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Do seedling functional groups reflect ecological strategies of woody plant species in Caatinga?

ABSTRACT

It is assumed that morphological traits of seedlings reflect different strategies in response to environmental conditions. The ecological significance of this has been widely documented in rainforests, where habitat structure and species interactions play an important role in community assembly. However, in seasonally dry ecosystems, where environmental filtering is expected to strongly influence community structure, this relationship is poorly understood. We investigated this relationship between functional groups of seedlings and life history traits and tested whether functional group predicts the ecological strategies employed by woody species to deal with the stressful conditions in seasonally dry ecosystems. Seedling functional groups, life history traits and traits that reflect ecological strategies for occupying seasonally dry environments were described for twenty-six plant species. Seedlings of species from the Caatinga vegetation exhibited a functional profile different from that observed in rainforests ecosystems. Phanerocotylar-epigeal seedlings were the most frequently observed groups, and had the largest range of ecological strategies related to dealing with seasonally dry environments, while phanerocotylar-hypogeal-reserve seedlings exhibited an increase in frequency with seasonality. We discuss these results in relation to those observed in other tropical forests and their ecological significance in seasonally dry environments.

Keywords:
dry forest; environmental filtering; functional traits; initial establishment; recruitment; seasonality

Introduction

Approaches using functional groups have been successfully used in ecology as effective methods for synthesising patterns within and among communities and for describing mechanisms related to abiotic factors and biotic interactions based on the morphological and physiological traits of species (Cornelissen 2003Cornelissen JHC, Lavorel S, Garnier E, et al. 2003. A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Australian Journal of Botany 51: 335-380.; Lavorel 2007Lavorel S, Díaz S, Cornelissen JHC, et al. 2007. Plant functional types: are we getting any closer to the holy grail? In: Canadell JG, Pataki D, Pitelka L. (eds.) Terrestrial ecosystems in a changing world. The IGBP Series. Berlin Heidelberg, Springer-Verlag. p. 149-164. ). Functional groups are defined as sets of species showing similar responses to environmental conditions, with similar effects on ecosystem functioning (Díaz & Cabido 2001Dı́az S, Cabido M. 2001. Vive la différence: plant functional diversity matters to ecosystem processes. Trends in Ecology & Evolution 16: 646-655.). This approach seems to be especially useful in simplifying the complexity of species-rich communities and to relate species traits and adaptive strategies for certain environmental conditions.

Earlier studies have suggested that the variation in seedlings’ cotyledon traits may reflect different establishment strategies among woody species (Vogel 1980Vogel EF. 1980. Seedlings of dicotyledons. Wageningen, Center for Agricultura Publishing and Documentation.; Garwood 1996Garwood NC. 1996. Functional morphology of tropical tree seedlings. In: Swaine MD. (ed.) The ecology of tropical forest tree seedlings. Man and the Biosfere Series. Vol. 18. Paris, Unesco/Parthenon. p. 59-129.). Seedling traits may play a role in the establishment of juveniles, since this stage is a critical phase in the life cycle and for the reproductive success of plants. Different systems have been proposed to classify seedling stages based on functional morphology (Ng 1978Ng FSP. 1978. Strategies of establishment in Malayan forest trees. In: Tomlison PB, Zimmerman MH. (eds.) Tropical trees as living systems. Cambridge, Cambridge University Press. p. 129-162. ; Vogel 1980Vogel EF. 1980. Seedlings of dicotyledons. Wageningen, Center for Agricultura Publishing and Documentation.; Miquel 1987Miquel S. 1987. Morfologie fonctionnelle de plantules d`species forestières Du Gabon (Functional morphology of forest species from Gabon). Bulletin du Muséum National d’Histoire Naturrelle 4: 101-121.). More recently, Garwood (1996Garwood NC. 1996. Functional morphology of tropical tree seedlings. In: Swaine MD. (ed.) The ecology of tropical forest tree seedlings. Man and the Biosfere Series. Vol. 18. Paris, Unesco/Parthenon. p. 59-129.) reviewed these systems and proposed a broader classification, combining three characteristics from cotyledons: exposure (phanerocotylar - exposed/ cryptocotylar - hidden), position (epigeal - hypocotyl developed with elevated cotyledon/ hypogeal - cotyledon under or at ground level) and texture (foliaceous - main function of photosynthesis/ reserve - fleshy). Such combinations include five possible morpho-functional groups of seedlings likely to occur in nature: Phanerocotylar-Epigeal-Foliaceous (PEF), Phanerocotylar-Epigeal-Reserve (PER), Phanerocotylar-Hypogeal-Reserve (PHR), Cryptocotylar-Epigeal-Reserve (CER) and Cryptocotylar-Hypogeal-Reserve (CHR).

