Observations on the biogeography of the Amotape-Huancabamba Zone in northern Peru.
The Huancabamba Depression in the Andes of northern Peru has been considered an important biogeographical barrier. It is an area where the Andean cordilleras are partially interrupted by the Rio Chamaya / Rio Maranon system. The Central and Eastern Cordilleras are entirely interrupted by these deep valleys. Only the Western Cordillera extends over the region, and it has its lowest point, 2145 m, at the Abra de Porculla, in the Department of Lambayeque (the physical geography of the area is described in more detail by Duellman, 1979; politically, Peru is divided into departments; departments are subdivided into provinces). The area was not recognized as an important center of overall biodiversity until very recently, when mounting evidence led Young and Reynel. (1997) to propose a recognition of the eastern part of the region around the Huancabamba Depression as an important hotspot of biodiversity. This judgment has since received strong support from a compilation of endemic taxa of the Department of Cajamarc a (which lies completely in this area) by Hensold (1999), which lists a total of 318 endemic angiosperm taxa. This number is a minimum estimate, because it excludes the extremely speciose Orchidaceae.
It has been hypothesized that the narrowness and low altitude of the Andean chain and the resulting disruption of (especially high Andean) habitats in this area have been important factors limiting the dispersal of montane taxa between the Northern and Central Andes (Vuilleumier, 1968; Molau, 1988; Prance, 1989; Ayers, 1999). This biogeographical barrier has been variously called the Northern Peruvian Low, the Huancabamba Deflexion, the Piura Divide, and the Huancabamba Depression.
However, Berry (1982) argued against the theory of a phytogeographical barrier on the basis of the unusual (and frequently endemic) species of Fuchsia L. found in this region. He highlighted the fact that there is an entire region that is unusual in species composition and shows equal affinities to the Northern and Central Andes. He intercalated a distinct Amotape-Huancabamba Zone between the two regions on his map of phytogeographical zones for Fuchsia (Fig. 1). His Amotape-Huancabamba Zone extends from the extreme south of Ecuador to northern Peru and narrows to the east, but he did not indicate precise limits in his text or illustration.
Ayers (1999) also emphasized the extraordinary species richness on both sides of the Huancabamba Depression for the high-altitude genus Lysipomia Kunth (Campanulaceae) and stated that 50% of the species known from the genus occurred in this area. A rough calculation on the basis of her data reveals that there are about three times as many species of Lysipomia per unit area in this region as in the rest of the range of the genus. Ayers concluded that the barrier effect of the Huancabamba Depression has been dramatic but that specific habitat conditions in the area also contribute to the high level of diversification in Lysipomia. Fjeldsa (1995) discussed the importance of arid inter-Andean valleys as dispersal barriers for Andean birds and came to a conclusion that agrees well with Berry's (1982) postulate: The mere presence of physical barriers is of less importance than are "some specific ecological conditions prevailing on both sides of the gap" (Fjeldsa 1995: 98). The Ecuadorean part of the Amotape-Huancab amba Zone was briefly discussed by Jorgensen et al. (1995; it is their "southwestern region"), who emphasized that the area is poorly studied but nevertheless appears rather isolated in comparison with the other Ecuadorean zones (relationships to adjacent Peru were not discussed).
I will discuss the phytogeography of this zone with respect to distribution patterns in Loasaceae, which are particularly suited for such a comparison. The alpha-taxonomy of the group is now largely known, and the group is very diverse in the Andes, with their absolute center of diversity in northern Peru (Fig. 2; Appendix 1). The primary questions addressed are: Can the Huancabamba Depression itself be considered a biogeographical barrier, or is there a distinct phytogeographical zone that might better be considered a phytochorion in its own right? What factors contribute to its high biodiversity? Can the observations made on Loasaceae be generalized and applied to other groups of organisms?
The analysis is primarily based on revisionary studies on the family Loasaceae (Weigend, 1998, 1999, 2000a, 2000b; Weigend & Rodriguez R. 1998; Weigend et al., 1998; Dostert & Weigend, 1999; Rodriguez & Weigend, 1999) and Ribes. A total of 30 weeks of field studies were carried Out between 1995 and 2001 in all relevant provinces of Ecuador and all Andean departments of Peru. Additional data and collections were provided by T. Franke and A. Hofreiter (1999, Peru, Departments of Pasco, Huanuco, Amazonas), M. and T. Hofreiter (1998, Ecuador, Province of Loja), E. F. Rodriguez R. (1998-2000, Peru, Departments of Cajamarca, La Libertad, Amazonas), V. Quipuscoa (2000, Peru, Department of San Martin), A. Cano E. (2000, Peru, Department of San Martin), and N. Dostert (1998, Peru, Departments of Cajamarca, San Martin, Amazonas). Until 2000, data from the Department of Huanuco and the northern parts of the Department of Ancash (the Callejon de Conchucos) were still unsatisfactory, so a collecting trip was taken in 2001 (March 5-April 1), which largely closed that gap.
