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Contributions of Leguminosae to young and old stands of neotropical forests under different environmental conditions

Abstract

Key message

Potentially nodulating Leguminosae species had high density and biomass in young stands of forests in Northeast Brazil, except in a dry forest on a low-fertility soil.

Context

Leguminosae species, especially potentially nodulating ones, appear to be important components of tropical secondary forests, although information is still scarce concerning their contributions to richness and biomass under different environmental conditions.

Aims

To evaluate the contribution of Leguminosae to the aboveground biomass and density of young and old forest stands in six sites, with different climate and soil conditions, in northeastern Brazil.

Methods

The biomass of plants was estimated using allometric equations in ten plots in one young and one old forest stand in each site. Leguminosae were separated into nodulating and non-nodulating species based on literature.

Results

Leguminosae, mainly nodulating species, displayed the largest number of species among all families and the largest biomass and density in young stands. There was more similarity in Leguminosae species composition between young and old stands in dry than in humid forests.

Conclusion

Nodulating species make considerable contributions to the biomass of the initial successional stages of forests in Northeast Brazil — confirming the importance of the family for natural forest regeneration, especially in dry environments.

Introduction

Secondary forests are becoming predominant in the tropics as a result of the substitution of old-growth forests by crops and pastures and the eventual abandonment of these activities, leading to the natural regeneration of the native vegetation (Aide and Grau 2004; Arroyo-Rodríguez et al. 2017; FAO 2018). Leguminosae species are particularly abundant in secondary neotropical forests (Gei et al. 2018), in both dry (Lebrija-Trejos et al. 2008; Souza et al. 2012; Lopes et al. 2012) and humid regions (Aidar et al. 2001; Pereira et al. 2003; Oliveira-Filho et al. 2004; Romero-Duque et al. 2007; Guedes et al. 2012; Souza et al. 2012). The Leguminosae appear to have competitive advantages over the species of other families due to their symbiotic relationships with nitrogen-fixing bacteria, particularly in soils with low N availability (Freitas et al. 2010; Gei et al. 2018). As succession advances, the density of Leguminosae decreases in some areas (Oliveira et al. 2006; Álvarez-Yépiz et al. 2008), while remaining high in others (Souza et al. 2012; Cabral et al. 2013). No clear explanation has been provided for this difference, but it could be related to the ecological advantage of fixation, since in the areas where the density of Leguminosae remains high, the pioneer N-fixing species tended to be replaced by non-N-fixing species (Souza et al. 2012; Cabral et al. 2013).

The role of Leguminosae, especially potentially nodulating species, can vary not only along successional stages but also under different environmental conditions (Gehring et al. 2008; Gei et al. 2018). In general, total species richness tends to be higher, but the proportion of Leguminosae lower, in humid as compared to dry forests (Ferraz et al. 1998; Alcoforado-Filho et al. 2003; Valdez-Hernández et al. 2014). A higher proportion of Leguminosae plant density and stem basal areas has also been reported in dry than in humid forests (Lebrija-Trejos 2008; Valdez-Hernández et al. 2014; Gei et al. 2018). Dry tropical forests usually have higher soil N losses than humid forests, due to lower recycling in the plant-soil system, as evidenced by their higher soil and plant 15N signals (Amundson et al. 2003; Aranibar et al. 2004; Freitas et al. 2015), making N fixation especially advantageous under dry conditions (Gei et al. 2018). The importance of Leguminosae may also differ between forests growing in high- and low-fertility soils. Under low fertility, nutrients other than N may be more limiting, and N-fixing Leguminosae would have fewer ecological advantages (Vitousek et al. 2013; Freitas et al. 2015). However, there is little specific information available in terms of the proportions of Leguminosae and nodulating Leguminosae biomass in relation to the total taxa, particularly considering successional stage, type of climate, or soil fertility (Gehring et al. 2008; Souza et al. 2012; Gei et al. 2018).

