Plant Ecology 139: 259264, 1998. 1998 Kluwer Academic Publishers. Printed in the Netherlands.

259

The signicance of re intensity in creating local patchiness in the Chilean matorral

Departamento de Ecolog a, Ponticia Universidad Cat olica de Chile, Casilla 114-D, Santiago, Chile; Author for correspondence, Present address: Milena Holmgren, Department of Ecology and Evolutionary Biology, University of Utrecht, P.O. Box 80084, 3508 TB Utrecht, the Netherlands; 1 Present address: GEF 1 UN Plaza, NY, NY10017, USA
Received 22 October 1997; accepted in revised form 21 August 1998

Alejandro M. Segura, Milena Holmgren , Juan J. Anabal on & Eduardo R. Fuentes1

Key words: Chilean matorral, Disturbance, Postre, Resprout, Seedling recruitment, Shrublands

Abstract The hypothesis that high and low intensity human-made res can produce ecologically different effects in the Chilean matorral is examined. We compared the abundance of naturally established seedlings under shrubs burned by low and high intensity res on ve north and ve south facing slopes. On south facing slopes, we found 54 shrubs burned by low intensity res and only 4 shrubs burned by high intensity res. In contrast, north facing slopes had approximately the same number of shrubs burned by low and high re intensity res (24 versus 19, respectively). We only found seedlings under shrubs burned by low intensity res and most of them were of Muehlenbeckia hastulata and Trevoa trinervis. Also viable seeds were only found under shrubs burned by low intensity res. Results indicate that re intensity can be an important factor determining species distribution patterns in the matorral. Introduction re in central Chile can be interpreted as strategies to cope with a rather novel evolutionary challenge. Resprouting and seedling establishment are the two basic, although not mutually exclusive, plant responses after res described for Mediterranean ecosystems (Keeley 1977, 1986; Kruger 1983). In central Chile, most shrub species of the matorral vegetation have the capacity to resprout after res (Altieri & Rodriguez 1974; Cody & Mooney 1978; Araya & Avila 1981). The second type of response, namely an enhancement of the germination rate, has only been shown to exist in Chile when tested in the laboratory, but not under eld conditions. For example, seeds of Trevoa trinervis, Muehlenbeckia hastulata, and Colliguaya odorifera, when heated in an oven at 100 C for ve minutes, germinate at higher rates than controls (Muoz & Fuentes 1989). But in eld experiments designed to simulate the effects of high intensity res that consume the shrubs, all seeds within the rst 5 cm of soil, where most of the natural seed bank is located, were killed (Muoz & Fuentes 1989).

Fires in central Chile are currently caused by humans (Araya & Avila 1981) and quite common during the spring and summer seasons (Avila et al. 1988). Unlike other areas with a similar climate around the world (California, southwestern Cape, southwestern Australia, and the Mediterranean Basin), central Chile has no summer lightning, and therefore, it has been hypothesized that here there are no natural re sources (Mooney 1977; Armesto & Gutierrez 1978). Within this perspective, plant postre responses in central Chile have to be interpreted as preadaptations to a new source of disturbance. Nevertheless, it has been argued that volcanism, an unusually frequent phenomenon in Chile, could have been a non-human ignition source during the evolution of the evergreen shrubland vegetation (matorral) and thus a selective pressure on traits favoring postre recovery (Fuentes & Espinoza 1986). From this point of view, the various plant responses to

260 Not all res affecting the matorral though, are intense enough to consume all the aboveground biomass on a slope. Fires usually have locally patchy effects which leave a slope as a mosaic of consumed shrubs mixed with lightly burned ones. In this paper, we test the hypothesis that res of different intensity have ecologically different effects on the postre regeneration of matorral. Whereas high intensity res destroy the soil seed bank, it is conceivable that under lightly burned shrubs there is signicant seed survival and hence the potential for a different species composition during postre recovery. If this hypothesis is correct, this mechanism would facilitate an understanding of species distributional patterns. had been burned about seven and twenty months before the sampling. On each slope, we counted all the seedlings within a 4 m2 plot centered around each burned shrub. A total of 101 shrubs, burned by either low or high intensity res, were sampled. To compare resprouting versus seedling establishment responses after re, we selected other ve slopes burned about seven months prior to the sampling (three north-facing and two south-facing slopes). On each slope, we used two 30 m-long linear transects to estimate the proportion of resprouting shrubs of different species. To estimate the resprouting volume, we measured two perpendicular canopy diameters and the height of each resprouted shrub intersected by the transect. Along the same transects, we counted all the seedlings found in 30 m 2 m plots.