Additional data used are from revised herbarium specimens, which included loans from the major international herbaria (B, BM, CGE, E, F, G, HBG, HUH, K, NY, OXF, P, US, W, WU) and all important local and national herbaria in Peru and Ecuador (CPUN, CUZC, HUT, HAO, LOJA, MOL, QCNE, QCA, USM). There are now field data from direct observations for a very large part of the relevant area, and the very unequal documentation of the flora of different parts of the cordilleras in Peru in the herbaria has been largely overcome. In spite of the relative wealth of data there is still unsatisfactory documentation from the southern part of the Department of San Martin in Peru (very few collections) and the Cordillera del Condor in Ecuador (Province of Zamora-Chinchipe, no Loasaceae reported so far). However, overall documentation is now very good, and any additional data from future collecting trips are unlikely to overturn the major trends reported here.
Many of the arguments rely heavily on the interpretation of phylogenetic relationships and perceived species groupings. These are based on detailed morphological studies both in the herbarium and in the field, but molecular studies are only now under way. The theses here proposed will be tested more rigorously once resolved phylogenies are available for the taxa discussed here.
The terms "Northern Andes," "Central Andes," and "Southern Andes" are used inconsistently in phytogeography. In the present article I adopt a definition based on physical geography: The Northern Andes are north of the Huancabamba Depression (at 4-6[degrees] S); the Central Andes are south of the Huancabamba Depression and end approximately in central Bolivia (the spur of the Andes near Santa Cruz, at 18[degrees] S); and the Southern Andes are south of this region.
The region around the Huancabamba Depression is here called the Amotape-Huancabamba Zone, following Berry (1982). Other, more appropriate names are conceivable, but it seems better to adhere to that established term. On the coast the southern limit of the zone lies south of the Rio Chicama drainage system (Peru, Department of La Libertad, Trujillo), the highlands of Conchucos (Peru, Department of Ancash, Province of Corongo), and Tayabamba (Peru, Department of La Libertad, Province of Pataz); and its northern limit are the Rio Jubones (Ecuador, Province of El Oro, Machala) and Rio Zamora (Ecuador, Province of Zamora-Chinchipe) drainage systems. An overview over the region is given in Figure 1.
V. Results and Discussion
A. DELIMITATION OF THE AMOTAPE-HUANCABAMBA ZONE
The crucial phytogeographical features of the delimitation of the Amotape-Huancabamba Zone are the overlap of southern and northern species or species groups and the presence of certain plant groups that are either endemic to this area or have at least their highest species concentration in it.
The northern limit is thus easily defined on the western slope of the Andes. It represents the northern distribution limit of typically southern groups and groups centered in the Amotape-Huancabamba Zone-e.g., Nasa olmosiana (Gilg ex J. F. Macbr.) Weigend (Fig. 3), N. bicornuta (Weigend) Weigend (Fig. 4), and N. ser. Carunculatae. The northern limit is thus found in the Rio Jubones drainage system. On the eastern slope a floristic distinction is more difficult, because few Loasaceae have been reported from this area. There is a conspicuous paucity of collections from Loasaceae and Ribes, but it can be clearly seen from the distribution data that widespread taxa ranging from Colombia into Ecuador (Ribes hirtum Willd., R. ecuadorense Jancz., and Nasa triphylla subsp. papaverifolia (Kunth) Weigend, southernmost collections in the Province of Azuay) are absent south of the Rio Zamora drainage system. In or south of that drainage system they are replaced by either endemic species or species otherwise found in nort hern Peru.
