Functional recovery of secondary tropical forests.

One-third of all Neotropical forests are secondary forests that regrow naturally after agricultural use through secondary succession. We need to understand better how and why succession varies across environmental gradients and broad geographic scales. Here, we analyze functional recovery using community data on seven plant characteristics (traits) of 1,016 forest plots from 30 chronosequence sites across the Neotropics. By analyzing communities in terms of their traits, we enhance understanding of the mechanisms of succession, assess ecosystem recovery, and use these insights to propose successful forest restoration strategies. Wet and dry forests diverged markedly for several traits that increase growth rate in wet forests but come at the expense of reduced drought tolerance, delay, or avoidance, which is important in seasonally dry forests. Dry and wet forests showed different successional pathways for several traits. In dry forests, species turnover is driven by drought tolerance traits that are important early in succession and in wet forests by shade tolerance traits that are important later in succession. In both forests, deciduous and compound-leaved trees decreased with forest age, probably because microclimatic conditions became less hot and dry. Our results suggest that climatic water availability drives functional recovery by influencing the start and trajectory of succession, resulting in a convergence of community trait values with forest age when vegetation cover builds up. Within plots, the range in functional trait values increased with age. Based on the observed successional trait changes, we indicate the consequences for carbon and nutrient cycling and propose an ecologically sound strategy to improve forest restoration success.

Does leaf flushing in the dry season affect leaf traits and herbivory in a tropical dry forest?

In tropical dry forests (TDFs), stem-succulent deciduous species produce leaves during the dry season which coincides with the period of lower herbivore abundance. In this study, we evaluated the effects of abiotic factors (precipitation and day length) on the vegetative phenology of three stem-succulent deciduous species (Cochlospermum vitifolium, Commiphora leptophloeos, and Manihot anomala) during 2 years. In addition, we compared leaf damage by herbivores and leaf defensive traits (specific leaf area, thickness, and content of phenolic compounds) on leaf cohorts produced before and during the rainy season by these stem-succulent deciduous species. We also evaluated herbivory and defensive traits on leaves produced during the rainy season by 14 non-succulent deciduous species. There was a positive effect of precipitation and day length on the amount of green leaves exhibited by the three stem-succulent species. The leaf cohort produced during the dry season by stem-succulent species showed lower leaf damage and content of phenolic compounds than the cohort produced during the rainy season by the same species and by non-succulent deciduous species. Leaf damage was only affected (positively) by the content of phenolic compounds, suggesting the production of induced defenses during leaf expansion. In general, herbivory levels were low in this study (0.57-6.37%) when compared with other TDFs, suggesting that a scape from herbivores due to anticipated leaf production is a weak selective force affecting plant fitness. These variations in leaf traits are mostly related to contrasting water conservation strategies among phenological groups. Further studies should evaluate other defensive and nutritional traits, as well as their variations along the leaf lifespan, to unravel herbivory patterns in TDFs.

Wet and dry tropical forests show opposite successional pathways in wood density but converge over time.

Tropical forests are converted at an alarming rate for agricultural use and pastureland, but also regrow naturally through secondary succession. For successful forest restoration, it is essential to understand the mechanisms of secondary succession. These mechanisms may vary across forest types, but analyses across broad spatial scales are lacking. Here, we analyse forest recovery using 1,403 plots that differ in age since agricultural abandonment from 50 sites across the Neotropics. We analyse changes in community composition using species-specific stem wood density (WD), which is a key trait for plant growth, survival and forest carbon storage. In wet forest, succession proceeds from low towards high community WD (acquisitive towards conservative trait values), in line with standard successional theory. However, in dry forest, succession proceeds from high towards low community WD (conservative towards acquisitive trait values), probably because high WD reflects drought tolerance in harsh early successional environments. Dry season intensity drives WD recovery by influencing the start and trajectory of succession, resulting in convergence of the community WD over time as vegetation cover builds up. These ecological insights can be used to improve species selection for reforestation. Reforestation species selected to establish a first protective canopy layer should, among other criteria, ideally have a similar WD to the early successional communities that dominate under the prevailing macroclimatic conditions.

