Journal of Arid Environments 75 (2011) 1e6

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Plant Area Index and microclimate underneath shrub species from a Chilean semiarid community Y. Tracol a, d, *, J.R. Gutiérrez a, b, c, F.A. Squeo a, b, c a

Center for Advanced Studies in Arid Zones (CEAZA), Terrestrial biology, Casilla 599, La Serena, Chile Departamento de Biología, Facultad de Ciencias, Universidad de La Serena, Casilla 599, La Serena, Chile c Institute of Ecology and Biodiversity (IEB), Santiago, Chile d Centre de Recherches sur les Ecosystèmes d’Altitude, Chamonix Mont-Blanc, France b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 6 March 2007 Received in revised form 23 February 2010 Accepted 6 August 2010

In drylands, environmental conditions under shrub canopy differ from those found in open sites. We should expect that microclimate conditions under shrubs with distinct canopy architecture should also be different. Plant Area Index (PAI) of the three most abundant shrubs species (Porlieria chilensis, Adesmia bedwellii and Proustia cuneifolia) in Bosque Fray Jorge National Park, north-central Chile was measured using a Plant Canopy Analyzer. During two years (2004e2005), we recorded the Relative Humidity and Air Temperature underneath and away from the canopy of the shrubs. The three shrub species showed significant differences in PAI. Microclimate at 30 cm and 2 m above the soil in the open conditions were drier and warmer than underneath shrub canopies. Vegetation patches generate moderate microclimate conditions. Canopy structure can buffer climatic variability, contributing to high herbaceous productivity as well as shrub recruitment. Reflecting shrub architecture and observed PAI values, the lowest microclimate variations were observed under the canopies of P. chilensis, followed by P. cuneifolia and finally A. bedwellii. We bring a novel approach quantifying the Plant Area Index instead of the Plant cover and using a low cost method that integrates the distribution of leaves and may be derived from remote sensing products. Ó 2010 Elsevier Ltd. All rights reserved.

Keywords: Desertification Native species Nurse effect

1. Introduction Shrubs in arid and semiarid lands have been considered as “fertile islands” or “nurse plants” because they improve the herbaceous development and seedling emergence under their canopies (Gutiérrez et al., 1993a). Soil under shrub canopies has a crucial role concerning microorganism functioning and nutrient turnover depending on the shade effect resulting of the light canopy interception (Tiedemann and Klemmendson, 1973; Del Pozo et al., 1989). Particularly in dry areas, processes structuring diversity and interactions shift from competition to facilitation depending on water and nutrient availability (Holmgren et al., 1997). According to Holmgren et al. (1997), facilitation occurs when benefits of available water exceeds the costs of light limitation.

Abbreviations: PAI, Plant Area Index; RH, Relative air Humidity; T, air Temperature. * Corresponding author. Center for Advanced Studies in Arid Zones (CEAZA), Terrestrial biology, Casilla 599, La Serena, Chile. Tel.: þ56 51 334856/33 (0)4 50 53 45 16; fax: þ56 51 334741. E-mail address: [email protected] (Y. Tracol). 0140-1963/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jaridenv.2010.08.002

Numerous studies have highlighted the role of positive plant interactions in all biomes (Garcia-Moya and McKell, 1970; Bertness and Callaway, 1994; Callaway, 1995; Brooker and Callaghan, 1998; Callaway et al., 2002). These authors hypothesized that availability of soil resources, protection against grazing, and microclimate may explain this pattern and facilitate the growth of understory plants. Nevertheless, shading from shrub canopy in arid systems may limit the physiological response of associated annuals and cacti below (Franco and Nobel, 1989; Holmgren et al., 1997; Forseth et al., 2001). In North American (Chihuahuan, Mojave and Sonoran), Australian, and Chilean deserts the absence of some annual plant species or decrease of physiological processes under shrubs can be explained by their intolerance to shade (Jaksic and Montenegro, 1979; Franco and Nobel, 1989; Gutiérrez et al., 1993a; Forseth et al., 2001). According to Polis (1993), the spatial heterogeneity of landscape is due in part to different shrub composition in vegetation patches. Our aim is to analyze the relationships between canopy characteristics and microclimate under shrubs in semiarid northern Chile to clarify conditions associated with patterns of plant species richness and biomass distribution.