The southern limit of the Amotape-Huancabamba Zone on the western slope of the Andes, in the Central Cordillera, and the inter-Andean valleys is the southernmost distribution limit of typically northern taxa-N. humboldtiana (Urb. & Gilg) Weigend, N. peltata group--and taxa endemic to--Nasa macrothyrsa (Urb. & Gilg) Weigend, N. laxa (J. F. Macbr.) Weigend, and N. pteridophylla Weigend (Fig. 4), or centered in the Amotape-Huancabamba Zone-e.g., the Ribes andicola group and most species of the Passiflora lobbii group. It also includes the ranges of five of the seven species of the Nasa stuebeliana group and the entire range of the typical subspecies of Nasa picta (Hook. f.) Weigend. The eastern slope of the Andes presents more problems in the delimitation of a clear phytogeographical border. Extensive collections in the last few years and my own field studies have dramatically improved our understanding, but some gaps in our knowledge remain. Some northern taxa have their southern limit north of the Huancabamba Depression--Nasa loxensis (Kunth) Weigend--or they reach south of it. The number of northern groups then dramatically diminishes as we go south and are found in the Cordillera Colan (Department of Amazonas, Province of Bagua: Nasa anderssonii Weigend, N. dyeri (Urb. & Gilg) Dostert & Weigend of southern Ecuador) and in the Callacalla region (above Leymabamba, Department of Amazonas, Province of Chachapoyas: Nasa umbraculifera E. Rodr. & Weigend and an undescribed species of Ribes that is close to Ecuadorean species). Collections in the adjacent Province of Bolivar (Department of La Libertad) also documented the presence of various Northern Andean plant groups (N. triphylla group, N. carnea group, Ribes andicola Jancz.) and groups typical of the Amotape-Huancabamba Zone (such as the Nasa steubeliana group and endemic Mentzelia heterosepala Weigend & E. Rodr.). The southernmost known collections. of northern plant groups and typical Amotape-Huancabamba groups are from the Province of Pataz (Department of La Lib ertad), coinciding rather exactly with the limit of the Amotape-Huancabamba Zone on the western slope of the Andes as defined above. Collections both in the Rio Santa system and in the Province of Sihuas (Department of Ancash) -- i.e., the region immediately south of the Amotape-Huancabamba Zone -- failed to turn up representatives of either northern groups or Amotape-Huancabamba groups. The southern groups that enter the Amotape-Huancabamba Zone on the eastern slope consistently have their northern limit in the Province of Chachapoyas (Department of Amazonas: N. cymbopetala group).
The naturalness of these delimitations is underscored by the fact that the taxa defining these limits have different ecological requirements, so that the delimitation does not just reflect the absence of one particular habitat type on the other side. Thus, across the Andean cordilleras the limits of the Amotape-Huancabamba Zone can be rather clearly defined on the basis of the plant groups studied here. The crucial defining features (high levels of endemism, overlap of northern and southern groups) of the zone are not restricted to the western slope: There may be a wider area of overlap in the Eastern Cordillera than in the Western Cordillera, which is partly explained by presence of the Rio Maranon, which runs south to north, and may also reflect the more gradual climatic changes on the eastern slope and the less-dissected nature of its habitats. In spite of the relative uniformity of the vegetation types along the eastern slope of the Andes and in the Maranon Valley there seems to be a massive species turno ver from north to south in the Amotape-Huancabamba Zone in Loasaceae and Ribes. Our data on Ribes, the Pass flora lobbii group, and Loasaceae uniformly show this pattern. In all three groups the Amotape-Huancabamba Zone appears to be the area with the highest species turnover anywhere in the Andes north of Cuzco. The area north of Cuzco could be second major phytogeographical division, and the Santa Cruz area in Bolivia certainly ranks equal as an important division because it represents the southernmost limit of all tropical Ribes, tropical Loasaceae, and the Pass flora lobbii group.
B. LEVELS OF DIVERSITY
The diversity patterns for the genus Nasa Weigend in the Northern and Central Andes are summarized in Figure 2. It is immediately apparent that the Amotape-Huancabamba Zone has a higher species total than do either the Northern or Southern Andes. The genus Caiophora C. Presl is the only large genus that has its center of diversity outside this area. The high species number in the Amotape-Huancabamba Zone is particularly striking if we consider its area in comparison with the Northern and Central Andes: The total size of Andean habitats suitable for Loasaceae in both the Northern and Central Andes is five to six times as large as in the Amotape-Huancabamba Zone. If we correct the number of species for the difference in area, we find that there are about eight times as many species of Loasaceae per unit area in the Amotape-Huancabamba Zone as in the Central Andes and about seven times as many species per unit area as in the Northern Andes.
The Amotape-Huancabamba Zone is also a center of diversification in other plant groups, such as the Pass flora lobbii group (Skrabal et al., 2001), Fuchsia (Onagraceae; Berry, 1982), Calceolaria L. (Molau, 1988), and Asteraceae, where there are various endemic genera (e.g., Chucoa Cabreara, Caxarnarca M. 0. Dillon & Sagast., Fucaldea Poir.) and numerous endemic species (e.g., in Barnadesia Mutis ex L.f., Onoseris Willd. and Trixis P. Browne; Ferreyra, 1995).