Therefore, we addressed the following questions: (1) Are the species richness, plant density, and total aboveground biomass of Leguminosae greater in younger than in older forests? Our hypothesis is that Leguminosae, especially N-fixing species, dominate in initial successional stages. (2) Does the relative importance of Leguminosae in terms of species richness, plant density, and biomass differ under different climates? And does the stand age (successional stage) interact with climate? Our hypothesis is that Leguminosae presence is higher in forests in drier climates. (3) Are the richness, plant density, and biomass of Leguminosae species greater in forests growing on high-fertility soils than on low-fertility soils? Our hypothesis is that nutrient limitations (other than N) may restrict the advantages of N-fixing Leguminosae species growing in low-fertility soils, reducing their participation in the forest. And (4) is Leguminosae species composition different under diverse environmental conditions? Our hypothesis is that the adaptations of Leguminosae will lead to a larger dissimilarity of species composition between younger and older stands growing under humid as opposed to dry conditions.

Material and methods

Study area

The study was carried out in tropical forests in northeastern Brazil which are exposed to a wide range of environments and contain considerable diversity of species of the Leguminosae family. Rainfall decreases in an east to west direction, from the humid coastal zone to a sub-humid transition zone and to the semi-arid interior lands, where isolated montane areas have slightly higher rainfall than the surrounding areas (Table 1). The transition and semi-arid zones have a large diversity of soil types, with contrasting fertility of those derived from highly weathered sedimentary material and those less weathered soils derived from crystalline parent material. Regolithic Neosols and the Latosols of the sub-humid and semi-arid zones are typically low-fertility soils while Argisols and Luvisols have higher fertility levels (Sampaio 2010). The coastal zone was originally covered with humid forests, mostly substituted by sugarcane fields. The montane areas were also covered by humid forests, but only small forest patches remain. The sub-humid and semi-arid zones were mostly covered by thorny deciduous dry forests (known as caatinga), and about half of the area is still covered by native vegetation, mostly regenerating forests that are the fallow part of the prevalent slash and burn agricultural system (Sampaio 2010). In the Araripe plateau, with highly weathered and low-fertility soils, the vegetation is a non-thorny deciduous dry forest (known as carrasco), with some characteristics similar to those of savannas (cerrado). That heterogeneity also includes higher soil N losses in dry areas (Freitas et al. 2015), which could result in greater advantages for nitrogen-fixing Leguminosae species (despite the generally low soil N concentrations in all areas).

Table 1 Site characteristics of the different native tropical forest fragments of different ages studied in northeastern Brazil

Young and old stands of six native forest types were selected along an east-west transect approximately 560 km long in northeastern Brazil (7° 42′ 51.7″ S and 34° 59′ 35.4 W to 7° 19′ 25.5″ S and 40° 05′ 00.1″ W) (Table 1). The forest fragments selected (from east to west) correspond to (1) humid coastal forest, part of the Atlantic Forest; (2) sub-humid high-fertility forests typical of agreste caatinga; (3) sub-humid low-fertility sandy caatinga forest; (4) humid montane (Brejo) forest; (5) semi-arid high-fertility (sertão caatinga) forest; and (6) semi-arid low-fertility (Carrasco) forest (Fig. 1). Characteristics of the soils of the areas are listed in Appendix Table 4. Two different stands (between 0.3 and 17 km apart) were sampled in each area, one old and one young. Information concerning their ages and previous land uses were based on studies conducted in the areas and/or conversations with residents (Table 1).

Fig. 1
figure 1

Map of the study area with the distribution of young and old stands, along an east-west transect in Pernambuco state, Brazil

Ten 20 × 20 m plots were established along a single transect through each forest stand, with 10 m between plots. In the sub-humid and semi-arid forests, all living plants with stem diameters ≥ 3 cm at 1.3 m above ground level (DBH) in every plot (except for lianas and epiphytes) were identified and had their stem diameters measured. In cases of plants branching below 1.3 m, the diameters of all of their branches were measured, their areas were determined and summed, and the equivalent diameter of that sum was calculated. In the humid forests, the inclusion criterion for measuring the living plants was DBH ≥ 5 cm and the other procedures were the same adopted for the sub-humid and semi-arid forests.