Overall, these functional groups of seedlings can reflect the different strategies that plant species use for their initial establishment (Kitajima 1996Kitajima K. 1996. Cotyledon functional morphology, patterns of seed reserve utilization and regeneration niches of tropical tree seedlings. In: Swaine MD. (ed.) The ecology of tropical forest tree seedlings. Man and the Biosfere Series. Vol. 17. Paris, Unesco/Parthenon. p. 193-210.; Garwood 1996Garwood NC. 1996. Functional morphology of tropical tree seedlings. In: Swaine MD. (ed.) The ecology of tropical forest tree seedlings. Man and the Biosfere Series. Vol. 18. Paris, Unesco/Parthenon. p. 59-129.; Baraloto & Forget 2007Baraloto C, Forget PM. 2007. Seed size, seedling morphology, and response to deep shade and damage in neotropical rain forest trees. American Journal of Botany 94: 901-911). For example, PEF seedlings generally develop from small seeds with small reserves, thus resulting in quick development and rapid colonisation in the early stages of succession. In contrast, CHR seedlings generally come from large seeds with large reserves and slow development associated with later successional stages (Ng 1978Ng FSP. 1978. Strategies of establishment in Malayan forest trees. In: Tomlison PB, Zimmerman MH. (eds.) Tropical trees as living systems. Cambridge, Cambridge University Press. p. 129-162. ; Hladik & Miquel 1990Hladik A, Miquel S. 1990. Seedling types and plant establishment in an African Rain Forest. In: Bawa KS, Hadley M. (eds.) Reproductive ecology of tropical forest plants. Man and the Biosfere Series. Vol. 7. Paris, Unesco/Parthenon. p. 261-282.). Furthermore, groups of seedlings have different light requirements, with PEF seedlings able to grow fast in high light environments compared to CHR seedlings, which are more strongly associated with light-limited environments (Kitajima 1996Kitajima K. 1996. Cotyledon functional morphology, patterns of seed reserve utilization and regeneration niches of tropical tree seedlings. In: Swaine MD. (ed.) The ecology of tropical forest tree seedlings. Man and the Biosfere Series. Vol. 17. Paris, Unesco/Parthenon. p. 193-210.). Additionally, seedlings with foliaceous cotyledons grow faster than species with reserve-type cotyledons, but survival after disturbances like grazing is five times higher in hypogeal cotyledons (Baraloto & Forget 2007Baraloto C, Forget PM. 2007. Seed size, seedling morphology, and response to deep shade and damage in neotropical rain forest trees. American Journal of Botany 94: 901-911).

Previous studies have shown that there is evolutionary convergence at the community level worldwide in these seedling traits (Ibarra-Manríquez 2001Ibarra-Manríquez G, Ramos MM, Oyama K. 2001. Seedling functional types in lowland rain forest in Mexico. American Journal of Botany 88: 1801-1812.; Zanne et al. 2005Zanne AE, Chapman CA, Kitajima K. 2005. Evolutionary and ecological correlates of early seedling morphology in East African trees and shrubs. American Journal of Botany 92: 972-978.), and a higher frequency of PEF and CHR seedling groups in Neotropical rain forests and of PHR, CER, and PER groups in moist Paleotropical regions (Ibarra-Manríquez 2001). However, little is known regarding the patterns of these functional groups with respect to decreasing rainfall. Especially in environments that experience strong seasonality, where the most limiting resource becomes water availability instead of light, and the role of species interactions in modulating community assembly is assumed to be less strong than in wet forests.