The isolated forest patches on the western slope of the Andes have attracted particular attention, are comparatively well studied (Dillon, 1994; Dillon et al., 1995), and are of special importance. According to Hensold (1999), 47% of the endemic angiosperms of Cajamarca are from these moist forests. However, the much less known, seasonally arid (scrub) forest types of the Andean slopes and inter-Andean valleys appear to be nearly equal in diversity and may even exceed the level of endemism found in the forests: Most endemic genera of the region are from this habitat type, and Hensold (1999) listed 83 endemic taxa, which amount to 35% of the total of endemic species of Cajamarca. This listing excludes taxa that are endemic not to Cajamarca but to the Amotape-Huancabamba Zone (i.e., such taxa as Mentzelia heterosepala and Dalechampia hutchisoniana Webster range into neighboring Amazonas or La Libertad). Thus, the overall number of taxa from inter-Andean valleys that are endemic to the Amotape-Huancabamba Zone i s probably much higher.
The phytogeographical data show broad agreement with the zoogeographical data. Duellman (1979) compared distribution patterns of amphibians and reptiles in the Amotape-Huancabamba Zone and found that the northern limit for many southern taxa and the southern limit of many northern species and species groups are in this region. In addition, the zone had a high incidence of endemism, with 30 (of 43) species and two genera of amphibians and reptiles. The number of endemic frog species has since dramatically increased by the description of another 18 species of the genus Eleutherodactylus from the Amotape-Huancabamba Zone (Duellman & Pramuk, 1999). Detailed, comparable data from other groups of amphibians and reptiles are missing, but there can be no doubt that the Amotape-Huancabamba Zone is an important center of diversification for these groups of organisms. The data now available support the view that the Huancabamba region is a hotspot of biodiversity, as Young and Reynel (1997) proposed.
C. THE HUANCABAMBA DEPRESSION -- A PHYTOGEOGRAPHICAL BARRIER?
The question of whether the Huancabamba Depression has been an important phytogeographical barrier for Nasa is clearly answered by the data presented in Table I, which compares the barrier effect of the Huancabamba Valley with that of the middle Maranon Valley near Cajamarca (Balsas). The data are not really congruent, in that the comparison for the Huancabamba Valley has to be made for a much wider area because the cordilleras immediately adjacent to the depression are virtually unknown. Thus the data for the Huancabamba Depression include all taxa that occur up to 100-120 km south, whereas for the Maranon Valley the corridor is only 50 km wide. This should lead to an exaggeration of the barrier effect by the inclusion of narrowly endemic taxa from relatively distant areas (Monte Seco, Department of Cajamarca) for the Huancabamba Depression (whereas these are excluded for the Maranon). In spite of this artifact, the figures for the Huancabamba Depression are identical to those from the Maranon for the high-a ltitude taxa. Overall similarity between the floras on both sides of the Huancabamba Depression is higher because there are more low-altitude Loasaceae in this area. The altitudinal distribution of these Loasaceae is such that they are not affected by the "gap," so they can migrate readily. Also, altitudinal vegetation zones were repeatedly much lower during the Pleistocene than they are at present, and this certainly made migration along the Western Cordillera possible even right through the Chamaya Valley and relatively easy for plants even of very high altitudes. Because the Maranon Valley runs north and south it was probably permanently sheltered from moist air coming from the east and the west, leading to a persistent presence of semiarid conditions in the valley. This explains both the abundance of endemic plant species adapted to this type of habitat and the fact that even during a depression of vegetation zones, migration across the Maranon Valley was probably difficult for plants from high-lying, hum id habitats. The absence of a barrier effect of the Huancabamba Depression, as found in Loasaceae, is congruent with the data presented for other groups of organisms (Fuchsia, Berry, 1982; Asteraceae, Ferreyra, 1995; and reptiles and amphibians, Duellman, 1979; Duellman & Pramuk, 1999).
D. OVERLAP BETWEEN THE NORTHERN AND SOUTHERN GROUPS
Rather than a sharp dividing line between a Northern Andean flora and the Central Andean flora, there really is a broad zone of overlap. This is especially true for low- and mid-elevational taxa. Nearly all species groups of Nasa enter the Amotape-Huancabamba Zone (Appendix 1), with the exception of one exclusively Northern Andean group (Nasa venezuelensis group in northern Colombia and Venezuela). The respective northern and southern groups in the Amotape-Huancabamba Zone grow in habitats that correspond to those they also colonize in their main distribution areas: The N. cymbopetala group is exclusively found in puna habitats at the base of rocks in the Central Andes, the habitat it also occupies in the Amotape-Huancabamba Zone -- e.g., N. ranunculifolia (Kunth) Weigend, Fig. 5. The closely allied Northern Andean group around Nasa grandiflora (Desr.) Weigend is found on the margins of moist thickets and cloud forest, where it also grows in the Amotape-Huancabamba Zone -- N. weberbaueri (Urb. & Gilg) Weigend , N. umbraculifera, Fig. 3.