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Tools used in this study mixed simultaneously two approaches to quantify the microclimate conditions under and outside the shrub with HOBO data logger and the shade amount derived from Plant Area Index (and Sky visible fraction) measured by a Plant Canopy Analyzer. The Plant Area Index (PAI, m2 m2) corresponds to the one-sided plant area per ground area or the sum of Stem and Leaf Area Indices (SAI and LAI, respectively) as a function of total ground area. Due to the strong influence of the vegetation on climate (Bonan, 1993; Chase et al., 1996), ecosystem functioning (Tracol et al., 2006), radiative transfer balance (Bégué, 1993), and hydrological models, the PAI and more specifically the LAI represents an accurate parameter to approximate vegetative productivity, the gas surface exchange (transpiration), the solar radiation absorption surface, and interception surface of precipitations. The PAI has two additional important advantages: it is a non-destructive method (tested in arid ecosystem: White et al., 2000) and it is a large-scale index readily monitored by remote sensing (Baret and Guyot, 1991; Bégué, 1993; White et al., 2000; Huete et al., 2002). Due to the high proportion of bare soil and the scale of study of the Chilean semiarid zones, the field measurements of shrubs are necessary to complement (and ground truth) results from remote sensing (White et al., 2000). 2. Materials and methods 2.1. Study sites Bosque Fray Jorge National Park (9959 ha), a World Biosphere Reserve, is located right on the coast in the north-central Chilean semiarid zone (30 380 S, 71400 W, 85 km south of La Serena and 385 km north of Santiago). It is a transitional zone between the central Mediterranean region and the hyperarid Atacama Desert to the north. Our field study was carried out in an interior valley, “Quebrada Las Vacas” (230 m elevation). Mean annual rainfall is 145.4  31.3 mm (1 SE) (1989e2002, Fray Jorge weather station) with 90% falling during the cold months (MayeSeptember). However, periodic El Niño Southern Oscillation (ENSO) events cause strong inter-annual variation (e.g., rainy El Niño years, 1991, 229 mm; 1992, 233 mm; 1997, 434 mm; 2000, 244 mm and 2002, 337 mm, vs. dry La Niña year, 1998, 2.2 mm). The maximum daily temperature is 24  C in summer and the minimum daily temperature is 4  C in winter. Fog and coastal breezes strongly influence plants by contributing water, particularly during the dry season. Conditioned by climate, the plant community is characterized by spiny drought-deciduous (sclerophyllous) and evergreen shrubs 2e3 m in height, with an herbaceous understory and low vegetated sandy areas. Major species of shrub layer include Porlieria chilensis (Zygophyllaceae), Proustia cuneifolia (Asteraceae) and Adesmia bedwellii (Papilionaceae) which form the characteristic vegetation pattern of the “matorral.” The shrub species richness and cover has remained relatively constant for the last 50 years, about 60% (Gutiérrez et al., 1993b, 1997). The herbaceous layer corresponds mainly to an ephemeral community, with annuals (e.g. Plantago hispidula, Camissonia dentata, Viola pusilla, Eryngium coquimbanum, Lastarriaea chilensis, Calandrinia sp.), geophytes (Alstroemeria sierrae, Leucocoryne purpurea, Rhodophiala phycelloides), and a suffruticose perennial species, Chenopodium petiolare. Herbaceous cover has changed dramatically according the climate variability (Gutiérrez et al., 1997, 2004). A complete account of plant species composition and abundance at the site is supplied in Gutiérrez et al. (1993b, 2004).

