A phytosociological analysis and synopsis of the dry woodlands and succulent vegetation of the Peruvian Andes

A phytosociological approach to dry forest and cactus communities on the occidental slopes of the Peruvian Andes is presented in base of 164 plots carried out following the Braun-Blanquet method. From them, 52 have been made recently, and the other 112 were taken from the literature. After a multivariate analysis, using a hierarchical clustering and a detendred correspondence analysis, the Acacio-Prosopidetea class (dry forest and cactus communities, developed on soils with some edaphic humidity or precipitations derived from El Niño Current), the Opuntietea sphaericae class (cactus communities of central and southern Peru, on few stabilized rocky or sandy soils) and the Carico-Caesalpinietea class (dry forests of the Peruvian coastal desert, infl uenced by the maritime humidity of the cold Humboldt Current), are differentiated. Within the Acacio-Prosopidetea class, two alliances are commented: the Bursero-Prosopidion pallidae (with two new associations Loxopterygio huasanginis-Neoraimondietum arequipensis and Crotono ruiziani-Acacietum macracanthae), and the new alliance Baccharido-Jacarandion acutifoliae (with the new associations Armatocereo balsasensis-Cercidietum praecocis and Diplopterydo leiocarpae-Acacietum macracanthae). For the Opuntietea sphaericae class, the association Haageocereo versicoloris-Armatocereetum proceri (Espostoo-Neoraimondion) is described on the basis of plots from hyperarid localities of central Peru. Finally, a typological classifi cation of the studied plant communities is given.


INTRODUCTION
Dry forests and cactus communities are widely extended in South America (Blanco et al. 2013).In Peru, they are concentrated on the western slopes of the Andean Cordillera, in the inter-Andean valleys, and in the north of the country (Linares-Palomino et al. 2003).There, in the north, dry forests are further extended as a continuation of the Ecuadorian dry forests (Aguirre et al. 2006).These plant formations in Peru, with rainfall less than 500 mm/year, are linked to the uplift of the Andean Cordillera in the Paleocene, and the strengthening of the cold ANTONIO GALÁN-DE-MERA et al.Humboldt Current in the Eocene (Livermore et al. 2005), evolving a hyperarid period in the Atacama Desert (Luebert and Gajardo 2005) which isolated some territories with a large number of endemic plants (Galán de Mera et al. 1997).
The Peruvian endemic cactus occur also within northern dry forests around the Amotape-Huancabamba Zone (Weigend 2002), and the occidental Andean slopes and inter-Andean valleys, contributing to the original plant communities of this country.Thus, a new phytosociological contribution along the Peruvian Andes is reported in this paper, with the aim to understand better the beta-diversity of these dry plant communities throughout the syntaxonomical units.

STUDY AREA
The studied area covers circa 1600 Km along the occidental slopes of the Peruvian Andes up to 3000 m asl, where vegetation changes from succulent vegetation to the Andean shrublands.We have taken data from the southern Peruvian border in the Tacna Department (approximate latitude-18°01'S-70°14'W) to North Peru in the Cajamarca Department (approximate latitude-07°16'S-79°08'W). In the Cajamarca Department, the succulent vegetation around the Huancabamba Depression (06°03'S-79°04'W) and in the Marañón valley (between 06°35'S-78°06'W and 05°45'S-78°41'W) were also investigated as well the wide coast of the Arequipa Department in southern Peru (approximate latitude-17°02'S-71°43'W).
The tropical climate in all the studied localities is arid (0-300 mm) to dry (300-500 mm), except for some sites of the northern, where annual precipitation can reach 900 mm.The annual average temperatures oscillate between 15°C to 25°C.For a bioclimatic diagnosis of Peruvian syntaxa, the bioclimatic model of Rivas-Martínez is followed (Rivas-Martínez andRivas-Saenz 1996-2009), where data from meteorological stations between infra-and supratropical belts with hyperarid to dry precipitation range, have been considered.For its intervals and nomenclature see Table I.Durka 1997), where percentage intervals of species presence were transformed into symbols (< 10% = +, 11 to 20% = 1, 21 to 40% = 2, 41 to 60% = 3, 61 to 80% = 4, and > 81% = 5); their references are given in the Appendix I. Table SIII (Supplementary Material) shows the plots of the new associations and alliances; their localities are presented in the Appendix II.
In order to improve the manual classifi cation of the columns of Table SII, a hierarchical clustering producing a dendrogram has been made, using the similarity index (UPGMA) of Bray and Curtis (1957), which takes into account the abundance values of the plants of the plots.A detrended correspondence analysis (DCA) is provided in order to discuss how columns are grouped.This statistical analysis was performed by PAST 3.04 program (Hammer 2014).
To discuss the higher phytosociological units and their relationships with the vegetation neighboring Peru, some works from Ecuador (Aguirre et al. 2006, Weigend 2002, 2004), Colombia (Rangel et al. 1997, Ruiz et al. 2002) and Chile (Luebert and Gajardo 2005), have been consulted.As a result, some new associations and other phytosociological units are described.
The nomenclature of taxa in the text and tables follows The Plant List (2013).For the nomenclature of syntaxonomical units, the International Code of Phytosociological Nomenclature is followed (Weber et al. 2000).

