Journal of Arid Environments 126 (2016) 12e22

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Journal of Arid Environments

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Vegetation of Bosque Fray Jorge National Park and its surrounding matrix in the Coastal Desert of north-central Chile

* Francisco A. Squeo a, b, , Andrea P. Loayza a, Ramiro P. Lopez a, Julio R. Gutierrez a, b a Departamento de Biología, Universidad de La Serena and Instituto de Ecología y Biodiversidad (www.ieb-Chile.cl), Casilla 554, La Serena, Chile b Centro de Estudios Avanzados en Zonas Aridas (www.ceaza.cl), Chile article info abstract

Article history: Within its almost 9000 ha, Bosque Fray Jorge National Park (BFJNP) possesses a natural mosaic of Received 20 February 2015 vegetation formations dominated by thorn scrub (63.3% of the park) and scrub with cacti and other Received in revised form succulents (34.1%); these formations, whose covers are above 40%, are representative of the Coastal 7 October 2015 Desert vegetation. Additionally, BFJNP has 230 ha (2.6%) of a relict fog forest. This unique combination of Accepted 16 October 2015 vegetation formations, partly explains the high plant richness of the park. We discuss the climatic Available online 21 December 2015 and topo-edaphic factors associated with each type of vegetation formation. Compared to BFJNP, the surrounding vegetation matrix shows evidence of changes in both the Keywords: fl Plant diversity dominant vegetation and their plant covers; moreover, it is oristically depauperate relative to the park. Plant community This territory also includes agricultural land and plantations of non-native shrubs, as well as goat herding Land cover and small, inter-dispersed human settlements. Its main land cover types are: scrub (50%), scrub with Relict fog forest succulents (34%), agricultural land (8%), secondary prairies (3.5%), and plantations of non-native shrubs Conservation (1.6%). Approximately 22% of this area presents high levels of anthropization. Additionally, two wind farms (217 wind turbines) have begun operating within the vicinity of BFJNP within the past two years. BFJNP provides more than a mere representative sample of the current vegetation; it constitutes a remnant of the natural vegetation that once dominated the Coastal Desert before European colonization. Whereas the relict fog forest has been historically isolated, the desert vegetation is increasingly losing connectivity outside the park. We discuss the consequences of this isolation in terms of long-term maintenance of biodiversity. We argue that plant communities at BFJNP are the best available model for ecological restoration projects in this region of Chile. © 2015 Elsevier Ltd. All rights reserved.

1. Introduction cartography originally used to delimit the park. BFJNP is divided into two unequal subsections (Fig. 1): the main area (8880 ha, Fray Bosque Fray Jorge National Park (BFJNP) is located on the coast Jorge hereafter) is located to the north of the Limarí River, whereas of the Coquimbo Region, Chile, just south of the Atacama Desert. It the second area (114 ha, Talinay henceforth) is located on the was declared a National Park in 1941 and a World Biosphere hilltop of Cerro Talinay, south of the Limarí River. Reserve in 1977. In 1981, three National Parks (Bosque Fray Jorge, During the late Miocene, BFJNP was completely underwater and Punta del Viento and Talinay) merged to create what is currently presently contains a series of marine terraces that reflect tectonic BFJNP (CONAF, 1998). The official area of BFJNP reported by CONAF blocks of recent geologic origin, and which have sustained torren- (1998) is 9959 ha; however, the most recent spatial data reveals a tial erosion dynamics (Novoa-Jerez et al., 2004a). There are three current size of approximately 8994 ha (CONAF, 2004). This distinct geomorphological units in BFJNP (from west to east): 1) the discrepancy can be attributed to changes in the boundaries of coastal terrace (uplifted during the PlioceneePleistocene); 2) the neighboring human communities and/or from different coastal massif of Altos de Talinay (reaching heights of up to 660 m a.s.l.) and; 3) tilted blocks forming hills and dry ravines that include Quebrada de Las Vacas (formed during the Pliocene). Altos de Talinay started uplifting during the Pliocene and reached its * Corresponding author. Departamento de Biología, Universidad de La Serena, maximum height in the Pleistocene (Paskoff, 1993; Novoa-Jerez Casilla 554, La Serena, Chile. E-mail address: [email protected] (F.A. Squeo). et al., 2004a). A submarine trench of 1000 m is located http://dx.doi.org/10.1016/j.jaridenv.2015.10.013 0140-1963/© 2015 Elsevier Ltd. All rights reserved. F.A. Squeo et al. / Journal of Arid Environments 126 (2016) 12e22 13