Analyzer integrating radiation transmittance through the canopy from 0.32 to 0.49 mm at five different view zenith angles (0e7, 16e28 , 32e43 , 47e58 , and 61e74 ) (more details in Li-Cor, 1990; Welles and Norman, 1991). It is a hand-held instrument, whose optical sensor includes a fisheye lens (combined focal length: 8 mm) and five silicon detectors allowing simultaneous measurements of the radiation coming from the sky. PAI was measured at two spatial scales every month along four 75 m line transects (15 m apart) in each of 8 study plots (75 m  75 m). On each transect, we recorded at the beginning one reading at 2 m above ground (and above the plant canopy) and 8 readings at 30 cm above the ground and spaced 10 m along it. To minimize the influence of canopy gaps (and resulting PAI underestimation) we used a 45 view cap (Li-Cor, 1990). Thus, monthly PAI for each plot was based on 32 readings beneath and 4 readings above canopies. We also measured PAI seasonally (spring, summer, autumn and winter) under 8 focal individuals of each of the three dominant shrub species (e.g., one randomly selected individual of each species per plot). For each shrub, we recorded PAI by 4 readings beneath the canopy and oriented in the four cardinal directions with a 90 view cap. We designate the PAI values as PAIpc, PAIpcu and PAIab for P. chilensis, P. cuneifolia, and A. bedwellii, respectively. Following recommendations by Li-Cor (1990), measurements were performed before sunrise, when the proportion of diffuse radiation was high, and the canopy around the sensor was shaded from direct solar radiation by placing the operator between the sensor and the sun. A view cap was used for obscuring the operator. The relative humidity and air temperature data at 30 cm above soil surface, under and away from canopies were recorded with HOBO H8 Pro Series data loggers (HOBO data loggers, ONSET Computer Corporation) beginning July 2003. Four HOBOs per plot were placed randomly, with three under the crown of the dominant shrubs at half radius from the trunk and one outside the canopy. Each sensor was calibrated and protected from solar radiation and rodents by a plastic cylinder and mesh. Net air temperature (T) and relative humidity (RH) differences were calculated under and outside the shrub’s canopy respectively as RHunder  RHoutside and Tunder  Toutside Environmental data (temperature and relative humidity) were analyzed with a triple within-subject repeated measure ANOVA (GLM procedure) with SPSS software. Between-subject factors were

2.2. Field measurements We monitored the shrub layer with PAI measurements from October 2004 to January 2006 with a Li-Cor LAI-2000 Plant Canopy

Fig. 1. Climatic data, a) rainfall, b) Air temperature and c) Relative Air Humidity (RH) in the “Bosque Fray Jorge National Park” for the 2003e2005 periods (maximum and minimum daily values are presented for b and c).

a

b

75 65 55 45 35 25 15 5 -5

c

d

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00:00 04:00 08:00 12:00 16:00 20:00

00:00

65 55 45 35 25 15 5 -5

Net difference RH (%)

5 4 3 2 1 0 -1 -2 -3 -4 -5 5 4 3 2 1 0 -1 -2 -3 -4 -5

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RH Net difference (%)

Tº Net difference (ºC)

Tº Net difference (ºC)

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04:00 08:00 12:00 16:00 20:00 00:00

Time (hours)

Time (hours)

Fig. 3. Air temperature (continuous line) and Relative Humidity (dotted line) Net Difference between under and outside the canopy of Porlieria chilensis, during a typical day in a) Spring b) Summer, c) Autumn and d) Winter. Net differences were calculated as RHunder  RHoutside and Tunder  Toutside.

similar they differed in their distribution. In 2003, about 70% of the annual rainfall fell in the first event (Fig. 1a). Air Temperature (T) and relative humidity (RH) recorded under canopy at 30 cm above soil surface showed both interannual (T30 cm:F2.24 ¼ 10.04, p < 0.0007; RH30 cm:F2.24 ¼ 21.95, p < 0.0001) and seasonal (T30 cm:F3.125 ¼ 2273.38, p < 0.0001; RH30 cm:F3.125 ¼ 662.13, p < 0.0001) differences (Fig. 1b,c). The climate data showed two contrasting seasons for our study site: summer (maximum water stress) and winter (minimum water stress). There were no significant differences in T and RH, at either 30 cm or 2 m above the soil surface, in open sites. Daily mean T and RH at 30 cm were not different beneath vs. away from shrub canopies. Consequently, the “shade effect” or the influence of canopy on microclimatic conditions as a protective umbrella was tested at midday, when the maximum solar radiation and water stress occur (Fig. 2aec). In general, T was lower under shrub canopies than in open sites for all three shrub species (F3.12 ¼ 6.51; p ¼ 0.0073), and midday RH was higher under than away from canopies (F3.12 ¼ 3.55;

