BlOTROPlCA 34(2): 319-322 2002

NOTES

Growth and Mortality Rates of the Liana Machaerium cuspidaturn in Relation to Light and Topographic Position’

KT word: seedlings; tropical rain firest; Yauni National Park, Amazonian Enrador.

death rate; lianaz; light intensiq; Machaerium cuspidatum (Fabaceae); rekztive growth rate;

LIANAS, OR WOODY VINES, CONTRIBUTE SUBSTANTIALLY to the total species richness in tropical rain forests (Gentry 1991, Appanah et al. 1993, Nabe-Nielsen 2001). They are important ecologically as a food source for forest animals (Emmons & Gentry 1983, Gentry 1985) and may influence forest dynamics by slowing tree growth (Featherly 1941, Clark & Clark 1990) or increasing treefall size by binding trees together (Pun 1984, Vidal et al. 1997). Lianas rely on their host trees for support and therefore do not require the heavy investments in supporting tissues that trees make (Darwin 1867, Castellanos et al. 1991). Lianas are generally found at high densities in gaps and along forest edges. Experimental studies have demonstrated increased liana growth rates in high-light environments (Baars & Kelly 1996) and they are often characterized as light demanding (Caball6 1984, Putz 1984, Hegarty & Clifford 1991).

In this paper, I present data on how variations in canopy openness and topographic position affect seedling growth and mortality for the canopy liana Machaeriurn cuspidaturn Kuhlm. & Hoehne (Faba- ceae). Growth rates of outplanted seedlings were compared to growth rates of seedlings and larger indi- viduals in the forest. The species has its center of distribution in lowland Ecuador and Colombia. Machaeriurn cuspidaturn is the most abundant liana species in the study area. It constitutes ca 11 percent of all liana individuals 1.0 cm DBH (diameter at breast height) or greater in both terra firme (non- inundated) areas and floodplains (R Burnham, pers. comm.). Preliminary surveys have shown that M. cuspidaturn seedlings are rare in floodplain areas (they constitute 6% of the total population of M. cuspidaturn on the floodplain) in comparison to bottomlands (where they constitute 22%) and hill areas (43%; J. Nabe-Nielsen, pers. obs.). This study addressed whether or not the population of large individ- uals in floodplains is maintained by faster growth of fewer surviving seedlings relative to terra firme forest.

The study was carried out in Yasuni National Park in Amazonian Ecuador near Estaci6n Cientifica Yasuni (OO040’S, 76”23’W), from October 1998 to February 2000. The forest is an old-growth tropical forest with few signs of disturbance except along roads. The area receives ca 3000 mm of rain per year (Ef: Nabe-Nielsen 200 1).

I measured growth and mortality rates of M. cuspidaturn seedlings in a total of 30 circular 1 m2 plots distributed equally on hilltop, bottomland, and floodplain areas. The hilltop plots were located on well- drained has; the bottomland plots were located in the flat terra firme areas between the hills; and the floodplain plots were located by N o Tiputini, the major river in the area. The degree of canopy openness was measured at the beginning and at the end of the experiment using Crown Illumination Ellipses (CIE; see description in Brown eta(. 2000), and the average of the two values was used in the analyses. CIE index values are scored on a scale from 1 to 5 by measuring the size of the holes between tree crowns using a series of ellipses drawn on a transparent board. Higher index values are scored in areas with a more open canopy. For each topographic position, five of the plots were selected in high-light environments and five were selected in low-light environments. The high-light plots were selected under trees with sparse foliage in areas receiving CIE values of 2.0 or 2.5. The low-light plots were selected in areas with CIE values equal to 1.0 under trees with dense foliage.

Thirty seedlings (individuals 1 3 0 cm high) were collected from shady understory conditions (CIE 5 1.5) under each of six parent plants in terra firme areas. The seedlings were selected haphazardly. One seedling from each of the parent plants was planted in each plot. The height of the seedlings was measured in October 1998, December 1998, and February 2000. The diameter was measured 2.0 cm above the ground in the first and the last census using metal calipers (precision: 0.05 mm). Seedlings dying within the first ten days after planting were excluded from all analyses. The growth rates of the outplanted

Received 10 May 2000; revision accepted 12 April 2001.