Fig. 1. Location of Bosque Fray Jorge National Park (BFJNP). The official boundary is shown as a continuous white line, roads are shows as black (paved) or thin black dashed (dirt or gravel) lines, and the 10 and 3 km buffers around Fray Jorge and Talinay, respectively, are shown as white dashed lines. 14 F.A. Squeo et al. / Journal of Arid Environments 126 (2016) 12e22 approximately 10 km from the coast, and runs parallel to Altos de Cerro Juan Soldado and El Tofo, which are 150 km north of Fray Talinay. Jorge, contain small fog-dependent relict populations of Kageneckia oblonga (Bollen); a small tree that is abundant in the periphery of 2. Origin of the flora of Bosque Fray Jorge National Park relict 0livillo forests at BFJNP and common in the Andes of central Chile. Perturbation regimes in the Pleistocene and Holocene also The woody components of Bosque Fray Jorge originate from affected the genetic diversity of shrub populations. For example, Paleogene flora, which corresponds to tropical lineages with Aus- Colliguaja odorifera populations located in the coastal mountain tralasian links that inhabited the southern portion of the South range have higher genetic diversity than populations in the Andes American continent before the breakup of occidental Gondwana of central Chile, suggesting the former may have been refuges (Bull- ~ (Villagran et al., 2004). Events that occurred at the end of the Ter- Herenu et al., 2005). tiary, such as the glaciation of occidental Antarctica and Patagonia, As a result of the mixing of these distinct floras (e.g., xeric lin- the formation of the Humboldt Current, the final uplift of the eages from the north and more mesic lineages from central and Andes, and the increase in aridity of the Atacama Desert, led to a southern Chile), the Coquimbo Region has the highest plant di- fragmentation and shrinkage of the northern edge of subtropical versity in Chile (Squeo et al., 2012). The xerophytic flora has ele- forests of the Pacific Coast and to the expansion of subtropical ments as old as those in the relict forest; some originated from the sclerophyllous forests of central Chile. These events would have ancient sclerophyllous forest of central Chile, whereas others coincided with the gradual tectonic uplift of Altos de Talinay be- evolved more recently in the Atacama Desert. Examples of some tween 5 and 2 million years ago, and produced a refuge that species with an old tropical origin are found both in the northern allowed the persistence of northern remnants of the subtropical (), and southern (Pouteria splendens) forest. coasts of the Region; both of these species have large fleshy fruits, The humid conditions present during the glacial periods of the recalcitrant seeds and no current legitimate dispersers (Loayza Pleistocene allowed the persistence and some degree of connec- et al., 2014). tivity of the relict forest of Olivillo (Aextoxicon punctatum) along the Based on phylogenies of some genera of , the flora of north-central Chilean coast (Villagran et al., 2004). However, dur- the Atacama Desert appears to have multiple origins, and is ing interglacial periods (including the current one) the increase in phylogenetically related to species in central and southern Chile, aridity heightened the discontinuities of the relict forest. In this the Mediterranean Andes, Patagonia, and the Monte Province of regard, the expansion of the semi-arid scrub and restriction of relict Argentina's Chaco Region (Urtubey et al., 2010). Floristic in- forests to hilltops with permanent fogs would have severed the terchanges between the southern edge of the Atacama Desert and connectivity of this forest to the sclerophyllous forest of central central Chile were possible due to the lack of large biogeographic Chile (Troncoso et al., 1980; Villagran and Armesto, 1980; Villagran barriers (Luebert, 2011). Moreover, palynological data reveals that et al., 2004). This fragmentation process has resulted in genetic central Chile experienced dry periods during the Holocene, which differentiation among the forest remnants. For example, Jara- may have led to the southern expansion of lineages from the Ata- Arancio et al. (2012) found a high degree of leaf morphological cama Desert (Villagran and Varela, 1990; Villa-Martínez and and genetic divergence between Drimys winteri populations in Villagran, 1997). PNBFJ and other Chilean populations. Similarly, there is evidence of high genetic differentiation between A. punctatum populations, 3. Fog as a water source suggesting a long history of restricted genetic exchange (Núnez-~ Avila and Armesto, 2006). Expansion of the arid scrub during the Relict Olivillo forests have been recognized as “fog-forests” for interglacial periods coupled with isolation of relict forest on hill- well over a century (Philippi, 1884; Munoz~ and Pisano, 1947). tops can also explain the presence of other remnants of the pale- Kummerow (1962, 1966) showed that fog condensation could ocommunity in ravines and hilltops of Chile's north-central coast. greatly exceed the water contributed by rainfall (ca. 350 mm), For example, A. punctatum forest relicts are restricted to the hilltop reaching over 1000 mm annually. Moreover, fog intensity is high of Cerro Santa Ines (32100S; 71290O), located in the southern limit during spring and early summer, when water is mostly needed, and of the Coquimbo Region (Francois, 2004). In the opposite direction, low during fall and winter (Cruzat-Gallardo, 2004), when most of

Table 1 Areal coverage for each land cover type at Bosque Fray Jorge National Park (BFJNP) and in the 10 and 3 Km buffers surrounding Fray Jorge and Talinay, respectively (see also Fig. 3). Based on CONAF (2004).