5 3

65

2

55

1

45

0

35

-1

25

-2

15

-3

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-4 -5

-5 00:00

3. Results 3.1. Climate and microclimate data Annual precipitation was 82.8 mm in 2003, 155 mm in 2004 and 92 mm in 2005. Despite annual rainfall for 2003 and 2005 was

RH Net difference (%)

temperature and relative humidity. Within-subject factors were year, season, month. All P values for within-subject analyses were Huynh-Feldt adjusted, a procedure that corrects for deviations in the spherecity assumption of the varianceecovariance matrix (von Ende, 2001).

75

4 Tº Net difference (ºC)

Fig. 2. Difference in air temperature (T) and Relative Humidity (RH) at midday, calculated as RHunder  RHoutside and Tunder  Toutside. In all figures, positive values on the y axis imply higher measurements under canopies. a) Porlieria chilensis, b) Proustia cuneifolia c) Adesmia bedwellii, (respectively, in a, b, c, PAI changes are plotted with red line and dots along the y-right axis e arrows: start of autumn e stars: typical days plotted Fig. 3). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article).

04:00

08:00

12:00

16:00

20:00

00:00

Time (hours) Fig. 4. Air temperature (continuous line) and Relative Humidity (dotted line) Net Differences between under and outside the canopy during a typical day of spring for Porlieria chilensis (black line), Proustia cuneifolia (red line) and Adesmia bedwellii (blue line). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article).

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PAI (m2m-2)

2.5 2.0 1.5 1.0 0.5 0.0

Spring 04 Summer 05 Autumn 05 Winter 05

Spring 05 Summer 06

TIME (Seasons) Fig. 5. Values of seasonal Plant Area Index (PAI) for the three dominant shrubs from spring 2004 to summer 2006. Porlieria chilensis (black triangle), Proustia cuneifolia (white square) and Adesmia bedwellii (black rhombus). Error bars correspond to the standard deviation of PAI (N ¼ 8 shrubs per species).

p ¼ 0.0048) (Fig. 2c). Additionally, differences of T and RH were greatest underneath P. chilensis (Fig. 2a), less under P. cuneifolia (Fig. 2b), and least under A. bedwellii (Fig. 2c). Differences in T and RH between canopy and open sites typically were highest at midday (Fig. 3aed). Microclimate under the canopy starts to differ from open sites with the first sunlight. Typical days of spring and summer show larger differences in microclimate conditions, whereas the opposite is true in winter. In summary, the microclimate underneath canopies is more constant and more humid as a result of lower temperature variation. For all three species, net differences for T and RH during sunny days in spring indicate greater protection of plants growing under the canopy for P. chilensis (evergreen), P. cuneifolia (deciduous) and A. bedwellii (semi-deciduous), respectively (Fig. 4). 3.2. Individual shrub and plot PAI The evergreen shrub, P. chilensis, had the highest average PAI (2.3  0.2 m2 m2) during the study period (Fig. 5). The strictly deciduous P. cuneifolia, had a higher PAI than the semi-deciduous A. bedwellii during spring and summer 2004 and 2005; during autumn and winter 2005, however, PAIpcu and PAIab were similar