Thus, the high diversity is partly explained by the coexistence of both southern and northern groups in the Amotape-Huancabamba Zone. This is true for all but one species of Caiophora entering from the south and is also true for Gronovia scandens L. (Loasaceae) from the tropical deciduous forests. Gronovia scandens is found throughout Mesoamerica and also in tropical deciduous forests in Venezuela, Colombia, and Ecuador. It enters Peru at the western foot of the Andes and finds its southern distribution limit around Chiclayo, in the Amotape-Huancabamba Zone. The same pattern is found in other plant families and genera, such as the Martyniaceae (Proboscidea Schmidel).
Along the same lines, it has been argued that the relict forests on the western slopes of the Andes represent the southern distribution limits for many Northern Andean species (Dillon, 1994; Nasa peltata group, Fig. 3; N triphylla group, Fig. 4). The (nonforest) habitats of the Amotape-Huancabamba Zone also represent the northern distributional limit for many species of the dry, western slopes of the Peruvian Andes, such as Presliophytum (Urb. & Gilg) Weigend (Loasaceae), which extends well into the zone but finds its northern limit at the latitude of Chiclayo. A whole suite of species finds its northern distribution limit in or just south of the Amotape-Huancabamba Zone. The entire lomas flora has its northernmost outliers in La Libertad. It should be emphasized that the Huancabamba Depression itself does not mark the distribution limit of the species and genera.
All of the genera and species groups that come from the south or the north end well before the Huancabamba Depression (i.e., Abra de Porculla, ca. 60[degrees] S) or reach well beyond it. The species group pair Nasa peltata group (from the north) and Nasa magnifica group (from the south) on the western slope is paralleled by the pair of the Nasa grandiflora group (from the north) and the Nasa cymbopetala group (from the south) on the Eastern Cordillera. Both pairs have zones of overlap between approximately 6[degrees][degrees]30' S and 80[degrees] S. Ayers (1999) mentioned a barrier effect as an important factor in high-elevation Lysipomia, but my observations of high-elevation taxa (Ribes, Saxifraga L., Nasa grandiflora group) do not reveal any such effect. Which of the two interpretations will ultimately be the more representative remains to be determined when data on a wider range of taxa are available.
E. DISPERSAL ACROSS THE CORDILLERAS
Both in the Northern and the Central Andes, the species groups of Loasaceae are usually restricted to one side of the mountains. This is not always the case in the Amotape-Huancabamba Zone. Typical species groups and species of the zone are found on its western slopes, eastern slopes, and inter-Andean valley (e.g., Nasa triphylla and Nasa stuebelii groups). Dispersal appears to have been frequent across the Western Cordillera in the Amotape-Huancabamba Zone. Duellman (1979) argued for a faunistic exchange between the Pacific lowlands and the Maranon Valley across the low passes of the Western Cordillera (Abra de Porculla); this pattern is also reflected in my botanical data.
The Rio Santa system has also been a point of entry for western-slopes taxa into the inter-Andean valleys (e.g., Nolana L.f., Presliophytum, and Cryptantha Lehm. ex G. Don), but here they do not reach the Maranon system, as they do in the Amotape-Huancabamba Zone. The only other area where western-slope species seem to have penetrated the valleys of the Eastern cordillera (i.e., along rivers that run into the Amazon Basin) to a major extent is in the Rio Apurimac system much farther south.