Land cover BFJNP Buffer Total

ha % ha % ha %

Urban and industrial areas 0.0 0.00 10.7 0.02 10.7 0.02 Agricultural land 1.2 0.01 3767.0 7.95 3768.2 6.68 Grassland 0.0 0.00 1648.7 3.48 1648.7 2.92 Scrublandegrassland 0.0 0.00 241.9 0.51 241.9 0.43 Scrubland 5756.4 64.00 23,776.6 50.16 29,533.0 52.37 Scrubland with trees 0.0 0.00 23.1 0.05 23.1 0.04 Scrub with succulents 3066.6 34.10 16,314.3 34.42 19,380.9 34.37 Succulent formation 0.0 0.00 713.9 1.51 713.9 1.27 Shrub plantation 0.0 0.00 750.9 1.58 750.9 1.33 Forest plantation 0.0 0.00 12.1 0.03 12.1 0.02 Native forest 169.0 1.88 0.0 0.00 169.0 0.30 Wetlands 0.0 0.00 69.2 0.15 69.2 0.12 Beaches and dunes 0.0 0.00 9.6 0.02 9.6 0.02 Others lacking vegetation 0.0 0.00 9.5 0.02 9.5 0.02 Rivers 0.6 0.01 54.1 0.11 54.7 0.10 Total 8993.7 100.00 47,401.6 100.00 56,395.4 100.00 F.A. Squeo et al. / Journal of Arid Environments 126 (2016) 12e22 15 the rain falls. located under the canopy (20). Similarly, trees from forest frag- Fog water is intercepted mainly by A. punctatum; hence, this ments located in areas that receive less fog have higher leaf angles, species is considered key in the structuring of the forest in Fray specific leaf mass, and water use efficiency (i.e., higher than d13C) Jorge. Gajardo et al. (1984) point that “the existence of the forest than those in from fragments in more humid areas. These data depends on the presence of the forest” suggesting that the forest suggest that there is a compromise in leaf angle between capturing canopy is fundamental to intercept fog. Additionally, shrub species fog (high angles of exposed leaves) and light (low angles under the located in the exposed front of the forest, such Baccharis vernalis, forest canopy). Ultimately, the water collected by leaves drains to also capture fog and act as nurse for species of the Olivillo the ground where it is taken up by the roots. community (Hernandez and Vita, 2004; Squeo et al., 2004). The amount of fog intercepted by the forest appears to strongly One of the mechanisms that favors the capture of fog by limit plant recruitment, which is evident from forest regeneration A. punctatum appears to be leaf angle. Squeo et al. (2004) demon- being restricted to the front exposed to the fog, whereas the older strated that leaves of A. punctatum from trees located on the leading and dying trees are located in the rear end of the fragments (Squeo edge of the forest (i.e., those that receive greater amounts of fog) et al., 2004). The season with highest vegetation growth coincides have higher angles with respect to the horizon (e.g., 67) than those with higher fog availability in the springesummer and is similar to

Fig. 2. Location relict forests within Bosque Fray Jorge National Park (BFJNP): Fray Jorge (Left) and Talinay (right). The forest fragments are shown in black (photointerpretation at a 1:5000 scale based on a Quick Bird image from April 23rd 2008, pixel resolution: 60 cm). Arrows and shaded polygons show areas with evidence of fire (source: Squeo et al., 2004). 16 F.A. Squeo et al. / Journal of Arid Environments 126 (2016) 12e22