(Fig. 5). In 2005, PAIpc, PAIpcu and PAIab declined markedly (25, 32.5, and 33%, respectively) (Fig. 5). The decline in PAI was more marked for the deciduous P. cuneifolia during the autumn season (due to leaf shedding), and least for the evergreen Porlieria. The decrease in PAI was observed for each species regardless of its foliar habit. In spite of the emergence of new leaves (Proustia) and shoot sprouts (all species) in winter 2005, PAI did not increase. PAI for A. bedwellii was close to that for P. cuneifolia after the leaf shedding in summer 2005. The annual mean PAI measured for 2005 (2.34  0.16 m2 m2) was close to PAIpc (Fig. 6). In spite of seasonal climatic variability which controls the shrub phenology (i.e., precipitation, temperature, relative humidity), the Coefficient of Variation of PAI is lower than 6.8%. As for individual shrubs, from the rainy 2004 year, the general PAI trend described a low decrease of about 16.8% during 2005. Only in August 2005 did PAI show an increase probably due to the start of shrub growth (leaves and stems). 4. Discussion and conclusions 4.1. Climate conditions and influences on the shrub dynamic Our results showed no differences in temperature and relative humidity between 2 m and 30 cm above ground in open sites. Neighboring plant cover evidently is not sufficient to change climatic conditions between shrubs up to 2 m high. Despite similar rainfall in 2003 and 2005, the distribution of rain was less variable in 2005, which should be more favorable for the vegetation. The intervening year (2004) with 145 mm annual rainfall was the wettest year of this study and when the highest values of PAI were measured for each species along the plot transects and individual shrubs. The combination of evergreen, deciduous and facultative deciduous species contributed to the low variability in PAI observed from 2004 to 2006 (CV ¼ 6.8%). In spite of these low changes, a decrease about 17e19% of PAI was observed. We attribute this shrub response to the combined action of extreme environmental conditions during summer 2005 and a dramatic decrease of rainfall between 2004 and 2005 (63 mm). Summer 2005 was particularly dry, as a result of high air temperature, low RH, lack of rainfall and high frequency of sunny days. In addition, at the individual scale we documented a similar decrease of PAI between 2004 and 2006 (25e33%). At the plot scale, the August measurements of PAI do not follow this trend, likely due to the start of leaf expansion of P. cuneifolia and other deciduous species. PAI for P. cuneifolia in winter 2005 was slightly but not significantly higher than that in autumn 2005. The comparison of PAI value for deciduous (P. cuneifolia) and facultative deciduous species (A. bedwellii) suggested that PAIab is similar to SAIpc (Stem Area Index) during autumn and winter when leaves have fallen. PAI values close to 2.2e2.3 m2 m2 characterize arid shrublands (Asner et al., 2003). 4.2. Microclimate conditions and associated PAI values

Fig. 6. Average Plant Area Index dynamics for 75  75 m plots in the Bosque Fray Jorge National Park, north-central Chile. Error bars correspond to the standard deviation of PAI (N ¼ 8 plots of 75  75 m).

Mean daily microclimate was not different under vs. away from shrub canopy. However, faced with these arid conditions, shrub canopy supplies shade and thus a natural barrier against the hard external conditions particularly at midday, which corresponds to the maximum daily stress time. Moreover, the canopy cannot buffer non-optimal environmental conditions during autumn when shade is minimal due to lack of leaves of P. cuneifolia, and consequently no different conditions between under and outside the shrub canopy. Decrease of PAIpc should be associated with the extreme 2005 summer and autumn conditions and thus the minimum T and RH differences observed between microclimate underneath and outside canopy of P. chilensis.