Biomass calculation

The aboveground biomass of each plant was estimated by allometric equations, using DBH as the independent variable. The general biomass equation used for the sub-humid and semi-arid forests was that established by Sampaio and Silva (2005): biomass (kg) = 0.173DBH2.295(cm). The general equation of Chave et al. (2001) was used for humid forests: biomass (kg) = exp(−2.19 + 2.54LN(DAP(cm))).

Species identification

Botanical material from each species was collected for identification by specialists and/or by comparisons with specimens deposited in the Federal Rural University of Pernambuco herbarium (PEUFR). The scientific names of the species were confirmed by consulting the W3 Tropics database (www.tropicos.org). The current classification of the Leguminosae sub-families followed The Legume Phylogeny Working Group (LPWG 2017). The Leguminosae species were separated into potentially N-fixing (henceforth designated as nodulating or N-fixing species) and non-N-fixing species (non-nodulating species) based on information published for the species or, in case of the absence of species information, for their genera (Faria and Lima 1998; Gehring et al. 2005; Sprent 2009; Freitas et al. 2010, 2015).

Statistical analysis

We analyzed differences in the biomass and in the plant density of pooled, Leguminosae, and nodulating species between young and old stands across the study sites using an analysis of variance. The analyses were conducted considering a split-plot (nested) design, in which the main plots corresponded to the six sites and the split plots to the young and old stands in each site. The 10 plots of each stand were considered replicates, but in fact they were pseudo-replicates. Therefore, the differences between forests may be due not only to their different climate and soil characteristics but also to local unknown characteristics. The data were log-transformed to attend normality criteria. The means were compared by the LSD (least significant difference) Student test at a significance level of 0.05. Analyses were carried out using the split-plot function of the agricolae package of the R program (R Core Team 2020).

Results

Biomass and density

The total aboveground biomass in the young stands of all forests varied from 20 to 24 Mg ha−1, except in the humid coastal forest where it reached 124 Mg ha−1 (Fig. 2). The total aboveground biomass in the old stands varied from 28 to 68 Mg ha−1 in the sub-humid and semi-arid forests and from 227 to 273 Mg ha−1 in the humid coastal and montane forests, respectively. The total biomass was significantly higher in the old stands of most forests, but not in the two low-fertility (sub-humid and semi-arid) forests.

Fig. 2
figure 2

Nodulating Leguminosae (A), all Leguminosae (B), and all tree and large shrub species (C) biomass in young and old stands of tropical forests under different environmental conditions in Northeast Brazil. Bars topped by the same small letter, comparing young and old stands in the same forest, and by the same capital letter, comparing young or old stands of the different forests, are not significantly different by the LSD test at a 0.05 probability level

Leguminosae biomass was similar in both young and old stands, and among the different forest types, except for a higher biomass in the old stand of the montane forest (Fig. 2), partly contradicting our first three hypotheses. However, relative to total forest aboveground biomass (Fig. 2) and plant density (Fig. 3), the proportions of the Leguminosae in the young sub-humid and semi-arid stands were higher than in the young humid costal and montane stands, confirming our second hypothesis (Table 2). The proportions of Leguminosae biomass in old stands tended to be lower than in the young stands in four of the forests (13 to 68%) but were similar in the sub-humid high-fertility and montane forests, partially confirming our first hypothesis.

Fig. 3
figure 3

Nodulating Leguminosae (A), all Leguminosae (B), and all tree and large shrub species (C) plant density in young and old stands of tropical forests under different environmental conditions in Northeast Brazil. Bars topped by the same small letter, comparing young and old stands in the same forest, and by the same capital letter, comparing young or old stands of the different forests, are not significantly different by the LSD test at a 0.05 probability level

Table 2 Proportions (%) of nodulating species aboveground biomass and plant density in relation to those of all Leguminosae and all tree and large shrub species and proportion of Leguminosae in relation to all tree species in young and old stands of tropical forests under different environmental conditions in Northeast Brazil

Most of the Leguminosae in the young stands belonged to nodulating species (Fig. 2), representing between 74 and 99% of the Leguminosae biomass (except in the montane [29%] and in the semi-arid low-fertility forest [1%]) (Table 2). The biomass of those nodulating species did not significantly differ between young and old stands of sub-humid and semi-arid forests (0.2 to 19.5 Mg ha−1) but were higher in the young stands of the coastal forest (31 versus 7 Mg ha−1) and higher in the old stands of the montane forest (39 versus 2 Mg ha−1) (Fig. 2).