Fig. 3. Land cover types and plant associations in Bosque Fray Jorge National Park (BFJNP) and in buffer zones. Based on CONAF (2004) and Squeo et al. (2003). Numbers refer to the vegetation formations in Table 3. F.A. Squeo et al. / Journal of Arid Environments 126 (2016) 12e22 17 other fog oases of northern Chile and Perú (Squeo et al., 1998, 2004, Encelia canescens e Haplopappus cerberoanus (ID #22; 12.8%) in the 2005), as well as in the coastal redwoods of central California coastal terrace, and Baccharis paniculata e Chenopodium petiolare (Johnstone and Dawson, 2010). Finally, lower survival and recruit- (ID #15; 10.9%) on the western slopes of Altos de Talinay (Fig. 3, ment of trees in BFJNP may occur as a response to lower fog fre- Table 3). Associations of Baccharis vernallis e Haplopappus hirtellus quency, a phenomenon that has been inferred in other coastal fog- (ID #16; 3.8%) and K. oblonga e Ribes punctatum e B. vernalis (ID dependent ecosystems during the last century (e.g., Johnstone and #39; 3.2%) can be found along the forest's periphery, to north and Dawson, 2010). south of the forest, respectively. The most common vegetation in the eastern slope of Altos de Talinay corresponds to a scrub with succulents dominated by Adesmia bedwellii e Proustia cuneifolia e 4. Floristic composition Puya chilensis (ID #53; 16.6%) and to a scrub composed of A. bedwellii e Porlieria chilensis (ID #9; 13.2%) in the lowest part of BFJNP has 440 species of native plants, 266 of which are Quebrada de Las Vacas. On the hills northeast of Quebrada de Las endemic to Chile. These endemics include 10 endangered and 84 Vacas, the dominant formations are scrub with succulents Gutier- vulnerable species (Squeo et al., 2001). The relict forest at BFJNP has rezia resinosa e Ophryosporus paradoxus e Trichocereus skottsbergii a total of 44 species, 29 of which are restricted to the forest (Arancio (ID #61; 10.8%) and A. bedwellii e T. skottsbergii (ID #54; 3.6%), et al., 2004a). There are 17 threatened species, three endangered coupled with scrub composed of P. cuneifolia e A. bedwellii (ID #44; (D. winteri, Lapageria rosea, and Peperomia coquimbensis) and 14 4.9%). vulnerable (Arancio et al., 2004b). This forest is characterized by the The vegetation of the A. bedwellii e Porlieria chilensis scrub at association among A. punctatum, D. winteri, Azara microphylla, Quebrada de Las Vacas (where the LTER Fray Jorge site is located, Myrceugenia correifolia and Rhaphithamnus spinosus. The fragments see Meserve et al., 2016 and Madrigal-Gonzalez et al., 2016) has that make up the forest are located in a narrow strip between 450 been described in detail by Gutierrez et al. (1993a, 2004). The plant and 660 m a.s.l. on the southwest facing slopes (Novoa-Jerez et al., community is characterized by spiny drought-deciduous (scle- 2004b), which are frequently exposed to fog (Squeo et al., 2004). rophyllous) and evergreen shrubs 2e3 m in height, an herbaceous The xerophytic scrub formations, in contrast, contain 400 species understory and low vegetated sandy areas. According to these au- that are distributed in a mosaic of different community types thors, the most common species in the shrub layer include (Squeo et al., 2001). Additionally, the forest's periphery contains 43 A. bedwellii, Porlieria chilensis and P. cuneifolia, which form the species that combine hygrophilous elements (e.g., Gaultheria “matorral”. Shrub species richness and cover has remained rela- mucronata and Gunnera tinctoria) with other elements character- tively constant for the last 50 years, about 55e60% (Gutierrez et al., istic of xerophytic species (e.g., Puya chilensis and Fuchsia lycioides). 1993a, 1997). The herbaceous layer corresponds mainly to an ephemeral community, with annuals (e.g., Plantago hispidula, 5. Vegetation Camissonia dentata, Viola pusilla, Eryngium coquimbanum, Las- tarriaea chilensis, Cistanthe coquimbensis), geophytes (Alstroemeria According to the Vegetation Registry of Coquimbo (CONAF, sierrae, Leucocoryne purpurea, Rhodophiala phycelloides), and a 2004; scale 1:50,000), the main land cover types at BFJNP are suffruticose perennial species (C. petiolare). scrub (64%) and scrub with succulent plants (34%) (Table 1). Ac- A characteristic element of the scrub formations in Fray Jorge is cording to CONAF (2004), the native forest located on the hilltops of Porlieria chilensis. This species plays a key role in arid ecosystems as Altos de Talinay has an area of 169 ha (1.9% of BFJNP); that is, 82 ha it performs hydraulic lift (Munoz~ et al., 2008; Morales et al., 2015), larger than what is reported by Novoa-Jerez et al. (2004b). and provides favorable conditions under its canopy for the estab- To determine the actual extent of the relict forest, we conducted lishment of other plant species (Gutierrez et al., 1993b; Tracol et al., a new and more precise photointerpretation that uses a 1:5000 2011). Density of Porlieria chilensis can reach 200 individuals ha 1. scale. Our results revealed that the forest covers an area of 189 and The population is made up almost entirely of adults, with little 41 ha in Fray Jorge and in Talinay, respectively (Fig. 2). This amounts representation of other age classes. There is very limited recruit- to a total of 230 ha of native forest in BFJNP (2.6% of its area), ment by seed; most of the new recruitment is vegetative (Loayza increasing by 61 ha the area reported in the Vegetation Registry. In et al., 2015). contrast, the scrub cover type in our analysis decreases by 0.7%. To compare the vegetation at BFJNP with that found in neigh- Within the relict forest, water availability determines two basic boring areas, we defined a buffer zone of 10 km around Fray Jorge plant associations: (1) A. punctatum e D. winteri is found in areas of and 3 km around Talinay; distances that correspond to the higher humidity due to persistent fog condensation, whereas (2) approximate width of each of these units. The area of the entire A. punctatum e M. correifolia is found in the drier, northern areas of buffer zone is 47,402 ha, and consists of scrub (50%) and scrub with the forest (Munoz~ and Pisano, 1947), where D. winteri is absent succulents (34%) (Table 1). Squeo et al. (2003) reclassified the (Squeo et al., 2004, 2005). database of the vegetation registry (CONAF, 1999, 2004) using an The dominant plant associations from east to west of Fray Jorge anthropization index based on land cover, and the dominant spe- correspond to the following: Ambrosia chamissonis e Frankenia cies present in a given polygon. A high value of this index is rep- chilensis (Plant association ID #10; 3.8% of BFJNP) along the coast, resented by land cover associated with human use (e.g., agricultural land, shrub plantations) or dominance of exotic or ruderal native species in natural land cover types. Most of BFNP's area (99%) has a Table 2 low anthropization index; conversely, 22% of the buffer zones are Area according to anthropization index for Bosque Fray Jorge National Park (BFJNP) and in the 10 and 3 Km buffers surrounding Fray Jorge and Talinay, respectively (see strongly anthropized (Table 2, Fig. 4). The land cover types that are also Fig. 4). Based on CONAF (2004) and Squeo et al. (2003). highly anthropized are: agricultural lands (8%), which include winter wheat (Triticum aestivum) that depends on winter precipi- Anthropization index BFJNP Buffer Total tation, and olive tree (Olea europea) plantations that have drip ha % ha % ha % irrigation systems; grasslands (3.5%) dominated by Avena barbata, Low 8890.3 98.85 37,207.1 78.49 46,097.4 81.74 Bromus berteroanus, and Pseudognaphalium viravira and; shrub High 103.4 1.15 10,194.6 21.51 10,298.0 18.26 plantations (1.6%, Atriplex nummularia)(Fig. 3, Table 3). Addition- Total 8993.7 100.00 47,401.6 100.00 56,395.4 100.00 ally, G. resinosa is a native, pioneer species that colonizes an area 18 F.A. Squeo et al. / Journal of Arid Environments 126 (2016) 12e22

Table 3 Areal coverage by land cover type and plant association for Bosque Fray Jorge National Park (BFJNP) and in the 10 and 3 Km buffers surrounding Fray Jorge and Talinay, respectively (see also Fig. 3). Based on CONAF (2004) and Squeo et al. (2003).

