Biological spectrum and dispersal syndromes in an area of the semi-arid region of north-eastern Brazil

The biological spectrum and diaspores dispersal syndromes of the species recorded in a stretch of vegetation in a semi-arid region within the Cariri Environment Protection Area, Boa Vista, Paraíba State (northeast) Brazil, are described. Collections were made from fertile specimens, preferentially bearing fruit, over a 15-month period. Life forms and syndromes were determined by field observations using specialized literature. One hundred and sixty-six species, distributed into 123 genera and 41 families, were reported. Abiotic syndromes (autochory and anemochory) represented 69.7% of all syndromes identified, whilst 30.3% of the species were classified as zoochory. In the life form spectrum therophytes represented 27.7% of species, followed by smalland medium-sized phanerophytes (23.5%) and chamaephytes (22.3%). The occurrence of hemicryptophytes (9%), cryptophytes (0.6%) and species that could not be classified according to their life forms was also recorded (16.9%). Results showed that the biological spectrum and the dispersal syndromes are highly relevant to understand the structure and function of this phytocenose, with subsidies for the development of other studies in the semi-arid areas of northeastern Brazil.


Introduction
The strong seasonality in semi-arid regions requires that species adopt strategies for their survival during the driest periods.For instance, certain plant species adapt temporary life forms which produce vegetative buds that are protected until environmental conditions allow the development of the aerial parts (MANTOVANI; MARTINS, 1988).This close relationship between environmental conditions, prevalent life-forms and a given area has generated a system of vegetation classification based on the degree of protection of vegetative buds and their position on the plant's principal axis with regard to the substrate.
Proposed by Raunkiaer (1934), the system classifies plants according to forms used to protect their perennating buds during unfavorable seasons, and groups them into five main classes: therophytes, cryptophytes, hemicryptophytes, chamaephytes and phanerophytes, according to their different resistance strategies to environmental conditions.Studies carried out in the caatinga region have demonstrated the predominance of therophytes over other life forms, at a proportion close to 40%, as underscored by Costa et al. (2006) and Porto et al. (2008).A high proportion of phanerophytes and chamaephytes, close to 30 and 15%, respectively, were also registered.
Dispersal syndromes comprise a series of morphological characters of fruit or seeds that, associated with the biology of the disperser, determines a specific mode of dispersal, which in turn is an adaptation that promotes the establishment, development and endurance of the vegetative species in a given environment ( VAN DER PIJL, 1982;RENNER, 1987;VASCONCELOS et al., 2010).Fruiting and dispersal are important stages of the reproductive cycle of angiosperms, with the dispersal process being the most sensitive and critical stage in a plant life history (BAWA et al., 1989).
From an ecological viewpoint, the dispersal of diaspores is a process of great importance for plant species because it enables them to expand their area of occurrence, decreases intraspecies competition and allows increase of their genetic variability into the population (HOWE; MIRITI, 2004).Efficiency of the dispersal mode also translates into increased recruitment of seedlings, by reducing competition and predation of seeds (HOWE, 1993).
According to Van der Pijl (1982), the richness and spatial distribution of plant populations are determined by dispersal modes and the frequency the diaspores reach favorable locations for the establishment of seedlings.In this context, Terborgh et al. (2002) found that the geographic distribution patterns of species and community structures depended on interactions between the community´s biotic and abiotic components.The natural dispersal of diaspores has also an important role in the natural regeneration of plant ecosystems, enabling the recolonization of degraded areas (DEMINICIS et al., 2009).According to Gentry (1983), information on dispersal ecology represents an important step in the understanding of the structure and function of plant communities in Neotropical forests, as well as in the restoration of degraded areas.
The frequency of different dispersal strategies is influenced by several factors, among which water availability in the environment is prominent, as observed by Silva and Rodal (2009).
Data on the dispersal syndromes in semi-arid regions of northeast Brazil have been expanded over the last decade.Since the first studies it has been observed that anemochoric species predominate in dry forests, while in humid forests zoochory is more important (HOWE;SMALLWOOD, 1982;GENTRY, 1983).This pattern was also observed in studies conducted by Barbosa et al. (2002), Griz and Machado (2001) and Griz et al. (2002).
Current study describes the floristic biological spectrum and dispersal syndromes of the flora in a conservation area (the Cariri Environment Conservation Area) in the semi-arid region of the northeastern state of Paraíba, Brazil, to verify whether the syndromes of the studied area are similar to those registered in other areas of the Brazilian northeast Caatinga region.