319

320 Nabe-Nielsen

a

1 .o,

b

0.3 0.~1 A

f P f

canopy Openness

-.-P Bottomland

-0.3 1 .O 1.5 2.0 2.5 3.0

canopy openness

FIGURE 1. (a) Mucbum'um cwpihrurn seedling mortality as a function of canopy openness. Canopy openness was measured with the CIE index (see text). The lines were fitted using a logistic regression with topographic position as a covariate. Each point indicates the average mortality of the seedlings in one plot. Some points have been moved slightly to ensure that they are all visible. (b) Relative growth rate as a function of canopy openness. Lines were fitted using linear regression. Topographic position was included as a covariate.

seedlings were compared to growth rates of all M. cwpiliaturn individuals from ten 20 x 250 m forest transects. Individuals 10 mm or less in diameter were only included from the central 10 x 250 m, and asexually produced plants (plants with visible remains of a branch that had connected them to their parent plant) were excluded. The transects were separated by a distance of at least 200 m. Eight transects were placed in terra firme and two were placed in floodplain areas. The height and diameter increment and canopy openness were measured over the same period for both plants in the transects and outplanted seedlings. Relative height growth rates ( R G h d and diameter growth rates (RG&iJ were calculated as the slope of the regressions of loglo(height) on time and loglo(diameter) on time, respectively. R G k g and R G b , were normally distributed (approximately) after being transformed logl~(lOOO * RGR + 1). Absolute growth rates for non-replanted individuals were calculated as the total length or diameter increment divided by the period between the censuses. Mortality as a function of CIE was analyzed using nominal logistic regressions, and growth rates as a function of CIE were analyzed using ANCOVA (analysis of covariance). Topographic position was used as a covariate in both kinds of analyses. All analyses were done with JMP for Macintosh (SAS 1994).

Over 15 months, 49 of the 180 outplanted M. cuspiliaturn seedlings died. Seedling mortality increased with canopy openness when differences among topographic positions were not taken into account (Fig. la; 2 = 12.79, df = 1, P < 0.001; logistic regression). Mortality was higher for floodplains than bottomlands, and was higher for floodplains and bottomlands than hilltops w = 44.73, df = 2, P < 0.0001). The model that included topographic position predicted seedling death correctly 42 percent of the time. When the hilltop plots were considered separately, mortality was not related to canopy openness w = 0.19, df = 1, P = 0.66).

The R G k g also increased with canopy openness (Fig. 1b; 41,1211 = 62.5, P < 0.0001; ANCOVA); it was generally higher on hilltops than bottomlands and even lower on the floodplains (&, 1211 = 3.4, P = 0.04). The slopes of the lines were not significantly different (P = 0.42; interaction in ANCOVA). Variations in canopy openness explained more of the variation in R G k g (30.7%; added @) than did differences in topographic position (3.8%). This trend was the same in both periods, but the RGkS was higher in all habitats during the second period (41,2901 = 125.3, P < 0.0001; ANCOVA). R G k g did not vary among seedlings from different parent plants. The variation in R G b , was partly explained by R G k g (41, 1231 = 48.6, P < 0.0001, 'L 0.28), but after removing the effect of RGkg, the diameter still increased more in areas with higher canopy openness (10%) and in more well-drained areas (additional 8%).

The largest of the non-replanted individuals had the highest absolute growth rate, whereas average

Notes 321

TABLE 1. Diameter and height growth per year f i r individualr of Machaerium cuspidatum growing in ten 0.5 ha transects in terra firme and jbodplain firest. Plants of clonal origin were not measured, and the height was not measured f i r individualr with a diameter greater than I0 mm as t h q were o$en vety long. SD is the standard deviation of the observations.