ID Land cover/plant association BFJNP Buffer Total

ha % ha % ha %

Grassland 0.0 0.00 1648.7 3.48 1648.7 2.92 1 Avena barbata e Bromus berteroanus 0.0 0.00 285.9 0.60 285.9 0.51 2 Bromus berteroanus 0.0 0.00 509.8 1.08 509.8 0.90 3 Pseudognaphalium viravira 0.0 0.00 853.0 1.80 853.0 1.51 Scrubland e Grassland 0.0 0.00 241.9 0.51 241.9 0.43 4 Avena barbata e Gutierrezia resinosa 0.0 0.00 201.2 0.42 201.2 0.36 5 Bromus berteroanus e Baccharis paniculata 0.0 0.00 25.9 0.05 25.9 0.05 6 Bromus berteroanus e Rapistrum rugosum 0.0 0.00 14.8 0.03 14.8 0.03 Scruband 5756.4 64.00 23,776.6 50.16 29,533.0 52.37 7 Acacia caven e Proustia cuneifolia 0.0 0.00 1.206.7 2.55 1206.7 2.14 8 Adesmia bedwellii e Baccharis paniculata 129.1 1.44 16.7 0.04 145.8 0.26 9 Adesmia bedwellii e Porlieria chilensis 1184.5 13.17 644.8 1.36 1829.3 3.24 10 Ambrosia chamissonis e Frankenia chilensis 337.8 3.76 857.4 1.81 1195.2 2.12 11 Baccharis linearis e Adesmia bedwellii 91.5 1.02 51.7 0.11 143.2 0.25 12 Baccharis linearis e Baccharis marginalis 10.1 0.11 142.9 0.30 153.0 0.27 13 Baccharis linearis e Baccharis paniculata 0.0 0.00 96.4 0.20 96.4 0.17 14 Baccharis marginalis e Muehlenbeckia hastulata 0.0 0.00 92.3 0.19 92.3 0.16 15 Baccharis paniculata e Chenopodium petiolare 980.4 10.90 837.5 1.77 1817.9 3.22 16 Baccharis vernalis e Haplopappus hirtellus 342.5 3.81 10.4 0.02 352.9 0.63 17 Chenopodium petiolare 211.1 2.35 155.5 0.33 366.6 0.65 18 Chuquiraga ulicina 0.0 0.00 12.0 0.03 12.0 0.02 19 Cordia decandra e Gutierrezia resinosa 0.0 0.00 135.8 0.29 135.8 0.24 20 Distichlis spicata e Sarcocornia fruticosa 5.7 0.06 24.1 0.05 29.8 0.05 21 Encelia canescens e Cristaria glaucophylla 0.0 0.00 26.4 0.06 26.4 0.05 22 Encelia canescens e Haplopappus cerberoanus 1.153.9 12.83 2281.0 4.81 3434.9 6.09 23 Eupatorium salvia e Ophryosporus paradoxus 0.0 0.00 310.5 0.66 310.5 0.55 24 Eupatorium salvia e Proustia cuneifolia 168.5 1.87 410.8 0.87 579.3 1.03 25 Fabiana viscosa 0.0 0.00 153.0 0.32 153.0 0.27 26 Gutierrezia resinosa e Acacia caven 34.9 0.39 707.7 1.49 742.6 1.32 27 Gutierrezia resinosa e Adesmia microphylla 0.0 0.00 792.7 1.67 792.7 1.41 28 Gutierrezia resinosa e Avena barbata 0.0 0.00 161.3 0.34 161.3 0.29 29 Gutierrezia resinosa e Baccharis paniculata 55.2 0.61 0.0 0.00 55.2 0.10 30 Gutierrezia resinosa e Bromus berterianus 0.0 0.00 39.6 0.08 39.6 0.07 31 Gutierrezia resinosa e Haplopappus cerberoanus 0.0 0.00 2952.6 6.23 2952.6 5.24 32 Gutierrezia resinosa e Proustia cuneifolia 101.6 1.13 2457.0 5.18 2558.6 4.54 33 Haplopappus cerberoanus e Acacia caven 111.3 1.24 147.9 0.31 259.2 0.46 34 Haplopappus cerberoanus e Baccharis paniculata 0.0 0.00 6192.6 13.06 6192.6 10.98 35 Haplopappus cerberoanus e Puya berteroniana 0.0 0.00 336.1 0.71 336.1 0.60 36 Haplopappus foliosus e Heliotropium stenophyllum 0.0 0.00 13.3 0.03 13.3 0.02 37 Heliotropium stenophyllum e Flourensia thurifera 22.9 0.25 0.0 0.00 22.9 0.04 38 Heliotropium stenophyllum e Pleocarphus revolutus 14.9 0.17 193.3 0.41 208.2 0.37 39 Kageneckia oblonga e Ribes punctatum e Baccharis vernalis 283.9 3.16 0.0 0.00 283.9 0.50 40 Ophryosporus paradoxus e Baccharis paniculata 0.0 0.00 75.5 0.16 75.5 0.13 41 Ophryosporus paradoxus e ambrosioides 0.0 0.00 44.4 0.09 44.4 0.08 42 Ophryosporus paradoxus e Junellia selaginoides 0.0 0.00 103.5 0.22 103.5 0.18 43 Pleocarphus revolutus e Gutierrezia resinosa 0.0 0.00 46.2 0.10 46.2 0.08 44 Proustia cuneifolia e Adesmia bedwellii 440.8 4.90 1043.8 2.20 1484.6 2.63 45 Proustia cuneifolia e Baccharis paniculata 0.0 0.00 528.6 1.12 528.6 0.94 46 Proustia cuneifolia e Bahia ambrosioides 75.7 0.84 0.0 0.00 75.7 0.13 47 Senecio murinus e Haplopappus cerberoanus 0.0 0.00 13.0 0.03 13.0 0.02 48 Senecio murinus e Senna cumingii 0.0 0.00 57.2 0.12 57.2 0.10 49 Senna cumingii e Proustia cuneifolia 0.0 0.00 215.0 0.45 215.0 0.38 50 Tessaria absinthioides e Pleocarphus revolutus 0.0 0.00 189.3 0.40 189.3 0.34 Scrubland with trees 0.0 0.00 23.1 0.05 23.1 0.04 51 Acacia caven e Schinus molle 0.0 0.00 0.6 0.00 0.6 0.00 52 Proustia cuneifolia e Gutierrezia resinosa e Acacia caven 0.0 0.00 22.5 0.05 22.5 0.04 Scrubland with succulents 3066.6 34.10 16,314.3 34.42 19,380.9 34.37 53 Adesmia bedwellii e Proustia cuneifolia e Puya chilensis 1492.9 16.60 1619.5 3.42 3112.4 5.52 54 Adesmia bedwellii e Trichocereus skottsbergii 319.4 3.55 992.8 2.09 1312.1 2.33 55 Baccharis marginalis e Puya chilensis 0.0 0.00 672.4 1.42 672.4 1.19 56 Bahia ambrosioides e Haplopappus cerberoanus 0.0 0.00 1029.8 2.17 1029.8 1.83 57 Eulychnia acida e Cordia decandra 0.0 0.00 1753.7 3.70 1753.7 3.11 58 Eulychnia acida e Trichocereus coquimbana 0.0 0.00 21.3 0.04 21.3 0.04 59 Flourensia thurifera e Eulychnia acida 0.0 0.00 4.1 0.01 4.1 0.01 60 Gutierrezia resinosa e Eulychnia acida 0.0 0.00 378.1 0.80 378.1 0.67 61 Gutierrezia resinosa e Ophryosporus paradoxus e Trichocereus skottsbergii 972.0 10.81 2457.2 5.18 3429.1 6.08 62 Gutierrezia resinosa e Proustia cuneifolia e Eulychnia acida 0.0 0.00 874.4 1.84 874.4 1.55 63 Haplopappus cerberoanus e Eulychnia acida 0.0 0.00 536.6 1.13 536.6 0.95 64 Haplopappus foliosus e Austrocylindropuntia miquelii 0.0 0.00 283.7 0.60 283.7 0.50 65 Heliotropium stenophyllum e Proustia cuneifolia e Eulychnia acida 0.0 0.00 32.3 0.07 32.3 0.06 66 Heliotropium stenophyllum e Puya chilensis 0.0 0.00 1058.4 2.23 1058.4 1.88 67 Heliotropium stenophyllum e Senecio adenotrichius 0.0 0.00 63.3 0.13 63.3 0.11 F.A. Squeo et al. / Journal of Arid Environments 126 (2016) 12e22 19