STATISTICAL ANALYSIS
The dendrogram of Figure 1 and Table SII    Figure 3 shows the distribution of Acacio-Prosopidetea and Opuntietea classes in Peru.The fi rst class is distributed in the north, while the second is widely distributed in central and southern Peru.

ALLIANCES AND THEIR ASSOCIATIONS
The Acacio-Prosopidetea class encloses the dry forests and succulent plant communities of northern Peru, infl uenced by the rainfall originating from the warm El Niño Current, and also forests on riverside humid soils of the Western Andes, between 100 and 2500 m asl (Galán de Mera et al. 2009).the alliance are Bougainvillea peruviana, Bursera graveolens, Capparicordis crotonoides, Cordia lutea, Croton lobatus, Deuterocohnia longipetala, Loxopterygium huasango, Onoseris odorata, and Prosopis pallida, according to the altitudinal distribution indicated by Ceroni Stuva (2003).In a recent work (Galán de Mera et al. 2013), the subhumid forests of the Annono cherimolae-Acacietum macracanthae association is mentioned between 2000-2500 m asl, but it is a very disturbed forest where we could not fi nd plots of suffi cient homogeneity.
Baccharido Opuntietea sphaericae class includes the cactus plant communities of central and southwestern Peru, and Chile, up 3000 m asl, on few stabilized rocky, or sandy soils (Fig. 3).Thus the concept of their distribution throughout South America has been amended, since the original description of Galán de Mera and Vicente Orellana (1996) that proposed a distribution throughout the Neotropics.Its Oreocereo-Neoraimondietalia order includes three alliances with a clear geographic distribution up to 3000 m asl: Espostoo melanostelis-Neoraimondion arequipensis (Galán de Mera et al. 2002aMera et al. , 2004)), extended through the hyperarid and semiarid thermotropical belt of central Peru (Fig. 1, branches 8 to 13; Fig. 2, group D), between the parallel 8°S and Ica Department (Fig. 3 Although Haageocerion decumbentis is a southern alliance, in the dendrogram (Fig. 1, branch 14) and also in the DCA (Fig. 2, group E), it is close to the cactus communities of central Peru with N. arequipensis, due to its low diversity and the absence of Corryocactus brevistylus.

Loxopterygium huasango, and Neoraimondia arequipensis).
Infratropical arid-semiarid cactus commu nity with Neoraimondia arequipensis and Haageocereus versicolor, enriched with small trees such as Bursera graveolens, Cercidium praecox, and Loxopterygium huasango, extending between 5ºS and 8ºS, with different inclinations up to 60%, from the surroundings of Sullana (Piura) to the North of Trujillo (La Libertad).The geological materials where it is placed are Cretaceous volcanic sedimentary soils, and Tertiary volcanic and plutonic rocks.
The plots of this association have been sampled in some localities to the South of the Cajamarca Department on Cretaceous volcanic sedimentary and Tertiary plutonic soils with heavy clay substrata.