Methods All measurements reported here were done on matorral slopes covering the coastal ranges west of Santiago, in the neighborhood of Lo Vasquez. The general aspect of the matorral in this area is similar to the extensively described Fundo Santa Laura (Mooney 1977), also on the coastal ranges and about 50 km to the north of Lo Vasquez. We found 16 burned slopes, relatively close to each other and with a known re date, and used them for three different purposes. We studied: (1) seed viability under shrubs burned at different re intensities on one slope, (2) abundance of naturally established seedlings under shrubs burned at different re intensities on ten slopes, (3) resprouting versus seedling establishment responses on ve slopes. To estimate the effects of re intensity on seed viability we took soil samples under shrubs burned by low intensity and high intensity res. It was considered to be a low intensity re when only leaves and smaller twigs were burned, and a high intensity re when practically all aboveground biomass was consumed and mainly ashes remained. Note that this denition refers to local effects which means that patches of a same re that burned at different intensities were considered as different res. On one slope, we sampled all of the burned shrubs and took two soil samples (0.4 0.4 0.05 m deep) under the projected canopy of each shrub. Samples were immediately brought to the laboratory where seeds were manually separated and tested for viability with the triphenyltetrazolium test (Roberts 1950; Smith 1951). Seedling abundance was estimated on ten slopes (ve south-facing and ve north-facing slopes) that Results Shrubs burned at different intensities depending on the slope direction. On the ve south-facing slopes, we found 54 shrubs burned by low intensity res and only 4 shrubs burned at high intensities. In contrast, on the ve north-facing slopes, we found 24 shrubs burned at low intensities and 19 shrubs burned at high intensities. No viable seeds were found under shrubs burned by high intensity res (Table 1). Under lightly burned shrubs, the proportion of viable seeds of Lithrea caustica (Anacardiaceae) and Trevoa trinervis (Rhamnaceae) did not differ (X2 = 0.03, p > 0.5), but both had a higher survival rate than the other species (X2 = 73.4, p < 0.001). Also seedling abundance under shrubs burned by low and high intensity res was different. We found a total of 1657 seedlings under 78 lightly burned shrubs and not a single seedling under the 23 severely burned shrubs inspected. The seedling bank under shrubs burned by low intensity res was dominated by Muehlenbeckia hastulata (Polygonaceae) and Trevoa trinervis (Table 2, X2 > 1000, p < 0.001), especially on north facing slopes (Table 2, G = 53.1, p < 0.001). The proportion of resprouting shrubs tended to be positively correlated with the average resprouting volume (Table 3, Pearson r = 0.59, p = 0.12). This means that the species with a larger number of resprouting shrubs tended to be the species with a larger resprouting canopy. Lithrea caustica, Quillaja saponaria (Rosaceae) and Schinus latifolius (Anacardiaceae) are both vigorous and frequent resprouters,

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Table 1. Seed viability under shrubs burned by low and high intensity res on one slope. Data show the number of viable and total seeds (mean s.e.) found within a 0.32 m2 sampling area under each shrub (n = number of shrubs). Low (n = 11) Viable Acacia caven Lithrea caustica Muehlenbeckia hastulata Peumus boldus Quillaja saponaria Trevoa trinervis Total 0 0.09 0.09 0 0 0 9.91 9.31 10 9.30 High (n = 3) Viable Total 0 0 0 0 0 0 0 0 0 8.67 0.88 0.33 0.33 0 63 27.21 72 26.31

Total 12.55 9.78 0.55 0.25 14.64 4.43 2.55 1.79 0.18 0.18 50.18 21.10 80.64 22.51

Table 2. Number of seedlings (mean s.e.) within a 4 m2 sampling area under shrubs burned by low intensity res on ve south and ve north facing slopes (n = number of shrubs). South-facing n = 54 Baccharis linearis Cryptocarya alba Lithrea caustica Maytenus boaria Muehlenbeckia hastulata Podanthus mitiqui Schinus latifolius Trevoa trinervis Total 0.06 0.03 0.13 0.1 0.04 0.03 0 2.89 0.66 0.06 0.04 0 5.83 1.71 9 2.09 North-facing n = 24 0 0 0.04 0.04 0.13 0.13 25.75 11.61 0 0.04 0.04 23 8.58 48.96 14.92