Table 3 (continued )

ID Land cover/plant association BFJNP Buffer Total

ha % ha % ha %

68 Ophryosporus paradoxus e Trichocereus skottsbergii 0.0 0.00 72.2 0.15 72.2 0.13 69 Pleocarphus revolutus e Proustia cuneifolia 0.0 0.00 48.5 0.10 48.5 0.09 70 Proustia cuneifolia e Eulychnia acida 205.8 2.29 2450.3 5.17 2656.1 4.71 71 Proustia cuneifolia e Trichocereus skottsbergii 0.0 0.00 365.3 0.77 365.3 0.65 72 Trichocereus skottsbergii e Eulychnia acida 76.4 0.85 578.1 1.22 654.5 1.16 73 Trichocereus skottsbergii e Gutierrezia resinosa 0.0 0.00 141.2 0.30 141.2 0.25 74 Trichocereus skottsbergii e Heliotropium stenophyllum 0.0 0.00 881.3 1.86 881.3 1.56 Succulent formation 0.0 0.00 713.9 1.51 713.9 1.27 75 Puya chilensis e Trichocereus skottsbergii 0.0 0.00 47.2 0.10 47.2 0.08 76 Trichocereus skottsbergii e Eulychnia acida e Avena barbata 0.0 0.00 666.7 1.41 666.7 1.18 Shrub plantation 0.0 0.00 750.9 1.58 750.9 1.33 77 Atriplex nummularia 0.0 0.00 750.9 1.58 750.9 1.33 Forest plantation 0.0 0.00 17.7 0.04 17.7 0.03 78 Eucalyptus globulus 0.0 0.00 17.7 0.04 17.7 0.03 Native forest 169.0 1.88 0.0 0.00 169.0 0.30 79 Aextoxicon punctatum e Myrceugenia correifolia e Drimys winteri 169.0 1.88 0.0 0.00 169.0 0.30 Wetlands 0.0 0.00 63.6 0.13 63.6 0.11 80 Juncus sp. 0.0 0.00 63.6 0.13 63.6 0.11 Total area 8993.7 100.00 47,401.6 100.00 56,395.4 100.00