Another factor contributing to high regional diversity is the narrow endemicity of most species found in the Amotape-Huancabamba Zone (at least in Ribes, Loasaceae, and the Passiflora lobbii group). The relict forest of Monte Seco (Department of Cajamarca), with an area of only 2500 ha, has a total of five taxa of Loasaceae, all of which are endemic to the area (three species, two subspecies). Similarly, the Otuzco-Contumaza region has a total of eight species of Loasaceae, of which five are endemic species and one is an endemic genus (Xylopodia Weigend). This pattern holds true for other sites (e.g., Canchaque, Province of Huancabamba, Department of Piura). The relict forests on the Pacific slope of the Andes (Dillon et al., 1995) usually have the most narrowly endemic species, whereas the taxa found in the Central Cordillera and on the eastern slope tend to be slightly more widespread (in spite of the fact that the latter region is less known and should therefore have smaller known ranges). There is strong altitudinal separation of species, and the wet versus dry sides of mountain ranges usually have differing species compositions (Nasa ser. Alatae, Weigend, 2000a; Passiflora lobbii group, Skrabal et al., 2001). The forest species are usually the most narrowly endemic taxa, especially on the western side of the Andes, but many of the species of relatively (at least seasonally) arid habitats are also narrowly endemic (e.g., Nasa urentivelutina Weigend).
The patterns of distribution and endemism recognized in data on herbaceous plant groups, amphibians, and reptiles are not as evident in data on the distribution of woody species (Prance, 1989) or Andean birds (Fjeldsa, 1995). This may reflect one of the idiosyncrasies of the Amotape-Huancabamba Zone: It represents a complex mosaic of relatively small habitat fragments. Habitat fragmentation is conducive to speciation in taxa that can maintain viable populations in small habitats, such as herbaceous plant species and small vertebrates with slow and inefficient dispersal over unfavorable terrain. Small but viable populations of these organisms may then diverge very rapidly through random drift and/or adaptive pressures. Tree species and birds may not be able to maintain viable isolated populations in these small habitat fragments, and birds, at least, will readily cross physical barriers that are all but insurmountable for other organisms (or diaspores). Even if isolated populations of long-lived, woody species are viable, evolutionary divergence will nevertheless be considerably slower than in herbaceous taxa because of the longer generation time (generation-time effect). It is to be expected that in taxa with low dispersal ability and short generation time the level of endemism will be much higher than in easily dispersed taxa with a long generation time. This is certainly one of the reasons why the genus Caiophora (perennial herbs with wind-dispersed seeds) has far fewer narrow endemics than does the genus Nasa (often annual or short-lived perennial herbs with barochoric seeds). In spite of the fact that percentages of endemism in woody plants are usually expected to be lower than in herbaceous species, numerous shrub species and some tree species are endemic to the Amotape-Huancabamba Zone, as can be seen from Hensold (1999), especially among the Melastomataceae.
G. ECOLOGICAL DIFFERENTIATION
Another important factor contributing to the high species number in the Amotape-Huancabamba Zone is the colonization of atypical habitats by many species of Loasaceae; i.e., habitats where either the entire genus or at least all the other species of the respective groups are not usually found. At least three different lineages have colonized steep, dry, scree slopes independently of each other. Nasa urentivelutina comes from a urentivelutina comes from an otherwise exclusively mesophilic, forest-dwelling group (Nasa ser. Alalae, Weigend, 2000b). Nasa macrothyrsa and N. connectans and (Nasa ser. Carunculatae) represent a lineage that evidently arose from mesophilic Nasa ser. Saccatae. The endemic genus Xylopodia is closely related to the genus Klaprothia Kunth, which is primarily found in cloud forests. It is particularly striking that the colonization of dry habitats and concomitant morphological changes (coriaceous leaves, dense indument, underground storage structures) appear to have evolved in various plan t groups independently, both in Loasaceae (xylopodia in Xylopodia, indument in Nasa urentivelutina) and outside Loasaceae (storage roots in Caxamarca and Fuchsia pachyrrhiza P. Berry & B. A. Stein). We cannot be and Fuchsia pachyrrhiza P. Berry & B. A. Stein). We cannot be certain how to explain this striking convergence, but one conceivable scenario is that pockets of seasonally dry vegetation arose in relative isolation from older and more extensive arid vegetation (e.g., on the western slope of the Andes in central and southern Peru), so that in situ evolution of drought-tolerant taxa was possible in these unsaturated ecosystems.
Another habitat colonized by species of Nasa in this region is formed by the tropical deciduous forests. This vegetation type is usually free of Loasaceae, even where they are directly adjacent to moister forests with numerous species of Nasa (e.g., in the Sierra Nevada de Santa Marta and the Magdalena Valley in Colombia or on the western flank of the Andes in Ecuador). In the Amotape-Huancabamba Zone, these deciduous forests on the foothills of the Andes Zone, these deciduous forests on the foothills of the Andes are home to four endemic taxa of Nasa (three species and one subspecies), which are restricted to this habitat. Another striking example of the colonization of a new habitat is Nasa laxa from the region of Contumaza (Department of Cajamarca) of Nasa ser. Saccatoe. All of its close relatives are plants in disturbed sites, usually growing in full sun. Nasa laxa grows in deep shade under Podocarpus trees accompanied solely by shade-loving pteridophytes. This is a habitat where members of Nasa ser. Alat ae would be expected, but they are absent from the western slope of the Andes, so this could be another example of colonization of an unsaturated ecosystem.
