beneath tall forest stands in Parque Nacional Puyehue is slightly higher than values typically reported for closed-canopy tropical rainforests (Canham et al. 1990; Torquebiau 1988).

Light levels were only slightly lower beneath Chusquea quila thickets than in understories of neighbouring tall forest stands (Fig. 1). Insufficient light availability per se is therefore possibly not a sufficient explanation of the failure of shade-tolerant tree species to regenerate in gaps occupied by bamboo. The sudden onset of shading resulting from the very rapid growth of bamboos (up to 9m per year according to Veblen 1982) may also pose problems for tree seedlings. The juveniles of most Chilean rain forest trees have leaf lifespans > 2 years (Lusk & Contreras 1999), and as production of new leaves is probably the most important mechanism of acclimation to light environment, their foliage turnover rates may limit their ability to adjust to sudden changes (cf. Mohammed & Parker 1999).

Leaf area indices measured for Chusquea thickets were slightly higher than those measured for tall forest (Fig. 2). This is surprising, as interspecific variation in leaf area indices of woody plants is thought to be determined mainly by leaf-level light compensation points (Givnish 1988), and the scarcity of Chusquea beneath dense tree canopies suggests that it is less tolerant of shade than the seedlings of associated tree species such as Aextoxicon punctatum and Laureliopsis philippiana.

How do Chusquea thickets then develop such high leaf area indices? The very rapid growth rates documented by Veblen (1982) for Chusquea spp. imply that light environments of individual Chusquea leaves will change rapidly during the growing season, older leaves quickly becoming shaded by newer ones. The process of leaf senescence and abscission may lag behind the production of new leaves, and furthermore inspection of Chusquea thickets shows that dead leaves are retained on culms for some time. However, the LAI-2000 does not distinguish between dead and live leaves, both of which cause light extinction. The actual area of live leaves above compensation point is therefore almost certainly lower than the leaf area index of 6.1 estimated in this study, although it is difficult to gauge the magnitude of this error.

The abundance and persistence of Chusquea thickets in many old-growth Chilean rain forests (Veblen et al. 1996), their thorough occupancy of site resources (as evident from high leaf area index and light extinction), and their inhibition of tree regeneration, suggest that it is inappropriate to regard them as "seral" vegetation. In view of their abundance in the landscape, and the scarcity of tree regeneration beneath thickets, it seems likely that bamboos can cycle through more than one generation on sites colonised after tree falls, thus retaining individual sites for several decades. A positive-feedback vegetation switch model (Wilson & Agnew 1992) therefore seems appropriate for the dynamics of old-growth forests in the region. Both vegetation phases of old-growth forest (tall forest and Chusquea thickets) appear to promote their own continued occupancy of the site, suppressing invasion by the other phase (Fig. 3). Disturbance by tree-falls effects a switch from tall forest to Chusquea, and although episodes of bamboo dieback are assumed to provide the main opportunities for reestablishment of tall forest, this reverse switch may be probabilistic rather than deterministic, depending on stochastic variation in production of viable seed by bamboos and trees. The switch back to tall forest could also be facilitated by encroachment of neighbouring canopy tree crowns, reducing light levels and hence depressing the vigour of bamboos.

ACKNOWLEDGMENTS

 

This work was funded by FONDECYT grants 1980084 and 1000367.

REFERENCES

Canham, C.D., J.S. Denslow, W.J. Platt, J.R. Runkle, T.A. Spies & P.S. White. 1990. Light regimes beneath closed canopies and tree-fall gaps in temperate and tropical forests. Can. J. For. Res. 20: 620-631.

Givnish, T.J. 1988. Adaptation to sun and shade: a whole plant perspective. Austral. J. Plant Physiol. 15: 63-92.

González, M.E. 1999. Tree regeneration responses to mass flowering and death of the bamboo Chusquea quila in south-central Chile. (Masters Thesis) Dept. Geography, University of Colorado, 82 pp.

Hiura, T., J. Sano & Y. Konno. 1996. Age structure and response to fine-scale disturbances of Abies sachalinensis, Picea jezoensis, Picea glehnii, and Betula ermanii growing under the influence of a dwarf bamboo understory in northern Japan. Can. J. For. Res. 26: 289-298.

Hollinger, D.Y. 1987. Photosynthesis and stomatal conductance patterns of two fern species from different forest understoreys. J. Ecol. 75: 925-935.

Lusk, C.H. & O. Contreras. 1999. Foliage area and crown nitrogen turnover in temperate rain forest juvenile trees of differing shade tolerance. J. Ecol. 87: 973-983.

McDonald, D. & D.A. Norton. 1992. Light environments in temperate New Zealand podocarp rainforests. New Zealand J. Bot. 16: 15-22.

Machado, J.L. & P.B. Reich. 1999. Evaluation of several measures of canopy openness as predictors of photosynthetic photon flux density in a forest understorey. Can. J. For. Res. 29: 1438-1444.

Mohammed, G.H. & W.C. Parker. 1999. Photosynthetic acclimation in eastern hemlock [Tsuga canadensis (L.) Carr.] seedlings following transfer of shade-grown seedlings to high light. Oecologia 13: 117-124.

Pickett, S.T.A & P.S. White. 1985. The Ecology of Natural Disturbance and Patch Dynamics. Academic Press, New York.

Schnitzer, S.A., J.W. Dalling & W.P. Carson. 2000. The impact of lianas on tree regeneration in tropical forest canopy gaps: evidence for an alternative pathway of gap-phase regeneration. J. Ecol. 88: 655-666.

Schulze, E.D., F.M. Kelliher, C. Körner & R. Leuning. 1994. Relationships among maximum stomatal conductance, ecosystem surface conductance, carbon assimilation rate and plant nitrogen nutrition: a global ecology scaling exercise. Annu. Rev. Ecol. Syst. 25: 629-660.

Torquebiau, E.F. 1988. Photosynthetically-active radiation environment, patch dynamics and architecture in a tropical rainforest in Sumatra. Austral. J. Plant Physiol. 15: 327-342.

Veblen, T.T. 1982. Growth patterns of Chusquea bamboos in the understorey of Chilean Nothofagus forests and their influences in forest dynamics. Bull. Torr. Bot. Club 109: 474-487.

Veblen, T.T., F.M. Schlegel & B. Escobar. 1980a. Structure and dynamics of old-growth Nothofagus forests in the Valdivian Andes, Chile. J. Ecol. 68: 1-31.

Veblen, T.T., F.M. Schlegel & B. Escobar. 1980b. Dry matter production of two species of bamboo (Chusquea coleou and C. tenuiflora) in south-central Chile. J. Ecol. 68: 397-404.

Veblen, T.T., C. Donoso, T. Kitzberger & A.J. Rebertus. 1996. Ecology of Southern Chilean and Argentinean Nothofagus Forests. In: Veblen, T.T., R.S. Hill & J. Read (Eds.), The Ecology and Biogeography of Nothofagus Forests, pages 293-353. Yale University Press, New Haven.

Welles, J.M. & J.M. Norman. 1991. Instrument for indirect measurement of canopy architecture. Agron. J. 83: 818-825.

Wilson, J.B. & A.D.Q. Agnew. 1992. Positive feedback switches in plant communities. Adv. Ecol. Res. 23: 263-326.