that has been cleared for agriculture or by fire, and whose presence establishment of invasive grasses, which affect both plant com- also indicates anthropogenic disturbances. In North American de- munity structure and composition by influencing competitive dy- serts other species of Gutierrezia (e.g., Gutierrezia microcephala, G. namics between native and exotic plant species (Gutierrez et al., sarothrae) are also indicators of overgrazing (Carey, 1994). 2010; Madrigal et al., 2011; Meserve et al., 2016). The main natural vegetation formations in the buffer zones e include scrub associations of H. cerberoanus B. paniculata (ID #34; 7. New impacts: wind farms 13.1%), E. canescens e H. cerberoanus (ID #22; 4.8%), G. resinosa e H. e cerberoanus (ID #31; 6.2%), and G. resinosa P. cuneifolia (ID #32; Two wind farms, El Arrayan and Talinay II, have become oper- e 5.2%), and scrub with succulents P. cuneifolia Eulychnia acida (ID ational in the vicinity of BFJNP within the past two years (Fig. 1). e e #70; 5.2%), G. resinosa O. paradoxus T. skottsbergii (ID #61; 5.2%) The first is located 1 km from the northwest edge of BFJNP e (Table 3, Fig. 3). Of these, only E. canescens H. cerberoanus y (authorized installed capacity 115 MW, 50 wind turbines), and the e e G. resinosa O. paradoxus T. skottsbergii are also dominant in second is 1800 m to the west of Cerro Talinay (authorized 500 MW, BFJNP. 167 wind turbines). An extensive network of roads and platforms were established to install these wind farms and have impacted the 6. Fires and other older impacts vegetation. Although the companies in charge have partially miti- gated these impacts, the natural landscape has been inevitably The hilltops of Altos de Talinay show evidence of forest fires in transformed. the late 18th century and during the 19th century (Fuentes and Finally, cellular antennas have been installed on the hilltop of Torres, 1991). Most of this evidence is in the south-central region Cerro Talinay, within the protected area and at the edge of the relict of the forest (Fig. 2). Apparently, there has only been one small fire forest. Their construction only marginally affected the forest and in the northern region that involved three adult A. punctatum trees their impact was partially compensated with an irrigated planta- located in an isolated fragment (northernmost arrow in Fig. 2). The tion of forest species. area where the forest trail is located (i.e., Sendero in Fig. 2) also had a fire on its west-facing slope. Moreover, there is evidence of a fire 8. Bosque Fray Jorge National Park: a biosphere reserve in the scrub of east-facing slopes of El Solon, which only marginally compromised the forest. In Las Papas, there are signs of agriculture Biosphere reserves are typically organized into three interre- and of a lesser fire, which did not affect an area larger than 1.5 ha. lated and sequential zones known as the “fried egg model”: the The largest area of the forest affected by fires is near Centinela, core area, the buffer zone, and the transition area (Araya, 2009). where natural forest regeneration has been observed, but without BFJNP includes the core area, but lacks both the buffer zone and the D. winteri recruitment (Squeo et al., 2004). transition area. This characteristic is common to other biosphere Agriculture, timber extraction, and cattle have also impacted reserves in Chile established before 1995 (Araya, 2009), because at BFJNP. For example, Las Papas (formerly the southern limit of the the time the “fried egg” land-use scheme was not a mandatory park) had potato (Solanum tuberosum) and wheat crops until the requirement. 1970s (Fuentes and Torres, 1991). According to Munoz~ and Pisano Although BFJNP has a conservation management plan in place (1947), timber extraction at Portezuelo de La Labranza caused the (CONAF, 1998), the area is not immune to accidents and other im- disappearance of D. winteri in that locality. These authors also pacts resulting from global change. Currently, all land surrounding report cattle ranching throughout the forest until 1943; thus, BFJNP is private; therefore it is unlikely to expand as it was rec- trampling and grazing by cattle likely affected the forest's vegeta- ommended, in order to achieve the conservation goals committed tion structure. Cattle ranching activities continued from Las Papas by Chile in the Convention on Biological Diversity (Squeo et al., to Punta del Viento until the 1970s (Fuentes and Torres, 1991; Squeo 2012). An alternative to expand BFJNP is to create private pro- et al., 2004, 2005). Finally, changes in land cover have facilitated the tected areas, which would correspond to Category IV protected 20 F.A. Squeo et al. / Journal of Arid Environments 126 (2016) 12e22