Biodiversity recovery of Neotropical secondary forests.

Old-growth tropical forests harbor an immense diversity of tree species but are rapidly being cleared, while secondary forests that regrow on abandoned agricultural lands increase in extent. We assess how tree species richness and composition recover during secondary succession across gradients in environmental conditions and anthropogenic disturbance in an unprecedented multisite analysis for the Neotropics. Secondary forests recover remarkably fast in species richness but slowly in species composition. Secondary forests take a median time of five decades to recover the species richness of old-growth forest (80% recovery after 20 years) based on rarefaction analysis. Full recovery of species composition takes centuries (only 34% recovery after 20 years). A dual strategy that maintains both old-growth forests and species-rich secondary forests is therefore crucial for biodiversity conservation in human-modified tropical landscapes.

Understanding patterns of land-cover change in the Brazilian Cerrado from 2000 to 2015.

Clearing tropical vegetation impacts biodiversity, the provision of ecosystem services, and thus ultimately human welfare. We quantified changes in land cover from 2000 to 2015 across the Cerrado biome of northern Minas Gerais state, Brazil. We assessed the potential biophysical and socio-economic drivers of the loss of Cerrado, natural regeneration and net cover change at the municipality level. Further, we evaluated correlations between these land change variables and indicators of human welfare. We detected extensive land-cover changes in the study area, with the conversion of 23 446 km(2) and the natural regeneration of 13 926 km(2), resulting in a net loss of 9520 km(2) The annual net loss (-1.2% per year) of the cover of Cerrado is higher than that reported for the whole biome in similar periods. We argue that environmental and economic variables interact to underpin rates of conversion of Cerrado, most severely affecting more humid Cerrado lowlands. While rates of Cerrado regeneration are important for conservation strategies of the remaining biome, their integrity must be investigated given the likelihood of encroachment. Given the high frequency of land abandonment in tropical regions, secondary vegetation is fundamental to maintain biodiversity and ecosystem services. Finally, the impacts of Cerrado conversion on human welfare likely vary from local to regional scales, making it difficult to elaborate land-use policies based solely on socio-economic indicators.This article is part of the themed issue 'Tropical grassy biomes: linking ecology, human use and conservation'.

Carbon sequestration potential of second-growth forest regeneration in the Latin American tropics.

Regrowth of tropical secondary forests following complete or nearly complete removal of forest vegetation actively stores carbon in aboveground biomass, partially counterbalancing carbon emissions from deforestation, forest degradation, burning of fossil fuels, and other anthropogenic sources. We estimate the age and spatial extent of lowland second-growth forests in the Latin American tropics and model their potential aboveground carbon accumulation over four decades. Our model shows that, in 2008, second-growth forests (1 to 60 years old) covered 2.4 million km(2) of land (28.1% of the total study area). Over 40 years, these lands can potentially accumulate a total aboveground carbon stock of 8.48 Pg C (petagrams of carbon) in aboveground biomass via low-cost natural regeneration or assisted regeneration, corresponding to a total CO2 sequestration of 31.09 Pg CO2. This total is equivalent to carbon emissions from fossil fuel use and industrial processes in all of Latin America and the Caribbean from 1993 to 2014. Ten countries account for 95% of this carbon storage potential, led by Brazil, Colombia, Mexico, and Venezuela. We model future land-use scenarios to guide national carbon mitigation policies. Permitting natural regeneration on 40% of lowland pastures potentially stores an additional 2.0 Pg C over 40 years. Our study provides information and maps to guide national-level forest-based carbon mitigation plans on the basis of estimated rates of natural regeneration and pasture abandonment. Coupled with avoided deforestation and sustainable forest management, natural regeneration of second-growth forests provides a low-cost mechanism that yields a high carbon sequestration potential with multiple benefits for biodiversity and ecosystem services.