In markedly seasonal environments, community assembly is likely to be mediated more by environmental filtering than by biotic interactions (Grime 2006Grime JP. 2006. Trait convergence and trait divergence in herbaceous plant communities: mechanisms and consequences. Journal of Vegetation Science 17: 255-260.). Consequently, in such areas some species’ functional traits tend to be more conservative and genetically fixed. These species are thus expected to vary less between ontogenetic stages, since trait variations caused by environmental conditions are greater than those caused by ontogeny (Fu et al. 2013Fu H, Yuan G, Zhong J, Cao T, Ni L, Xie P. 2013. Environmental and ontogenetic effects on intraspecific trait variation of a macrophyte species across five ecological scales. PLoS ONE 8: e62794 Doi: 10.1371/journal.pone.0062794.
https://doi.org/Doi: 10.1371/journal.pon...
). For example, some traits such as wood density, leaf matter dry content and water potential are more stable and, at least in respect to species’ rank, tend to be more consistent across ontogenetic stages (Kitajima & Poorter 2010Kitajima K, Poorter L. 2010. Tissue-level leaf toughness, but not lamina thickness, predicts sapling leaf lifespan and shade tolerance of tropical tree species. New Phytologist 186: 708-721. ). As a result, some plant traits can be useful for gaining a better understanding of the ability of species to successfully establish in environments with strong filtering forces.

In Brazil, studies involving the functional morphology of native plant seedlings are strictly limited to a few species from the Cerrado, the Atlantic Forest and the Amazon floodplain (Ressel et al. 2004Ressel K, Guilherme FAG, Schiavini I, Oliveira PE. 2004. Ecologia morfofuncional de plântulas de espécies arbóreas da Estação Ecológica do Panga, Uberlândia, Minas Gerais. Revista Brasileira de Botânica 27: 311-323.; Leonhardt et al. 2008Leonhardt C, Bueno OL, Calil AC, Busnello A, Rosa R. 2008. Morfologia e desenvolvimento de plântulas de 29 especiesarboreasnativas da área da Bacia Hidrográfica do Guaíba, Rio Grande do Sul. Ilheringia 63: 5-14.; Feitoza et al. 2014Feitoza GV, Santos JUM, Gurgel ESC, Oliveira DMT. 2014. Morphology of fruits, seeds, seedlings and saplings of three species of Macrolobium Schreb. (Leguminosae, Caesalpinioideae) in the Brazilian Amazon floodplain. Acta Botanica Brasilica 28: 422-433.). This information is even scarcer for dry tropical forests, with studies restricted to species of economic value and failing to address functional components (Cunha & Ferreira 2003Cunha NCL, Ferreira RA. 2003. Aspectos morfológicos de semente e do desenvolvimento da planta jovem de Amburana cearensis (Arr. Cam.) A. C. Smith - Cumaru - Leguminosae - Papilionoideae. Revista Brasileira de Sementes 25: 89-96.; Feliciano et al. 2008Feliciano ALP, Marangon LC, Holanda AC. 2008. Morfologia de sementes, de plântulas e de plantas jovens de aroeira (Myracrodruon urundeuva Allemão). Revista de Biologia e Ciências da Terra 8: 110-118.). Since plants respond to environmental factors through a series of morphological, physiological or phenological traits, which impact growth, reproduction and survival (Violle et al. 2007Violle C, Navas ML, Vile D, et al. 2007. Let the concept of trait be functional! Oikos 116: 882-892.), the seedling stage represents the most critical phases of a plant’s life cycle, and these can determine the regenerative processes in plant communities.