Study area
Current study was developed on the Fazenda Salambaia, a rural area in the municipality of Boa Vista, in the central region of the Borborema plateau in the northeastern state of Paraíba, Brazil.According to Köeppen and Geiger (1928), the region's climate is Bshw or semi-arid hot climate, with a 8 -11-month dry season, an average temperature of 26°C and average annual rainfall not exceeding 600 mm (MOREIRA, 1988).The soils of the region are of the brown soil without calcium type, with dystrophic regosol areas (EMBRAPA, 2006).
The farm lies within the Cariri conservation area, specifically established to protect the scenic beauty of the region.The area comprises many rock formations where archaeological sites containing cave paintings and other records of prehistoric civilizations have been discovered.The vegetation of the studied area is characterized by sparse trees, shrubs and sappy thorny plants, or rather, predominantly dry shrub forest with xerophytic characteristics.Although it was not clear-cut in the last 20 years (according to information from a local resident), the local vegetation has been and is still impacted by goats, sheep and cattle grazing and trampling.

Field and laboratory procedures
Samples, collected every two weeks, between July 2010 and October 2011, consisted of fertile branches from individual trees, shrubs and herbaceous plants during walks through the area under analysis.After taxonomic identification, all species were classified by life form, according to a modified version (MUELLER-DOMBOIS; ELLENBERG, 1974) of Raunkiaer's (1934) classification system.So that the floristic biological spectrum of the vegetation could be determined, species were also classified according to fruit type, based on the morphological characteristics described by Van der Pijl (1982) and by Barroso et al. (1999), as well as the dispersal strategy adopted by each species, using specialized literature.The floristic list was prepared according to APG III ( 2009) and the species names and respective authors were verified in Forzza et al. (2014).
Following Van der Pijl (1982), the syndromes were classified into three groups: (a) zoochorous, when diaspores are dispersed by animals; for example, those with sweet flesh, and seeds with arils; species dispersed by insects, vertebrates and man are included in this group; (b) anemochorous, when the diaspores are adapted to wind dispersal, featuring structures such as feathers and wings; (c) autochorous, when the plants have their own dispersion mechanisms: seeds are either launched on the surrounding areas by any particular mechanism or they are simply released by the plant directly on the ground, or barochoric (gravity) which comprise species with explosive dispersal or dispersal by gravity.
Based on this dispersal syndrome classification, the community profile of a given area may be described according to the relative proportion of each dispersal strategy.The profile corresponds to the dispersion spectrum.However, it must be underscored that the object in current study is only the primary dispersal of diaspores.In other words, secondary events after departure from the parent plant were not observed.Following Barroso et al. (1999), a morphological classification of the fruit of the species that fruited during the period of data collection period was performed to characterize the syndromes.

Results
One hundred and sixty-six species, belonging to 123 genera and 41 families of angiosperms, were identified.Further, eight taxa were identified only at genus level and four taxa only at family level (Table 1).The richest family was Fabaceae, with 27 species recorded in this study.In terms of the floristic biological spectrum among the 166 species, therophytes (46) were predominant over other life forms, representing 27.7% of the total, whereas phanerophytes (39) and chamaephytes (37) respectively represented 23.5 and 22.3% (Figure 1).Fifteen species of hemicryptophytes have also been registered.They represent 9% of the cryptophytes species, or 0.6% of all the species recorded in the study area.The life form could not be determined in the remaining 28 species (16.9% of all recorded species).
When the dispersal modes of diaspores are taken into account (Figure 2), anemochorous is the predominant syndrome in the area, with 47 species, or 28.3% of total; followed by autochorous (43), or 25.9% of total, in which dispersal is the result of the plants' own mechanisms, such as explosive dehiscence of dry fruits or gravity.Only 39 species are zoochorous, with 23.5% of total.This factor depends on the activity of animals so that dispersal may occur within an adequate distance from the parent plant.Dispersal syndromes were not identified in 37, or 22.3% of the 166 species.This was due to the absence of fruit on the vegetative material collected which identified the type of fruit and consequently, the dispersal form adopted.
Twenty-two out of the 39 zoochorous species had fleshy fruit, such as the Cactaceae, whereas 17 species produced dry fruit, such as Boerhavia diffusa (Nyctaginaceae).Among the autochorous species, most had dry fruit, such as the Fabaceae species that produced legume or loment fruit types.All anemochorous species had dry fruits, featuring dispersal units (whether fruit or seeds) with tissue expansions such as wings or other structures that facilitated transport by wind, such as Serjania glabrata (Sapindaceae), Schinopsis brasiliensis (Anacardiaceae) and Cochlospermum vitifolium (Bixaceae).