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Plant cover, traditionally used to estimate shade, has been replaced here by Plant Area Index. As Padilla and Pugnaire (2006) pointed out, shade leads to reduced soil water evaporation, lower soil and air temperature, and decrease of radiation reaching annual plants; Forseth et al. (2001) documented that shrub cover decreased solar radiation by about 45%. We bring a novel approach to quantifying cover using the Plant Area Index estimated with a low cost method that integrates the distribution of leaves and may be derived from remote sensing products. Facilitation appears to be essential for growth, fitness, and even survival in some plants, with implications for diversity and community dynamics, especially in arid stressed environments (Pugnaire et al., 1996; Padilla et al., 2004). This effect is more common in environments where abiotic factors or herbivory limit plant performances, such as the Chilean semiarid zone (Meserve et al., 2003). The importance of facilitation increases during droughts and illustrates a shift from competition to facilitation (Holmgren et al., 1997). In our study, both climatic variables measured (RH and T) confirm that the microclimate under shrub canopy during dry conditions is distinct from that away from canopies. Air temperature under the shrub is lower than outside the shrub canopy. In contrast, higher moisture conditions are observed underneath shrub canopy. These contrasted conditions under and outside the shrub canopy are concordant with a typical pattern of interaction which result in a strong influence on community structure and dynamics, and is responsible for the presence or absence of particular species, especially in Mediterranean and arid zones (Padilla and Pugnaire, 2006; Gutiérrez et al., 1993a). The most favorable microclimate in our study was that provided by the canopy of P. chilensis, making this the most successful nurse plant at our site (Gutiérrez et al., 1993a) (GómezAparicio et al., 2005). 4.3. Conclusions Niering et al. (1963) demonstrated that associations between plants could be more advantageous than detrimental, and coined the term “nurse plant syndrome”. Research in recent decades has increased our understanding of the tradeoffs between facilitation and competition. For example, Gutiérrez et al. (1993a) documented the consequences of interactions between favorable shrubs (nurse plants) and target (or protégé) plants, as well as correlated biotic and abiotic variables. In spite of numerous experiments about shrub protection and shelter during the last decade few quantitative conclusions have been offered about shading amount and microclimatic conditions relationships (Callaway and Walker, 1997; Callaway et al., 2002; Forseth et al., 2001; Franco and Nobel, 1989; Maestre et al., 2003, 2005; Moro et al., 1997; Pugnaire et al., 1996). In relation with quantitative results about the effect of canopy shade, and of consequent reductions in solar radiation, we recommend efforts to study the impact of light availability from a physiological perspective, which has the ability to characterize and quantify limitations in the efficiency of water use (Forseth et al., 2001). Canopy structure can buffer climatic variability, contributing to high herbaceous productivity as well as shrub recruitment. Reflecting shrub architecture and observed PAI values, the lowest microclimate variations were observed under P. chilensis, followed by P. cuneifolia and finally A. bedwellii. The highest PAI of P. chilensis was concordant with this and illustrates the highest net difference between conditions under vs. away from the canopy, conferring the best protection effect among the three studied species. Such advances allow a better understanding of integrated processes involved in the semiarid shrubland ecosystems and should improve the success rate of restoration management procedures. In addition to suggest the use of native shrub species,