Table 3. Resprouting and seedling establishment postre responses. Shrub data show the proportion of resprouting shrubs and the canopy volume produced per shrub (mean s.e.). The number of seedlings (mean s.e.) comes from ten 60 m2 sampling plots in the same sites where shrubs were sampled. Shrubs Shrub numbers Azara dentata Cryptocarya alba Lithrea caustica Muehlenbeckia hastulata Peumus boldus Quillaja saponaria Schinus latifolius Trevoa trinervis 3 2 77 6 18 2 17 Seedlings Resprouting proportion 1 0.5 0.53 0.33 0.67 1 0.47 Resprouted foliage (m3 ) 0.115 0.057 0.001 0.001 0.363 0.082 0.002 0.002 0.186 0.109 0.376 0.155 0.019 0.016 0 0 0.2 0.13 53.1 28.33 0 0 0.1 0.1 124.4 23.03

262 whereas Peumus boldus (Monimiaceae) and Trevoa trinervis resprouted less frequently and with less vigor. The relative frequency with which different species resprouted was not signicantly correlated with the number of seedlings they produced (Table 3, Pearson r = 0.39, p = 0.33). However, species such as Trevoa trinervis and Muehlenbeckia hastulata, that produced the largest number of seedlings under lightly burned shrubs, tended to have a low frequency of resprouting. In contrast, species such as Quillaja saponaria, Schinus latifolius and Azara dentata (Flacourtiaceae) which had high resprouting rates tended to have negligible, if any, capacity to produce seedlings after the res (Table 3). between species, both in the proportion of individuals that exhibit the response and in the amount of foliage they produce (see also Araya & Avila 1981; Muoz & Fuentes 1989). Both quantities tend to be positively associated in the eld. In addition, seedling establishment under lightly burned shrubs differs between species. The species that undoubtedly show the strongest response here are Trevoa trinervis and Muehlenbeckia hastulata, two of the species that Muoz & Fuentes (1989) earlier reported as being stimulated by a short heat treatment in the laboratory. These were also the species they most frequently found under the projected canopy of the shrubs that they examined. Because they did not distinguish between high and low intensity res, and because of the high frequency with which they also found these same two species under the projected crowns of shrubs that had been cut and not burned, they thought the pattern was due to postre recolonization or to a general germinating response related to the removal of the canopy and exposure to sunlight. The present results cannot exclude this latter canopy removal effect, but suggest an additional effect related to the tolerance of the seed banks to re or, more accordingly with the results by Muoz & Fuentes (1989), at least a small enhancement in their establishment rates. Muehlenbeckia hastulata and Trevoa trinervis show relatively strong seed survival and germination responses to re that other species do not share. Concomitantly, these two species tend to have weak resprouting responses. In all the sites examined, we did not nd resprouting Muehlenbeckia hastulata, and less than 50% of the Trevoa trinervis had resprouted. Araya & Avila (1981) found resprouting Muehlenbeckia hastulata in Cuesta Barriga, a few kilometers further south of our sites in Lo Vasquez, where Muehlenbeckia hastulata is very abundant. But also there, Muehlenbeckia hastulata resprouted weakly compared with other matorral species such as Lithrea caustica, Trevoa trinervis, Acacia caven, Cryptocarya alba, Kageneckia oblonga and Quillaja saponaria. Their data also suggest that colonizing species such as Baccharis linearis and Colliguaya odorifera are weak resprouters, very comparable to Muehlenbeckia hastulata. This dichotomy is suggestive of the evolutionary strategies that Keeley (1977, 1986) and Kruger (1983) postulated for shrubs of the California chaparral, the Australian kwonga, and the fynbos of the Western Cape area. They distinguished between resprouters, seeders and facultative resprouters. Whereas re-