Species composition

Leguminosae comprised the highest number of species among all plant families present in each forest type (Table 3; Appendix Table 6), the humid forests containing more Leguminosae species than the sub-humid or semi-arid forests, following the overall pattern of higher total numbers of taxa. The old stands had more Leguminosae species more than the young stands, except in the sub-humid low-fertility forest, where both stands had only three Leguminosae species.

Table 3 Numbers of all families and species, all Leguminosae and nodulating Leguminosae species of trees and large shrubs in young and old stands of tropical forest under different environmental conditions in Northeast Brazil. Total of 10 plots (0.4 ha)

In the sub-humid and semi-arid forests, species of the mimosoid clade (former Mimosoideae) of the Caesalpinioideae sub-family corresponded to more than half of the species in all localities (Appendix Tables 5 and 6) and had the largest proportions of Leguminosae biomass. Most of the mimosoids belonged to the tribe Mimoseae. A single species of Papilionoideae, belonging to the tribe Swartzieae (Amburana cearensis (Allemão) A.C.Sm.), was present in the young stand of the semi-arid high-fertility forest. Of all Leguminosae species, only those of the mimosoid clade of the tribes Mimoseae and Ingeae have been referred to as capable of forming nodules with N-fixing bacteria (Appendix Table 5). In the semi-arid low-fertility forest, only the species of the tribes Ingeae (mimosoid clade), Sophoreae, and Swartzieae (Papilionoideae sub-family) were considered nodulating species.

In the young stand of the humid montane forest, however, the largest proportion of Leguminosae biomass belonged to Caesalpinioideae species outside the mimosoid clade (Appendix Tables 5 and 6). This difference in predominant clades in relation to the drier forests confirmed our fourth hypothesis. In the young stand of the humid coastal forest, the mimosoid clade comprised the largest number of species and the greatest biomass, followed by the Papilionoideae sub-family, with the mimosoid species belonging to the tribe Ingeae and the Papilionoideae species belonging to the tribes Dalbergieae, Sophoreae, and Swartzieae. All species or genera of mimosoid and Papilionoideae have been reported as nodulating. The tribes in the montane forest were almost identical to those in the coastal forest, although the genera differed in most cases. All mimosoid species, and two of the three species of Papilionoideae in the montane forest, have been considered nodulating.

In all young stands (except in the sub-humid high-fertility forest), the species with the highest plant density belonged to Leguminosae: Mimosa tenuiflora (Willd.) Poir in the sub-humid low-fertility and semi-arid high fertility forests, Senegalia langsdorffii (Benth.) Seigler & Ebinger in the semi-arid low-fertility forest, Inga ingoides (Rich.) Willd in the coastal forest, and Copaifera langsdorffii Desf. in the montane forest (Appendix Table 5). The dominant species (32%) in the young stand of the sub-humid high-fertility forest (Appendix Table 6) was Croton blanchetianus Baill. (Euphorbiaceae), followed by two Leguminosae: Piptadenia stipulacea (Benth.) Ducke and Poincianella pyramidalis (Tul.) LP Queiroz. Contrasting with those young stands, the highest density in all old stands belonged to non-Leguminosae species, except in the species-poor sub-humid low-fertility forest, where M. tenuiflora comprised 55% of all plants.