Discussion
Results on dispersal syndromes show a predominance of abiotic vectors in dry areas and biotic vectors in more humid areas (FRANCKIE et al., 1974;HOWE;SMALLWOOD, 1982;GENTRY, 1983).According to the last author, there is a defined pattern in the frequency of dispersal syndromes where zoochory is the most frequent form in the species of Neotropical rainforests.This fact may be related to several factors, such as conditions of greater humidity and water availability in the environment, or the presence of different species of frugivorous animals, such as birds, rodents, bats and an array of invertebrate species, especially insects, that eat the fruit and disperse the seeds in the adjacent areas.In arid and semi-arid regions, the abiotic syndromes (anemochory and autochory) grow in importance, as several studies carried out on the caatinga have demonstrated (MACHADO et al., 1997;GRIZ;MACHADO, 2001;BARBOSA et al., 2002BARBOSA et al., , 2003)).In current study, the abiotic syndromes, autochory and anemochory, together represent 69.7% of the identified syndromes and corroborated the results of the previously mentioned investigations.
Acta Scientiarum.Biological Science Maringá, v. 37, n. 1, p. 91-100, Jan.-Mar., 2015  The pattern of dispersal syndromes is related to a greater frequency of dry fruit (dispersed on the ground by autochory or anemochory) in drier areas with marked seasonality, already detected in the Brazilian savannah (Cerrado) and reported by Batalha and Mantovani (2000), Figueiredo (2008) and Oliveira (1998).However, another study for the Cerrado by Costa et al. ( 2004) underscored a predominance of zoochorous species over other dispersal modes.
There is evidence that a gradual change in the dispersal spectrum exists, from humid areas, where the predominant species have zoochorous syndromes, to drier ones, where syndromes of autochory or anemochory are more common.The above has been reported by Silva and Rodal (2009) who documented the dispersal syndromes in three areas with different rainfall levels in northeast Brazil.Vicente et al. (2005) also registered differences in the frequencies of dispersal syndromes between humid and semi-arid locations.Barbosa et al. (2002) studied the phenology of woody species in the caatinga and reported the existence of a close relationship between the rainy season and the predominance of zoochorous species, whereas a higher percentage of autochorous and anemochorous species were reported in the dry season.According to Gentry (1983), differences in the amount and temporal distribution of rainfall are the most outstanding difference between wet and dry tropical forests, reflected in dispersal ecology.
Acta Scientiarum.Biological Science Maringá, v. 37, n. 1, p. 91-100, Jan.-Mar., 2015 In the case of the exclusive occurrence of smalland medium-sized phanerophytes in the studied area, similar data have been reported by Van Rooyen et al. (1990) for a semi-arid region in South Africa.According to these authors, the biological spectrum of species in an area indicates the survival strategy adopted by the local flora, while a high percentage of therophytes species represents an effective method for controlling water loss since the plant dies at the beginning of the dry season and avoids the water stress.Further, the seeds produced during its short life remain in the environment protected from desiccation by the seed coat and will grow when environmental conditions become favorable again, featuring an efficient escape strategy.
With regard to the life forms in the area under analysis, the therophytes form predominated and confirmed records in the literature showing the importance of this life form in the biological spectrum of other caatinga areas (ARAÚJO et al., 2005;RODAL et al., 2005;COSTA et al., 2006).It should be emphasized that the marked predominance of small-and medium-sized phanerophytes has been recorded in several studies on caatinga areas (ARAÚJO et al., 1995;ALCOFORADO-FILHO et al., 2003;FERRAZ et al., 2003).

Conclusion
Results of current investigation corroborate the few studies that address the biological spectrum and dispersal syndromes in caatinga areas and pointed the need for species to adopt strategies for their survival during the driest periods.It may also be inferred that both the biological spectrum and the dispersal syndromes are of fundamental importance for understanding the structure and function of this phytocenose and in particular the caatinga vegetation of northeast Brazil, perhaps one of the areas on the planet which is most threatened by anthropic action and yet one of the least known in terms of autoecology.

Figure 1 .
Figure 1.Percentage of life forms identified between species in the study area, Fazenda Salambaia, APA of Cariri, Paraíba State, Northeast, Brazil.Source: The authors.