Discussion Our results show that re intensity effects can be very local. The proportion of shrubs burned to ashes was much smaller on south (polar) facing than on north (equatorial) facing slopes, indicating that re reached there lower intensities. This is probably a consequence of the moister conditions that usually prevail on south facing slopes. South facing slopes are exposed to less solar radiation and have a larger shrub cover (Fuentes et al. 1984) than north facing slopes. As a consequence of this, air temperature will tend to be lower, relative humidity higher, and the wood and litter will stay moister, and therefore, tend to burn less intensively than the material on north facing slopes. On a given slope, shrubs also burned at different intensities. This variation within a slope could result from changes in wind, topography and species ammability (see Whelan 1995). Although human use of the landscape (e.g., through an effect on fuel accumulation and distribution) and timing of deliberate ignition can play an important role in explaining variations of re intensity, we believe that in our case the observed local differences in re intensity within and between slopes were likely produced by a combination of ecological factors. Our results suggest that these variations in re intensity have an important role in determining the fate of the stand after a re. In support of previous results by Muoz & Fuentes (1989), these ndings indicate that high intensity res tend to destroy the seed bank and thus eliminate the possibility of recolonization by this mechanism. In such cases, resprouting allows the maintenance of previously colonized space. Our evidence suggests that this resprouting capacity differs

263 sprouters are resilient to res only by resprouting and seedling establishment occurs in disturbance-free conditions, seeders require re to germinate and establish. Facultative resprouters have the capacity to resprout after res and to recruit seedlings in the postre environment. They are, in a way, the sum of the other two, more extreme strategies. Increasing re intensity tends to decrease seedling production of facultative resprouters and increase the one of seeders (Moreno & Oechel 1991). Recently, Keeley (1995) focused on the germination patterns to distinguish between plant life histories that could have evolved in response to periodic res, arguing that resprouting is a widespread trait in plants that, probably, has been present as a preadaptation to surviving res. He distinguished between disturbance-free recruitment, and disturbance-dependent recruitment with two modes: immediate postre showed by those species that restrict seedling recruitment to a short time immediately after re, and later postre showed by species that do not recruit seedlings immediately after re but potentially exploit the postre conditions for seedling establishment either because they resprout and ower in the rst year after re or because they disperse into the burned areas. How do these categories apply to central Chile? The re resilience exhibited by matorral shrubs seems to be different from what has been documented elsewhere. All shrub species currently present seem capable of resprouting from root crowns or lignotubers (Montenegro et al. 1983) and all of them, including weak and strong resprouters, have the capacity to establish seedlings in the absence of res (Fuentes et al. 1984, 1986, 1989), but some species, such as Trevoa trinervis and Muehlenbeckia hastulata, tolerate and are perhaps even stimulated to germinate and establish seedlings after low intensity res. Increasing re intensity decreases seed survival of all species. This is not a strategy that can be easily and uniquely associated with the volcanism-related re history of the matorral, at least until we have an understanding of how the patchiness in burning intensity is produced and of its relative frequency. Arroyo et al. (1995) hypothesized that many sclerophyllous elements of the central Chilean ora evolved directly in situ from ancient temperate rain forest and that perhaps some more drought tolerant species evolved at the present location of the Atacama Desert and migrated south to the present mediterranean region. This view regards re as a recent perturbation in the landscape which has not played a major role in the evolution of special life-history traits of the matorral species. Notwithstanding our lack of understanding of the evolutionary signicance of the responses to high and low intensity res, the evidence is consistent with the hypothesis that res are capable of modifying the composition of the matorral. Fires that consume all shrubs favor vigorous resprouters, with large lignotubers such as Lithrea caustica, Quillaja saponaria, Schinus latifolius, and Azara dentata (Montenegro et al. 1983). These species would tend to persist in the area so long as res are of the high intensity type. However, if the slope is affected by patchy burning intensities, there would be an additional germinating response by Trevoa trinervis and Muehlenbeckia hastulata. In addition to Muehlenbeckia hastulata and Trevoa trinervis, it is likely that Colliguaya odorifera, a species that in the laboratory behaves similarly to the other two, is also able to establish seedlings after low intensity res. In summary, this germination response could contribute to a temporary increase in shrub species diversity at the slope level if the burning intensity is patchy: at high intensity spots only vigorous resprouters would dominate while at low intensity patches, new species could be able to get established.

Acknowledgments We thank R. Fernndez, V. Lobos and H. Haltenhoff for providing us access and logistic help in the eld. M. McDonwell and M. Muoz gave us many suggestions on how to improve the manuscript. This research was funded by the FONDECYT Grant No. 6141989 to E. R. Fuentes and a doctoral support from the Andrew W. Mellon Foundation to A. M. Segura.

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