Here, we investigated the above mentioned associations between functional groups of seedlings and ecological strategies of plants in the Caatinga, a seasonally dry tropical forest in the northeast of Brazil. We predicted that favorable seasonally conditions for recruitment and growth for plant species recorded in this semi-arid region will play a preponderant role in the occurrence of different functional groups when compared to other tropical forests. To address these issues, we first investigated if functional groups of seedlings are related to features of the life histories of plants. Afterwards, we contrasted these functional groups of seedlings with plant traits that reflect the ecological strategies of plants with regard to markedly seasonal environments, and we compared the patterns found to those from other tropical forests.

Materials and methods

Study area

This study took place in the Mata da Pimenteira State Park (7°89’S 38°30’W), located near Serra Talhada municipality, Pernambuco state, northeastern Brazil. The nature reserve covers an area of about 887 ha of seasonally dry tropical forest, locally called Caatinga vegetation. In this semi-arid region, rainfall exhibits high interannual variability, with the majority of annual rainfall condensed into three months (Jan - Mar). Species in this region are predominantly deciduous, with over 90 % of individuals’ leaves falling during the dry season (ALA Lima unpubl. res.). According to the Köppen system the climate is BSwh', i.e. warm and dry with the rainy season occurring in the summer months. The annual rainfall is ca. 653 mm, with a mean temperature of 23.8 ± 0.92 ºC (Silva & Almeida 2013Silva TGF, Almeida AQ. 2013. Climatologia e Características geomorfológicas. In: Santos EM, Melo-Junior M, Silva-Cavalcanti JS, Almeida GVL.(orgs.) Parque Estadual Mata da Pimenteira: riqueza natural e conservação da Caatinga. Recife, EDUFRPE. p. 27-36. ). The annual evapotranspiration of 2000 mm far exceeds annual rainfall (Sampaio 1995Sampaio EVSB. 1995. Overview of the Brazilian Caatinga. In: Bullock SH, Mooney HA, Medina E. (eds.) Seasonally dry tropical forests. Cambridge, Cambridge University Press . p. 35-63.). Inside the nature reserve, soils are mainly of three classes: Litholic soils, Neossol soils and Cambisol soils (Silva & Almeida 2013Silva TGF, Almeida AQ. 2013. Climatologia e Características geomorfológicas. In: Santos EM, Melo-Junior M, Silva-Cavalcanti JS, Almeida GVL.(orgs.) Parque Estadual Mata da Pimenteira: riqueza natural e conservação da Caatinga. Recife, EDUFRPE. p. 27-36. ).

Data collection

We collected diaspores of woody species from July 2009 to July 2011, and obtained phenological information on northeast dry forests from the literature (Griz & Machado 2001Griz LMS, Machado IC. 2001. Fruiting phenology and seed dispersal syndromes in Caatinga, a tropical dry Forest in the northeast of Brazil. Journal of Tropical Ecology 17: 303-321.; Lima & Rodal 2010Lima ALA, Rodal MJN. 2010. Phenology and wood density of plants growing in the semi-arid region of northeastern Brazil. Journal of Arid Environments 74: 1363-1373.). Woody species were defined based on a previously phytosociological survey in this study area (Farias et al. 2016Farias SGG, Rodal MJN, Melo AL, Silva MAM, Lima ALA. 2016. Fisionomia e estrutura de vegetação de caatinga em diferentes ambientes em Serra talhada - Pernambuco. Ciência Florestal 26: 435-448.). Diaspores were manually collected, packed in plastic bags and taken to the laboratory, where seeds were then removed and germinated immediately. Twenty seeds from each species were planted in trays containing a mixture of sand and organic compost at a ratio of 1:1. The samples were maintained under the ambient conditions and were watered daily. We monitored all seedlings until they had at least one pair of protophilus (first true leaves); we then collected and dried them in a drying oven.

Next, we classified the seedlings into morphological and functional groups following Garwood (1996Garwood NC. 1996. Functional morphology of tropical tree seedlings. In: Swaine MD. (ed.) The ecology of tropical forest tree seedlings. Man and the Biosfere Series. Vol. 18. Paris, Unesco/Parthenon. p. 59-129.). This classification used ecologically important cotyledon features, such as exposure (phanerocotylar or cryptocotylar), position (epigeal or hypogeal) and function (foliaceous or reserve storage) to determine five functional groups of seedlings: phanerocotylar epigeal with foliaceous cotyledons (PEF), phanerocotylar epigeal with reserve storage cotyledons (PER), phanerocotylar hypogeal with reserve storage cotyledons (PHR), cryptocotylar hypogeal with reserve storage cotyledons (CHR) and cryptocotylar epigeal with reserve storage cotyledons (CER).