Other ecological niches whose presence contributes to the species richness of the zone are found in the wide variety of soil types. The nutrient-poor, acidic substrates in the extensive stretches of white sands on the eastern slope of the Andes in this region are an effective dispersal barrier for Nasa (which is restricted to more or less fertile soils), facilitating allopatric speciation. Conversely, on the basis of my own observations, these sandy soils appear to be the preferred habitats of other plant groups--e.g., Burmanniaceae, Eriocaulaceae, and numerous Gentianaceae, such as Symbolanthus G. Don and Macrocarpaea (Griseb.) Gilg--and some of them--e.g., Passiflora anastomosans (Lambert exDC.) Killip of Passiflora sect. Taconia--appear tobe edaphic endemics.
H. MORPHOLOGICAL DIVERSIFICATION
Taxonomic diversification can lead either to taxa that differ only marginally or to taxa that differ dramatically in having altogether new character states. The former type of diversification is typical of the postglacial diversification of many plant groups in Europe (Rubus L., Alchemilla L., Hieracium L.)and is similarly found in Loasaceae in North America and Mexico (some groups in Mentzelia L.). The second type of diversification is what is mainly found in the Amotape-Huancabamba Zone. There are numerous characters in Loasaceae of this region that are not found elsewhere, such as sepals differing in size in Mentzelia heterosepala, balloon-shaped flowers in Nasa olmosiona, pseudostipules in the N. Stuebelii group, shrubby habit in various independent lineages, bicolorous petals (N. picta), and primary and secondary leaf veins visually set off from the lamina (white veins, N. driesslei Weigend).
Thus, the species and species groups in the Amotape-Huancabamba Zone are strongly diversified in morphology. This argues either for an old age of the taxa or for a dramatically accelerated morphological evolution. Evidence in Loasaceae indicates that both factors have contributed. The presence of some relict taxa (xylopodia, basal to the entire subfamily Loasoideae and known only from the Province of Contumaza) argues for the great age of the flora, whereas the presence of many vicariant species (N. peltata group, N. triphylla group) in forests that may have been isolated only for a comparatively short time (Dillon, 1994) argues for rapid evolutionary divergence. The formation of habitat fragments (most conspicuous in the relict forests) may have contributed to an accelerated evolution by character release in what must have been essentially an island-like situation.
The overall picture emerging from the data presented here is complex. The Amotape-Huancabamba Zone appears to be a phytochorion, in the sense that inclusion of its southern part into the Central Andes and its northern part into the Northern Andes would be unnatural. The zone, as such, is held together by various characteristic species and species groups and even endemic genera, which form close ties both along the Andes (north to south) and across the Andes (east to west).
The Huancabamba Depression itself has not acted as a major dispersal barrier and does not mark the distribution limits of northern and southern groups. Diversity in the zone is extremely high (six to eight times higher than in the Northern or Central Andes for the groups under investigation). Factors contributing to the high diversity are the overlap of northern and southern species and species groups and the narrow endemicity of most taxa. Historically, diversification was probably aided by the mosaic nature of the habitats and by the (repeated) isolation of habitat fragments. In spite of the likely dynamic history of the area, it has also been a refuge area for at least some phylogenetically (by Andean standards) old taxa, and certain habitat types must have been in existence for a considerable amount of time.
The discoveries of recent decades (in the case of Loasaceae, during the last few years) indicate that we are at best beginning to understand the patterns of diversity in this region of the Andes. The patterns of endemism across taxonomic groups currently reflect more the amount of recent research effort than differences in actual levels of diversity (see Hensold, 1999). The Amotoapc-Huancabamba Zone is still poorly known, and so are the adjacent regions to the Zone is still poorly known, and so are the adjacent regions to the north and the south on the eastern slope of the Andes and the upper reaches of the Maranon Valley. Well-documented collections are urgently required from this entire region.
A sizable part of Andean biodiversity seems to be concentrated into this relatively small area, which makes effective protection of the diverse habitats of this zone a high priority. The narrow endemicity of many taxa renders them vulnerable to habitat destruction and makes the creation of only a few large reserves a fairly futile exercise. A system of many comparatively small but efficiently managed reserves could preserve a sizable part of the biodiversity of this region.