Discussion

Biomass and density

The biomass of the young stands of sub-humid and semi-arid forests were in the same range as those of other tropical dry forests throughout the world with up to 25 years of regeneration (17 to 31 Mg ha−1) (Becknell et al. 2012; Raharimalala et al. 2012; Rozendaal et al. 2017). The biomass of the old stands, however, was lower than those of most other dry forests, which usually had more than 72 Mg ha−1 (Read and Lawrence 2003; Raherison and Grouzis 2005; Vargas et al. 2008; Raharimalala et al. 2012; Becknell and Powers 2014). Low water availability is the probable cause of the low biomass in Brazilian dry forests, the closest to the equator with the highest potential evapotranspiration (Silva Filho et al. 2020). The biomass of the humid forests was within the ranges reported elsewhere (Fonseca et al. 2011; Poorter et al. 2016; Stas et al. 2017) for both young (76 to 100 Mg ha−1) and old stands (100 to 334 Mg ha−1), except for the low biomass of the young stand of the montane forest. The ranges were higher in humid forests than in dry forests, probably because of their greater water availability.

Our results with a high proportion of Leguminosae biomass and species richness in the sub-humid and semi-arid forests confirm the importance of the family in neotropical forests reported in previous studies (Aidar et al. 2001; Pereira et al. 2003; Oliveira-Filho et al. 2004; Romero-Duque et al. 2007; Lebrija-Trejos et al. 2008; Araújo et al. 2011; Crescencio et al. 2011; Souza et al. 2012; Guedes et al. 2012; Nascimento et al. 2014). High density and basal area proportions of Leguminosae plants have also been reported in other forests and tend to be higher in dry than in humid forests (Lebrija-Trejos et al. 2008; Valdez-Hernández et al. 2014; Gei et al. 2018). These results of basal area are similar to ours of biomass, which we estimated based on allometric equations using diameter as the independent variable.

The lower proportion of Leguminosae biomass in humid forests indicates that the family has a lower contribution to the forest stand where water is not limiting, partially confirming our second hypothesis. However, the absolute values of Leguminosae biomass were not lower in humid forests than in sub-humid and semi-arid forests, suggesting that greater water availability is not detrimental to Leguminosae. Higher water availability allows the establishment of more species, which together accumulate a higher total biomass. Higher species richness and aboveground biomass in humid than dry forests have been repeatedly reported, including those of Leguminosae (Lebrija-Trejos et al. 2008; Valdez-Hernández et al. 2014; Gei et al. 2018).

The low proportion of nodulating Leguminosae species in the semi-arid low-fertility forest indicates that N fixation is not a critical process in that environment, probably because of nutrient availability limitations, mainly phosphorus (Sampaio 2010). These low proportions confirm our third hypothesis. Most of the Leguminosae plants in this site were Senegalia langsdorffii, a non-nodulating species. Conversely, the high proportion of nodulating Leguminosae species found in most of the other forests suggests that N fixation is an important ecological process, especially in drier forests (Gei et al. 2018). However, data to support this hypothesis are scarce, highlighting the need of measurements of actual N fixation in tropical forest.

The similarities of the Leguminosae biomass between young and old forest stands (except the montane forests, where their biomass was higher in the old stand) lead to the conclusion that the family maintains its occupation of forest spaces even with advancing successional stages. That occupation may correspond to fewer plants with higher average biomass or greater numbers of plants with lower average biomass. The higher proportions of legume biomass in relation to the total biomass in young rather than old stands, however, do indicate that Leguminosae participation decreases along successional stages, confirming our first hypothesis. As the relative biomass and plant density of species other than N-fixing Leguminosae increase with age, it could be argued that N fixation during the initial successional stages increases N availability and allows other species to become established and prosper (Gehring et al. 2005; Sullivan et al. 2014; Gei et al. 2018).

In the humid forest, later successional species included other Leguminosae that eventually substituted pioneer species, while most of the Leguminosae species in the sub-humid and semi-arid forests were the same in both young and old stands. These later successional Leguminosae species could have N-fixation patterns different from those of the pioneer species of young stands, probably related to other environmental variables, such as shading. Detailed information concerning changes in N fixation along successional stages in tropical forests, however, remains scarce.