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artificial protection against grazers has to be implemented due to the high palatability of native shrubs. Additional research on nonpalatable species in heavily grazed sites is necessary to identify more potential “nurse” shrubs adapted to a non-protected zone. Acknowledgements This study was supported by grants of the Fondo Nacional de Investigación Científica y Tecnológica (FONDECYT 3060111 and 1030225, and 1070708), and the logistical support of the Corporación Nacional Forestal (CONAF) of Chile, the Center for Advanced Studies in the Arid Zone (CEAZA), and Institute of Ecology and Biodiversity (IEB). JRG thanks the Chilean Basal Financing Project (PFB-23) and the Fundación BBVA grant INTERCAMBIO (BIOCON06/ 105). We thank Douglas Kelt for his comments and review of the English correctness of the manuscript. References Asner, G.P., Scurlock, J.M.O., Hicke, J.A., 2003. Global synthesis of LAI observations: implications for ecological and remote sensing studies. Global Ecology and Biogeography 12, 191e205. Baret, F., Guyot, G., 1991. Potentials and limits of vegetation indices for LAI and APAR assessment. Remote Sensing of Environment 35, 161e173. Bégué, A., 1993. Leaf Area Index, intercepted photosynthetically active radiation, and spectral vegetation indices: sensitivity analysis for regular-clumped canopies. Remote Sensing of Environment 46, 45e59. Bertness, M.D., Callaway, R.M., 1994. Positive interactions in communities. Trends in Ecology and Evolution 5, 191e193. Bonan, G.B., 1993. Importance of leaf area index and forest type when estimating photosynthesis in boreal forests. Remote Sensing of Environment 43, 45e59. Brooker, R.W., Callaghan, T.V., 1998. The balance between positive and negative plant interactions and its relationship to environmental gradients: a model. Oikos 81, 196e207. Callaway, R.M., Brooker, R.W., Choler, P., 2002. Positive interactions among plants increase with stress. Nature 417, 844e848. Callaway, R.M., Walker, L.R., 1997. Competition and facilitation: a synthetic approach to interactions in plant communities. Ecology 78, 1958e1965. Callaway, R.M., 1995. Positive interactions among plants. Botanical Review 61, 306e349. Chase, T.N., Pielke, R.A., Kittel, T.G., Nemani, R., Running, S.W., 1996. Sensivity of a general circulation model to global changes in leaf area index. Journal of Geophysical Research 101, 7393e7408. Del Pozo, A.H., Fuentes, E.R., Hajek, E.R., Molina, J.D., 1989. Zonación microclimática por efecto de los manchones de arbustos en el matorral de Chile central. Revista Chilena de Historia Natural 62, 85e94. Forseth, I.N., Wait, D.A., Casper, B.B., 2001. Shading by shrubs in a desert system reduces the physiological and demographic performance of an associated herbaceous perennial. Journal of Ecology 89, 670e680. Franco, A.C., Nobel, P.S., 1989. Effect of nurse plants on the microhabitat and growth of cacti. Journal of Ecology 77 (n 3), 870e886. Garcia-Moya, E., McKell, C.M., 1970. Contribution of shrubs to nitrogen ecology of desert-wash plant community. Ecology 51, 81e88. Gómez-Aparicio, L., Valladares, F., Zamora, R., Luis Quero, J., 2005. Response of tree seedlings to the abiotic heterogeneity generated by nurse shrubs: an experimental approach at different scales. Ecography 28, 757e768. doi:10.1111/j.2005. 0906-7590.04337.x. Gutiérrez, J.R., Meserve, P.L., Kelt, D.A., 2004. Estructura y dinámica de la vegetación del ecosistema semiárido del Parque Nacional Bosque Fray Jorge entre 1989 y 2002. In: Squeo, F.A., Gutiérrez, J.R., Hernández, I.R. (Eds.), Historia Natural del Parque Nacional Bosque Fray Jorge. Ediciones Universidad de La Serena, La Serena, pp. 115e134. Gutiérrez, J.R., Meserve, P.L., Herrera, S., Contreras, C.L., Jaksic, F.M., 1997. Effects of small mammals and vertebrate predators on vegetation in the Chilean semiarid zone. Oecologia 109, 398e406. Gutiérrez, J.R., Meserve, P.L., Contreras, L.C., Vasquez, H., Jaksic, F.M., 1993a. Spatial distribution of soil nutrients and ephemeral plants underneath and outside the canopy of Porlieria chilensis shrubs (Zygophyllaceae) in arid coastal Chile. Oecologia 95, 347e352. Gutiérrez, J.R., Meserve, P.L., Jaksic, F.M., Contreras, L.C., Herrera, S., Vasquez, H., 1993b. Structure and dynamics of vegetation in a Chilean semiarid thornscrub community. Acta Oecologica 14, 271e285. Holmgren, M., Scheffer, M., Hutson, M.A., 1997. The interplay of facilitation and competition in plant communities. Ecology 78, 1966e1975. Huete, A., Didan, K., Miura, T., Rodriguez, E.P., Gao, X., Ferreira, L.G., 2002. Overview of the radiometric and biophysical performance of the MODIS vegetation indices. Remote Sensing of Environment 83, 195e213. Jaksic, F.M., Montenegro, G., 1979. Resource allocation of Chilean herbs in response to climatic and microclimatic factors. Oecologia 40, 81e89.

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