IX. Appendix 1 Species and Species Groups of Loasaceae, with Their General Patterns of Diversity Amotape- Northern Taxa Huancabamba Andes shared Zone Gronovia scandens 1 1 1 Presliophytum - - 1 Xylopodia - - 1 Mentzelia hispida group 1 1 3 (a) Klaprothia 2 2 2 Mentzelia aspera 1 1 1 Caiophora 1 1 5 Nasa grandiflora group 7 - 2 Nasa cymbopetala group - - 5 Nasa magnifica group 1 (?) - 1 Nasa peltata group 5 - 2 Nasa ser. Carunculatae - - 2 Nasa ser. Saccatae (excl. Nasa 1 - 9 triphylla group) Nasa ser. Saccatae: Nasa triphylla 5 3 6 group - species Nasa ser. Saccatae: Nasa triphylla 7 - 9 group - subspecies Nasa ser. Alatae 12 1 8 Taxa total (and percentage of 44 10 (9%) 57 species shared by adjacent areas) Taxa Central shared Andes Gronovia scandens - - Presliophytum 1 3 Xylopodia - - Mentzelia hispida group 1 3 Klaprothia 2 2 Mentzelia aspera 1 1 Caiophora 2 [+ or -] 10 (b) Nasa grandiflora group - - Nasa cymbopetala group - - Nasa magnifica group - 1 Nasa peltata group - - Nasa ser. Carunculatae - 2 Nasa ser. Saccatae (excl. Nasa 2 11 triphylla group) Nasa ser. Saccatae: Nasa triphylla - - group - species Nasa ser. Saccatae: Nasa triphylla - - group - subspecies Nasa ser. Alatae - 3 Taxa total (and percentage of 9 (9%) 40 species shared by adjacent areas) (a)The widespread species M. chilensis, with ca. 3 endemic subspecies. (b)Caiophora has not been revised for the central and southern Andes; 10 species is a conservative estimate. Fig. 2 Species numbers of the genus Nasa (Loasaceae) along the Andean cordilleras. Central America 2 2 Colombia 10 20 Ecuador 10 29 Norhtern Peru 20 50 Southern Peru 16 11 Bolivia 1 2 Chile 1 1 Key: gray = species numbers previously known (pre-1997) black = species numbers currently known (1997-2000). Note: Table made from bar graph Table I Comparison of the barrier effect of the middle Maranon Valley and the Huancabamba Depression, respectively, in relation to the altitudinal distributions of species numbers of Loasaceae Maranon Valley Species found on both sides of the Maranon Valley (ca. 900 m) Calla Calla slope No. % Taxa growing above 1500m 10 3 20 Taxa growing below 1500m 2 2 100 Total 12 5 30 Abra de Gelig Taxa growing above 1500m 7 Taxa growing below 1500m 2 Total 9 Huancabamba Depression Species found on both sides of the Rio Chamaya- Abra de Porculla Cordilleras of (600-2145 m) Tabaconas and Huancabamba No. Taxa growing above 1500m 9 3 Taxa growing below 1500m 6 5 Total 15 8 Species found on both sides of the Rio Chamaya- Abra de Porculla (600-2145 m) Cutervo- Santa Cruz % region Taxa growing above 1500m 20 8 Taxa growing below 1500m 70 6 Total 38 14
My sincere gratitude goes to the following colleagues and friends who helped me in my field studies: Manuel Gonzales (Cajamarca, Peru); Eric Rodriguez R. (Trujillo, Peru); Katja Weigend (Berlin, Germany); and Harald Forther, Nicolas Dostert, Thassilo Franke, Michaela Binder, Anton Hofreiter, and Jurgen Skrabal (Munich, Germany). I deeply appreciate the numerous helpful suggestions on the manuscript by Nancy Hensold (Chicago, Illinois), W. Duellmann (Lawrence, Kansas), Jim Luteyn (Bronx, New York), Paul Berry (Madison, Wisconsin), Ken Young (Austin, Texas), and Jason Grant (Neuchatel, Switzerland). I also thank Asuncion Cano E. (USM, Lima) and Victor Quipuscoa (HUSA, Arequipa), for making collections for me, and H. Lunser (FU Berlin), for preparing the maps. The financial contributions of the Studienstiftung des Deutschen Volkes, the Lewis B. and Dorothy Cullman Program for Molecular Systematics Studies (The New York Botanical Garden), and the Deutscher Akademischer Austauschdienst are gratefully acknowledged.
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|Publication:||The Botanical Review|
|Article Type:||Statistical Data Included|
|Date:||Jan 1, 2002|
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