The probable initial ecological advantage of N fixation is corroborated by the lower biomass proportions of nodulating species in the old stands of some forests, although with two notable exceptions. The first refers to the semi-arid low-fertility forest, where N-fixing Leguminosae were almost absent in both young and old stands, probably due to phosphorous deficiencies (Sampaio 2010), confirming our third hypothesis. The second exception was the montane forest, where the old stand accumulated high total Leguminosae and N-fixing Leguminosae biomass, following initial slow growth. The cause of this slow growth, of similar magnitude as seen in young stands of drier forests, is not clear but could be related to the shallow, rocky montane soils. Larger proportions of nodulating species in young than in old stands have been reported in other Brazilian semi-arid forests (Pereira et al. 2003; Cabral et al. 2013), as well as in the Amazon Forest (Gehring et al. 2008). These articles confirm our results, but studies on other forests in Northeast Brazil with similar characteristics to those we analyzed are necessary to avoid the confounding effects of our pseudo-replications.

Species composition

Nodulating Leguminosae belonging only to the mimosoid clade of the Caesalpinioideae sub-family were observed in all forests. Although predominant, and comprising larger proportions of the total Leguminosae than in other tropical dry forests (Romero-Duque et al. 2007; Álvarez-Yépiz et al. 2008; Crescencio et al. 2011), mimosoid clade genera were different in the humid and the sub-humid and semi-arid forests, confirming our fourth hypothesis. The predominance of the mimosoid clade agrees with global observations that the highest proportions of nodulating species occur in this group, considering that the mimosoid clade is equivalent to the former Mimosoideae sub-family (LPWG 2017), with 90% of its species being potentially nodulant (Sprent 1995).

The Caesalpinieae and Cassieae (both Caesalpinioideae) species in all forests belonged to non-nodulating genera, although those tribes do have species with proven nodulation (Roggy et al. 1999; Sprent 2009). With only a few exceptions, the nodulating genera of those tribes occur in South America and are mostly represented by lianas, herbaceous, or small shrub species (Alcoforado-Filho et al. 2003; Sprent 2009; Freitas et al. 2012). Therefore, nodulating species of Caesalpinioideae outside of the mimosoid clade might have been found if other strata had been sampled in this study.

Conclusions

The high plant density and aboveground biomass of Leguminosae species confirm their high contribution to the forest growth in the initial stage of succession during the natural regeneration of neotropical forests. The lower relative density and biomass of the Leguminosae species in the humid than in the dry forests (27% or less versus 40 to 90%) indicate that the importance of Leguminosae is lower when water is not a limiting factor and plant richness is higher. Most of the Leguminosae in both young and old stands were potentially N-fixing species, except in the semi-arid low-fertility forest, indicating a possible ecological advantage of N fixation.

Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

The authors are grateful to Dr. André L.A. Lima, André L. Melo, and Rubens Queiroz for the logistical support and contribution to identifications of some plant specimens.

Funding

Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) provided the scholarship of the first author, and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; Processos 472997/2012-2 and 403129/2013-3) provided financial support.

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Correspondence to Tânia L. Costa.

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Contribution of the co-authors Tânia Lúcia da Costa (doctorate student) did the field sampling, analyzed and interpreted the data, and wrote the article. Everardo Valadares de Sá Barreto Sampaio and Ana Dolores Santiago de Freitas (advisers) designed the project, choose the sampling sites, and helped with data analysis and writing of the article. Aleksandro Ferreira da Silva (doctorate student) helped with field sampling and data analysis. Elcida de Lima Araújo (member of the advisory committee) participated in discussing and writing the article.

Appendix

Appendix

Table 4 Characteristics of the superficial soil layer in the sites where the study was conducted (0–20 cm)
Table 5 Density (plants ha−1) of Leguminosae species and indication of the nodulation potential of specie, in tropical forest fragments with different ages (Y young, O old) in the northeast of Brazil
Table 6 Number of individuals (n), total plant density (PD, plants ha−1), total aboveground biomass (B, Mg ha−1), and total basal area (BA, m2 ha−1) of species in tropical forest fragments with different ages in Northeast Brazil

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Costa, T.L., Sampaio, E.V.S.B., Araújo, E.L. et al. Contributions of Leguminosae to young and old stands of neotropical forests under different environmental conditions. Annals of Forest Science 78, 48 (2021). https://doi.org/10.1007/s13595-021-01065-0

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Keywords

  • Aboveground biomass
  • N-fixing species
  • Nodulation
  • Plant density
  • Species richness