Size c h s

Height Diameter A height (cm/yr) A diameter (mm/yr)

h a ) (mm) N 2 SD Max f SD Max

530 290 3.2 7.5 85 0.3 0.4 1.7 >30-5100 198 7.8 21.4 144 0.3 0.5 2.1

>loo 510 71 2.4 76.5 178 0.1 0.3 1.4 >10-530 147 0.5 1.2 7.3 > 30-5 50 102 1.4 2.0 9.3 >50-5 100 46 0.7 2.1 5.7

growth varied less among plants in different size classes (Table 1). Nearly all the seedlings that had not been replanted were growing under shady understory conditions, and their R G h d did not differ from that of seedlings planted in low-light conditions ( F I ~ , 3541 = 1.1, P = 0.30; one-way ANOVA). In contrast to the RGRhgfs of outplanted seedlings, the R G h d of non-replanted seedlings did not appear to be affected by topographic position. The RGRhgf was lower for seedlings than for slightly larger plants, and it increased with increasing canopy openness. Very little of the variation in RG% was explained by variations in canopy openness, plant size class, and topographic position (I? = 0.07, 46, 5431 = 19.0, P < 0.0001; ANCOVA, insignificant interaction terms eliminated) for plants with a diameter of 10 mm or less.

In summary, both seedling growth and seedling mortality increased with canopy openness. Since M. cuspidaturn had low mortality in shady environments, it should be characterized as shade tolerant, even though it grows much faster in areas with an open canopy. A similar result was obtained by Baars and Kelly (1996). The five species of lianas in their study grew faster when exposed to elevated light levels and the most shade-tolerant species had the lowest relative growth rate at high-light intensities. The ability of M. cuspidatum to combine shade tolerance with faster growth in areas with hlgh-light intensities is probably crucial to it being the most successful liana in Yasuni. Furthermore, the ability of M. -pi- datum to tolerate shade may be quite uncommon among lianas. Pefialosa (1984) found liana seedlings only in gaps, and even though liana seedlings can occur in shady environments (Chalmers & Turner 1994), th is does not necessarily indicate that they are able to survive in shade.

Results of relatively small, short-term studies like the present one should be interpreted with caution. A species’ growth response may change among regions and with variations in the climate. As far as I am aware, the results presented here nevertheless provide the first direct evidence of seedling shade tolerance for a liana species.

The non-replanted individuals with the highest growth rates were always growing under high-light conditions, but only a small fraction of the plants in 111 sunlight were growing rapidly. The average growth rate of non-replanted seedlings was apparently not affected by topographic position. The reason was presumably that the only seedlings remaining on the floodplains were the ones growing in particularly favorable, well-drained places. The individuals with a diameter of 30 to 50 mm had mean diameter growth rates similar to the liana species studied by Pun. (1990) in Panama (1.4 mm/yr), even though only sun-exposed individuals were included in his study.

Mortality of the outplanted seedlings was much higher on the floodplains than on the terra firme sites, probably because of an inability to withstand inundation. This may also be the reason for the low seedling density in floodplain areas. Although it is impossible to infer long-term population dynamics based on a short-term study like the present one, the results of this study do not support the hypothesis that floodplain populations are maintained by faster growth of fewer surviving seedlings relative to terra firme forest. If individuals are more long-lived in the floodplains, this may offer an alternative explanation for the high floodplain population density. Individual longevity could result from the host trees being more long-lived on floodplains. As M. curpidatum is able to produce independent ramets when it re-

322 Nabe-Nielsen

roots after falling down together with its host tree (Nabe-Nielsen 2000), a higher treefall rate in flood- plains could also lead to a high population density.

I thank Finn Borchsenius and Neil Gale for helping me improve the manuscript, Charlotte Skov and Elisabeth A. Fischer for assistance with the fieldwork, the people at Universidad Cat6lica del Ecuador for logistic support and permission to work at Estaci6n Cientifica Yasuni, and INEFAN for granting the research permits. The work was supported by CTB (grant no. 11-0390, Danish Natural Research Coun- cil) and the European Science Foundation (TCR grant).

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Jacob Nabe-Nlelsen Department of Systematic Botany Institute of Biological Sciences University of Aarhus Universitetsparken building 137 DK-8000 Aarhus C, Denmark

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