Additionally, we classified plant species according to their dispersion mode as autochoric; anemochoric and zoochoric (Pijl 1982Pijl L. 1982. Principles of dispersal in higher plants. 3rd. edn. New York, Springer Verlag.). The seed size was divided into four size classes: < 0.5 cm; 0.5 - 1.0 cm; 1.1 - 2.0 cm; > 2 cm (adapted from Miquel 1987Miquel S. 1987. Morfologie fonctionnelle de plantules d`species forestières Du Gabon (Functional morphology of forest species from Gabon). Bulletin du Muséum National d’Histoire Naturrelle 4: 101-121.). Ecological traits related to ecological strategies for dealing with seasonal environmental conditions were obtained from previous studies performed in the same study area. Maximum height was obtained from Farias et al. (2016Farias SGG, Rodal MJN, Melo AL, Silva MAM, Lima ALA. 2016. Fisionomia e estrutura de vegetação de caatinga em diferentes ambientes em Serra talhada - Pernambuco. Ciência Florestal 26: 435-448.), while leaf lifespan, wood density and water potential in the dry season were obtained from Lima et al. (2012Lima ALA, Sampaio EVSB, Castro CC, Rodal MJN, Antonino ACD, Melo AL. 2012. Do the phenology and functional stem attributes of woody species allow for the identification of functional groups in the semiarid region of Brazil? Trees 26: 1605-1616.).

Data analysis

We used an Analysis of Similarity (ANOSIM) to test if the functional groups of seedlings were related to life history traits (seed size, habit and dispersion mode) of species and used a Nonlinear Multidimensional Scaling (NMDS) ordination based on 1000 permutations to visualise these relationships. We also conducted a Principal Component Analysis (PCA) to evaluate if seedling functional groups are related to plant traits (water potential, wood density, leaf lifespan and maximum height) which reflect ecological responses to environmental conditions. Plant trait values were log10-transformed to standardise and to normalise these variables. Additionally, we used linear regression to test whether the spectrum of seedling groups varied with rainfall conditions (a component of environmental filtering) comparing the frequency of seedlings’ functional groups recorded in different forests with the annual rainfall range. All analyses were performed using R software (R Development Core Team 2016R Development Core Team. 2016. R: Language and Environment for Statistical Computing. Vienna, R Foundation for Statistical Computing. http://www.R-project.org.
http://www.R-project.org...
).

Results

Seedlings from 26 species belonging to 24 genera and ten families were recorded (Tab.1). This value represents 53 % of the number of woody species registered in the Caatinga vegetation of the Mata da Pimenteira State Park. The families with the highest number of species were Fabaceae (eight), Euphorbiaceae (four) and Malvaceae (three), which are the most representative families in the Caatinga ecosystem (Moro et al. 2014Moro MF, Lughadha EN, Filer DL, Araújo FS, Martins FR. 2014. A catalogue of the vascular plants of the Caatinga phytogeographical domain: a synthesis of floristic and phytosociological surveys. Phytotaxa 160: 1-18.). PEF seedlings were the most prevalent functional group, recorded for 52 % of species, followed by 24 % PER seedlings and 16 % PHR seedlings from total number of species. CHR seedlings showed the lowest proportion, representing only 8 % of the woody seedlings studied. Among the five possible functional groups likely to occur, CER was the only group not registered.