Fig. 4. Anthropization index of the vegetation in Bosque Fray Jorge National Park (BFJNP) and the buffer zones. Based on CONAF (2004) and Squeo et al. (2003). F.A. Squeo et al. / Journal of Arid Environments 126 (2016) 12e22 21 areas of IUCN's Protected Areas Categories System. Nacional Forestal, Ministerio de Agricultura, República de Chile. Documento de trabajo N297. CONAF, 1999. Catastro y Evaluacion de Recursos Vegetacionales Nativos de Chile. 9. Conclusion Corporacion Nacional Forestal e Comision Nacional del Medio Ambiente, Santiago. fi CONAF, 2004. Catastro de Uso del Suelo y Vegetacion. Cuarta Region de Coquimbo. Of cially protected for 74 years, BFJNP owes its name to a relict Corporacion Nacional Forestal, La Serena. forest located on Altos de Talinay that represents only 2.6% of the Cruzat-Gallardo, A.A., 2004. El uso de las nieblas en la recuperacion del Parque park's area. However, BFJNP is much more that the relict forest; it Nacional Bosque Fray Jorge. In: Squeo, F.A., Gutierrez, J.R., Hernandez, I.R. (Eds.), Historia Natural del Parque Nacional Bosque Fray Jorge. Ediciones Universidad possesses a natural mosaic of vegetation formations characteristic de La Serena, La Serena, pp. 281e292. of the original Coastal Desert vegetation. As such, BFJNP protects a Fuentes, J.A., Torres, M.E., 1991. Estudio historico evolutivo de la interaccion del remnant of the natural vegetation that dominated the Coastal hombre del semiarido en una region del Norte Chico: Fray Jorge Reserva Desert before European colonization. Mundial de la Biosfera. Tesis para optar al Grado de Licenciado en Educacion y al Título de Profesor de Estado en Historia y Geografía. Universidad de La Serena. In contrast to the fog relict forest that been historically isolated, Francois, J.P., 2004. Eslabones de una cadena rota: El caso del bosque relicto de the xerophytic formations, which were once continuous, are pro- Santa Ines. In: Squeo, F.A., Gutierrez, J.R., Hernandez, I.R. (Eds.), Historia Natural gressively becoming isolated and losing their connectivity to hab- del Parque Nacional Bosque Fray Jorge. Ediciones Universidad de La Serena, La Serena, pp. 205e218. itats outside the park. Current evidence suggests that the Gajardo, R., Toral, M., Cubillos, V., 1984. Estudio de Regeneracion en el Bosque de consequences of this isolation may ultimately affect the mainte- Fray Jorge (Informe Final). Departamento de Silvicultura y Manejo, Facultad de nance of BFJNP's biodiversity. If the remnant areas that surround Ciencias Agrarias, Veterinarias y Forestales, Universidad de Chile. Gutierrez, J.R., Meserve, P.L., Jaksic, F.M., Contreras, L.C., Herrera, S., Vasquez, H., the park are not effectively protected, BFJNP will continue to remain 1993a. Structure and dynamics of vegetation in a Chilean semiarid thornscrub as only the yolk at the center of the “fried egg model”. community. Acta Oecol. 14, 271e285. Given that coastal areas in north-central Chile are experiencing Gutierrez, J.R., Meserve, P.L., Contreras, L.C., Vaquez, H., Jaksic, F.M., 1993b. Spatial distribution and soil nutrients and ephemeral plants underneath and outside a rapid land use transformation (Squeo et al., 2001), it becomes the canopy of Porlieria chilensis (Zygophyllaceae) shrubs in arid coastal Chile. essential not only to protect these areas, but also to understand the Oecologia 95, 347e352. dynamics of their natural vegetation. In an effort to protect and Gutierrez, 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 restore these areas, a newly proposed law aims to create a Service of zone. Oecologia 109, 398e406. Biodiversity and Protected Areas (SBAP in Spanish) in charge of Gutierrez, J.R., Meserve, P.L., Kelt, D.A., 2004. Estructura y dinamica de la vegetacion leading efforts to recover threatened species and restore ecosys- del ecosistema semiarido del Parque Nacional Bosque Fray Jorge entre 1989 y tems (Squeo et al., 2012). This law will also transfer the adminis- 2002. In: Squeo, F.A., Gutierrez, J.R., Hernandez, I.R. (Eds.), Historia Natural del Parque Nacional Bosque Fray Jorge. Ediciones Universidad de La Serena, La tration of public protected areas from CONAF (currently under the Serena, pp. 115e134. Ministry of Agriculture) to SBAP (under the Ministry of Environ- Gutierrez, J.R., Meserve, P., Kelt, D., Engilis, A., Previtali, M.A., Milstead, W.B., ment), and add private protected areas to the national system. Jaksic, F.M., 2010. Long-term research in Bosque Fray Jorge National Park: twenty years studying the role of biotic and abiotic factors in a Chilean semiarid Although, the first initiatives for the recovery of threatened species scrubland. Rev. Chil. Hist. Nat. 83, 69e98. have recently been implemented, there are still no formal initia- Hernandez, I.R., Vita, A., 2004. Reforestacion para la expansion de los bosquetes de tives for degraded ecosystem restoration. Finally, because over 99% Olivillo. In: Squeo, F.A., Gutierrez, J.R., Hernandez, I.R. (Eds.), Historia Natural del Parque Nacional Bosque Fray Jorge. Ediciones Universidad de La Serena, La of BFJNP has a low anthropization index, we argue that the majority Serena, pp. 307e319. of the vegetation communities in the park serve as appropriate Jara-Arancio, P., Carmona, M.R., Correa, C., Squeo, F.A., Arancio, G., 2012. Leaf reference conditions for ecological restoration of Coastal Desert morphological and genetic divergence in populations of Drimys (Winteraceae) in Chile. Genet. Mol. Res. 11, 229e243. ecosystems of north central Chile. Johnstone, J.A., Dawson, T.E., 2010. Climatic context and ecological implications of summer fog decline in the coast redwood region. PNAS 107, 4533e4538. Acknowledgments Kummerow, J., 1962. Mediciones cuantitativas de la neblina en el Parque Nacional Fray Jorge. Boletín Universidad de Chile 28, 36e37. Kummerow, J., 1966. In: Aporte al conocimiento de las condiciones climaticas del We thank Gina Arancio (Herbarium Curator, Universidad de La bosque Fray Jorge. Universidad de Chile. Facultad de Agronomía, Estacion e Serena) for plant identification, David Lopez help with GIS, and Experimental Agronomica, Boletín Tecnico, 24, pp. 21 24. Loayza, A.P., Carvajal, D.E., García-Guzman, P., Gutierrez, J.R., Squeo, F.A., 2014. Seed James Herlan for revising English usage. We also thank reviewers predation by rodents results in directed dispersal of viable seed fragments of an for their useful comments. Financial support has been provided by endangered desert shrub. Ecosphere 5 art43. Loayza, A.P., Rios, R.S., Carvajal, D.E., Gatica, A., 2015. Estado de conservacion de FONDECYT No. 1070808 to J. R. Gutierrez. 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