DISCUSSION
Within the Opuntietea class, southern Peru presents a high beta-diversity in terms of associations (Whittaker 1972), stimulated by the important infl uence of the cold Humboldt Current, coupled with the western rain shadow caused by the elevation of the Peru-Bolivia Altiplano (~ 4500 m asl) (Galán de Mera et al. 2012).According to the investigations of Schwarzer et al. (2010), the diversity of this territory is also a consequence of successive volcanic events.An example of this high diversity is that the Corryocaction brevistyli alliance is represented in the DCA (Fig. 2) by the separated groups F and G, where F shows the thermotropical associations with Neoraimondia arequipensis, and G are the meso-and supratropical ones.However, in the Espostoo-Neoraimondion alliance, only the thermotropical associations are found.
Peruvian dry forest communities are fl oristically and ecologically linked to those of the Caribbean Region and the north of southern America.Borhidi (1991) described the Cercidio-Prosopidetea class in Cuba, where Cercidium praecox, Prosopis juliflora (also reported for Peru), and different species of Capparis and Melocactus, are present.In Colombia, forests and cactus communities with Browningia, Capparis, Melocactus, Pereskia, and Prosopis julifl ora can also be found (Ruiz et al. 2002, Fernández Alonso 2006, Rangel 2012).To the South, Acacia macracantha, Annona cherimola, Espostoa lanata, Loxopterygium huasango, Prosopis pallida, Schinus molle, and others are present in Ecuador (Aguirre andDelgado 2001, Aguirre et al. 2006), belonging to the Acacio-Prosopidetea class (Galán de Mera et al. 2002a).However, on the western slopes of the Peruvian Andes and the coastal desert, dry forest and cactus communities with climate dependence, show some plants which support the originality of this type of vegetation with respect to those of Ecuador (Croton ruizianus, Encelia canescens, Krameria lappacea, Lycianthes lycioides, Melocactus peruvianus, Neoraimondia arequipensis, Trixis cacalioides, and Waltheria ovata).A particular phytogeographical element is Neoraimondia arequipensis, an endemic plant of Peru, which is distributed from Tacna to La Brea in Piura (Svenson 1946, Ostolaza 2011), within the Amotape-Huancabamba Zone (Weigend 2002).Acacio-Prosopidetea, with Cryptocarpo-Prosopidetalia order (Galán de Mera et al. 2002a), encloses the dry forests that stretch to the occidental slopes of the Andes in Piura to 8°S, in the surroundings of Trujillo, and coincide with the southern part of the Amotape-Huancabamba Zone (Weigend 2002).
Armatocereo balsasensis-Cercidietum praecocis (Table SII, column 9; Table SIII, plots 16 to 27), represented in the dendrogram as a separated association from those of Bursero-Prosopidion pallidae, really belongs to the Baccharido-Jacarandion acutifoliae alliance (see Fig. 2, group B), because it is an oriental association distributed through the Marañón Valley and the Huancabamba Depression.Among its fl oristic components, several occidental plants, such as Bursera graveolens, ANTONIO GALÁN-DE-MERA et al.
In general, dry forests can be found on deep soils along the Peruvian territory.These forests are replaced by succulent plant communities on rocky or sandy slopes (± 60%), or few stabilized soils.Independently of geomorphological aspects, the Acacio-Prosopidetea class extends from the 8°S parallel through northern Peru (Fig. 3), linked to the infl uence of the warm El Niño Current (50-900 mm/year).Even so, in the center and south of Peru it is also placed on soils with edaphic humidity which were suitable for crops from ancient times, but without cactus (Beresford-Jones 2009).Below the 8°S parallel, this class is substituted by several associations of the Opuntietea sphaericae class, which tolerate higher aridity (5-100 mm/year) and are infl uenced by the cold Humboldt Current.The forests and bushes of the Carico-Caesalpinietea class are marginal, being located in those places of the coastal desert with higher humidity (300-500 mm/year).

CONCLUSIONS
The hierarchical classifi cation of dry forest and succulent plant communities studied, resulted in the following syntaxonomical scheme of the Opuntietea, Acacio-Prosopidetea and Carico-Caesalpinietea classes in Peru.This scheme includes the proposal of two new alliances, fi ve associations and two subassociations.

TABLE I Bioclimatic belts and interval types of precipitation according to the bioclimatic model of Rivas-Martínez. It = 10 (T + m + M)[T: average annual temperature (in °C), m: average lowest temperature in the coldest month, M: average highest temperature in the coldest month], P: annual precipitation.
STUDYING THE VEGETAT, Biondi 2011)ological study of northern dry forests and cactus communities of the occidental slopes of Peruvian Andes, including some localities of the coastal desert, is presented.It is based on 164 plots carried out following the Braun-Blanquet method(Braun-Blanquet 1979, Biondi 2011).Fifty-two of them have been made recently by the authors, and the rest have been taken from numerous references from other authors.A synthetic table was made up with all the plots (TableSII-Supplementary Material) using SORT 4.1 program (Ackermann and