Table 1
Functional groups of 26 species of woody plants from Caatinga vegetation in the Mata da Pimenteira State Park, Brazil. Followed by seed size (1: < 0.5 cm; 2: 0.5 - 1.0 cm; 3: 1 - 2 cm; 4: > 2 cm.), dispersal mode (ane - anemochoric; auto - autochorous; zoo - zoochorous); habit (T: tree; S: shrub) of each species. Functional group: PEF - Phanerocotylar Epigeal Foliaceous; PER - Phanerocotylar Epigeal with Reserve; PHR - Phanerocotylar Hypogeal with Reserve, CHR - Cryptocotylar Hypogeal with Reserve.

We found no grouping in relation to functional groups of seedlings and species life cycle traits, such as seed size, habit and dispersal mode (R = 0.01, p = 0.42, Fig. 1). However, the functional classification of seedlings was related to the range of strategies exhibited by plant species to deal with stressful environmental conditions, where PEF seedlings showed the highest range of variation, followed by PER and PHR seedlings, respectively (Fig. 2). The first three axes of the PCA analysis explained 91.1 % of data variation. The first axis explained 43.0 % while the second and third explained 26.4 % and 21.7 %, respectively. The water potential in the dry season and the wood density traits were correlated with the first axis, the leaf lifespan with the second axis and the maximum height with the third axis.

Figure 1
Non-metric multidimensional scaling (NMDS) based on life history traits (seed size, dispersal mode and habit) showing the relationships between functional groups of seedlings among woody species recorded in the Mata da Pimenteira State Park, NE Brazil. Functional groups: PEF - Phanerocotylar Epigeal Foliaceous; PER - Phanerocotylar Epigeal with Reserve; PHR - Phanerocotylar Hypogeal with Reserve; CHR - Cryptocotylar Hypogeal with Reserve. Species: Amb_cea = Amburana cearesis, Ana_col = Anadenanthera colubrina, Ann_lep = Annona leptopetala, Asp_pyr = Aspidosperma pyrifolium, Bau_che = Bauhinia cheilantha, Com_lep = Commiphora leptophloeos, Cro_rha = Croton rhamnifolioides, Cyn_fle = Cynophalla flexuosa, Myr_uru = Myracrodruon urundeuva, Pip_sti = Piptadenia stipulacea, Poi_pyr = Poincianella pyramidalis, Pse_mar = Pseudobombax marginatum, Sap_gla = Sapium glandulosum, Seb_mac = Sebastiania macrocarpa, Spo_tub = Spondias tuberosa, Ziz_joa = Ziziphus joazeiro.

Figure 2
Principal Component Analysis showing plant species recorded in the Mata da Pimenteira State Park, NE Brazil, and their association with seed size, maximum height, leaf lifespan, wood density and water potential in the dry season and seedling functional groups. Functional groups: PEF - Phanerocotylar Epigeal Foliaceous; PER - Phanerocotylar Epigeal with Reserve; PHR - Phanerocotylar Hypogeal with Reserve. Plant Species: ssp1 = Amburana cearesis, ssp2 = Anadenanthera colubrina, ssp3 = Annona leptopetala, ssp4 = Aspidosperma pyrifolium, ssp5 = Bauhinia cheilantha, ssp6 = Commiphora leptophloeos, ssp7 = Croton rhamnifolioides, ssp8 = Cynophalla flexuosa, ssp9 = Myracrodruon urundeuva, ssp10 = Piptadenia stipulacea, ssp11 = Poincianella pyramidalis, ssp12 = Pseudobombax marginatum, ssp13 = Sapium glandulosum, ssp14 = Sebastiania macrocarpa, ssp15 = Spondias tuberosa, ssp16 = Ziziphus joazeiro.

The frequency of functional groups of seedlings varied in function of annual rainfall (R2 = 0.77, F = 10.59, p < 0.04, Tab. 2). The frequency of PER seedlings increased rainfall decreased, whereas CHR seedlings showed the opposite tendency.

Table 2
Percentage of morphofunctional groups between forest types according to rainfall (modified Ibarra-Manríquez 2001Ibarra-Manríquez G, Ramos MM, Oyama K. 2001. Seedling functional types in lowland rain forest in Mexico. American Journal of Botany 88: 1801-1812. increased by Ressel 2004Ressel K, Guilherme FAG, Schiavini I, Oliveira PE. 2004. Ecologia morfofuncional de plântulas de espécies arbóreas da Estação Ecológica do Panga, Uberlândia, Minas Gerais. Revista Brasileira de Botânica 27: 311-323. and this study). PEF - Phanerocotylar Epigeal Foliaceous; PHR - Phanerocotylar Hypogeal with Reserve; PER - Phanerocotylar Epigeal with Reserve; CHR - Cryptocotylar Hypogeal with Reserve; CER - Cryptocotylar Epigeal with Reserve; N - number of seedlings recorded in the representative value 50 to 75 % of the total woody flora in the site.

Discussion

We investigated the relationship between functional groups of seedlings - which are assumed to reflect strategies associated with seedling establishment - and species’ life history and plant functional traits associated with seasonal ecosystems. We found no pattern between functional groups of seedlings and plants’ life history traits. The absence of a relationship, especially between functional groups and seed size, may be due to the low frequency of CHR seedlings in the Caatinga vegetation. This functional group usually exhibits large seeds, with large reserves and slow development associated with the high capacity to survive in competitive environments, and thus these seedlings are less likely to be successful in the presence of strong abiotic restrictions such as those found in this semi-arid region.

In contrast, seedling functional groups were related to a range of plant functional traits that express ecological strategies to cope with drought conditions. Seedlings with protected cotyledon and reserve storage had a smaller range of values of traits related to ecological strategies, which indicates that these species are more similar in their environmental requirements and abilities to deal with variation in abiotic conditions. Instead, species that have exposed cotyledons during germination presented a broad variation of traits, which are represented by species with quick development, fast colonisation and growth rates. Such strategies are likely to be an important factor in dealing with a short growing season as experienced by plant species in seasonally dry tropical forests.

PEF and PER seedlings were the most frequent, differing from other Neotropical forests (Ibarra-Manríquez 2001Ibarra-Manríquez G, Ramos MM, Oyama K. 2001. Seedling functional types in lowland rain forest in Mexico. American Journal of Botany 88: 1801-1812.) where CHR seedlings represent a high proportion of species together with PEF, which always display the highest frequency. It is likely that this difference is due to differences in rainfall regimes, which can impose strong environmental filtering in the case of seasonal environments such as the Caatinga ecosystem. For instance, CHR seedlings are exceptionally frequent in forests with annual rainfall greater than 1500 mm (Garwood 1996Garwood NC. 1996. Functional morphology of tropical tree seedlings. In: Swaine MD. (ed.) The ecology of tropical forest tree seedlings. Man and the Biosfere Series. Vol. 18. Paris, Unesco/Parthenon. p. 59-129.) where habitat conditions confer an advantage to species with high competitive capacities. In contrast, we found that PEF and PER seedlings were the most successful at coping with broad differences in water availability, which may represent an important adaptive strategy for seasonally dry tropical forests.

Although this classification based on cotyledon types resulted in a categorical division of functional groups, the distinction between photosynthetic and storage cotyledons is not completely dichotomous, except for cryptogeal species, where the cotyledons are for storage only (Kidson & Westoby 2000Kidson R, Westoby M. 2000. Seed mass and seedling dimensions in relation to seedling establishment. Oecologia 125: 11-17.). For phanerocotylar epigeal species - those in which the cotyledons are exposed and located above the ground, as occurs in PEF and PER seedlings - storage and photosynthetic functions showed a continuous across species (Kidson & Westoby 2000Kidson R, Westoby M. 2000. Seed mass and seedling dimensions in relation to seedling establishment. Oecologia 125: 11-17.). It is likely that this is related to a broad range of strategies and niches, manifested by these groups as traits related to survival and be successful in varied conditions of the semi-arid region, as highlighted in PCA analysis.

Our analysis of seedling functional profile across sites with different average rainfalls showed an increase in PHR seedling with decreasing rainfall, while CHR seedlings showed the opposite tendency. It seems that the phanerocotylar strategy is an interesting mechanism by which such seedlings are exposed to the brief favourable environmental conditions in which their cotyledon can support an additional role in photosynthesis. In fact, Fabaceae, Euphorbiaceae and Malvaceae, the most common families recorded here and in the Caatinga ecosystem as a whole (Moro et al. 2014Moro MF, Lughadha EN, Filer DL, Araújo FS, Martins FR. 2014. A catalogue of the vascular plants of the Caatinga phytogeographical domain: a synthesis of floristic and phytosociological surveys. Phytotaxa 160: 1-18.), only presented species with phanerocotylar seedlings. Functional groups of seedlings were generally conserved within these families. Both Malvaceae and Euphorbiaceae exhibited only PEF seedlings, which suggests that species of these families are good initial colonizers and opportunists, as they grow rapidly during the rainy season. Fabaceae, which is the most diverse family in dry forests (Gentry 1995Gentry AH. 1995. Diversity and floristic composition of neotropical dry forests. In: Mooney HA, Bullock SH, Medina E. (eds.) Dry tropical forests. Cambridge, Cambridge University Press. p. 146-194.; Moro et al. 2014Moro MF, Lughadha EN, Filer DL, Araújo FS, Martins FR. 2014. A catalogue of the vascular plants of the Caatinga phytogeographical domain: a synthesis of floristic and phytosociological surveys. Phytotaxa 160: 1-18.; Vargas et al. 2015Vargas GG, Werden LK, Powers JS. 2015. Explaining legume success in tropical dry forests based on seed germination niches: a new hypothesis. Biotropica 47: 277-280.), showed PHR and PER seedlings in equal proportion. The fact that all species of this family have seedlings with reserves indicates a certain level of tolerance to highly varied and unpredictable climatic conditions, which is evidence of why this lineage is so successful in seasonally dry environments. Moreover, phanerocotyledons vary their position at several levels, conferring different strategies to species of this family, which may help Fabaceae species to occupy different niches in such environment.

Our findings provide broader knowledge regarding functional groups of seedlings, showing that the variation in frequency of these groups depends on annual water availability, which can reflect the role of environmental filtering as an important driver of assembly rules in seasonally dry tropical forests. Also, the most frequent functional groups exhibited a broad variation in plant traits, indicating that such groups could be related to survival in seasonally marked conditions such as those found in the Caatinga ecosystem. Future studies should focus on how these functional groups response to intra and inter-annual variation of rainfall in seasonally dry tropical forests to address the effects of seasonality driving changes at population and community levels. Furthermore, research efforts should be devoted to the dynamics of change in these strategies along gradients of seasonality and rainfall within the Caatinga ecosystem, which may assist in predicting plant species behaviour with regard to ongoing climate change.

Acknowledgements

We thank the Universidade Federal Rural de Pernambuco (UFRPE) for providing the scientific initiation scholarship granted to the first author.

References

  • Baraloto C, Forget PM. 2007. Seed size, seedling morphology, and response to deep shade and damage in neotropical rain forest trees. American Journal of Botany 94: 901-911
  • Cornelissen JHC, Lavorel S, Garnier E, et al 2003. A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Australian Journal of Botany 51: 335-380.
  • Cunha NCL, Ferreira RA. 2003. Aspectos morfológicos de semente e do desenvolvimento da planta jovem de Amburana cearensis (Arr. Cam.) A. C. Smith - Cumaru - Leguminosae - Papilionoideae. Revista Brasileira de Sementes 25: 89-96.
  • Dı́az S, Cabido M. 2001. Vive la différence: plant functional diversity matters to ecosystem processes. Trends in Ecology & Evolution 16: 646-655.
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Publication Dates

  • Publication in this collection
    06 Nov 2017
  • Date of issue
    Jan-Mar 2018

History

  • Received
    22 May 2017
  • Accepted
    15 Aug 2017
Sociedade Botânica do Brasil SCLN 307 - Bloco B - Sala 218 - Ed. Constrol Center Asa Norte CEP: 70746-520 Brasília/DF. - Alta Floresta - MT - Brazil
E-mail: acta@botanica.org.br