Biomass resilience of Neotropical secondary forests.

Land-use change occurs nowhere more rapidly than in the tropics, where the imbalance between deforestation and forest regrowth has large consequences for the global carbon cycle. However, considerable uncertainty remains about the rate of biomass recovery in secondary forests, and how these rates are influenced by climate, landscape, and prior land use. Here we analyse aboveground biomass recovery during secondary succession in 45 forest sites and about 1,500 forest plots covering the major environmental gradients in the Neotropics. The studied secondary forests are highly productive and resilient. Aboveground biomass recovery after 20 years was on average 122 megagrams per hectare (Mg ha(-1)), corresponding to a net carbon uptake of 3.05 Mg C ha(-1) yr(-1), 11 times the uptake rate of old-growth forests. Aboveground biomass stocks took a median time of 66 years to recover to 90% of old-growth values. Aboveground biomass recovery after 20 years varied 11.3-fold (from 20 to 225 Mg ha(-1)) across sites, and this recovery increased with water availability (higher local rainfall and lower climatic water deficit). We present a biomass recovery map of Latin America, which illustrates geographical and climatic variation in carbon sequestration potential during forest regrowth. The map will support policies to minimize forest loss in areas where biomass resilience is naturally low (such as seasonally dry forest regions) and promote forest regeneration and restoration in humid tropical lowland areas with high biomass resilience.

Phyllostomid bat occurrence in successional stages of neotropical dry forests.

Tropical dry forests (TDFs) are highly endangered tropical ecosystems being replaced by a complex mosaic of patches of different successional stages, agricultural fields and pasturelands. In this context, it is urgent to understand how taxa playing critical ecosystem roles respond to habitat modification. Because Phyllostomid bats provide important ecosystem services (e.g. facilitate gene flow among plant populations and promote forest regeneration), in this study we aimed to identify potential patterns on their response to TDF transformation in sites representing four different successional stages (initial, early, intermediate and late) in three Neotropical regions: México, Venezuela and Brazil. We evaluated bat occurrence at the species, ensemble (abundance) and assemblage level (species richness and composition, guild composition). We also evaluated how bat occurrence was modulated by the marked seasonality of TDFs. In general, we found high seasonal and regional specificities in phyllostomid occurrence, driven by specificities at species and guild levels. For example, highest frugivore abundance occurred in the early stage of the moistest TDF, while highest nectarivore abundance occurred in the same stage of the driest TDF. The high regional specificity of phyllostomid responses could arise from: (1) the distinctive environmental conditions of each region, (2) the specific behavior and ecological requirements of the regional bat species, (3) the composition, structure and phenological patterns of plant assemblages in the different stages, and (4) the regional landscape composition and configuration. We conclude that, in tropical seasonal environments, it is imperative to perform long-term studies considering seasonal variations in environmental conditions and plant phenology, as well as the role of landscape attributes. This approach will allow us to identify potential patterns in bat responses to habitat modification, which constitute an invaluable tool for not only bat biodiversity conservation but also for the conservation of the key ecological processes they provide.

Plant phenology and absence of sex-biased gall attack on three species of Baccharis.

BACKGROUND: Dioecy represents a source of variation in plant quality to herbivores due to sexual differences in intensity and timing of resource allocation to growth, defense and reproduction. Male plants have higher growth rates and should be more susceptible to herbivores than females, due to a lower investment in defense and reproduction. METHODOLOGY/PRINCIPAL FINDINGS: We compared resource investment to growth and reproduction and its consequences to herbivore attack on three Baccharis species along one year (B. dracunculifolia, B. ramosissima, and B. concinna). Phenological patterns presented by the three species of Baccharis were quite different over time, but the number of fourth-level shoots and plant growth rate did not differ between sexes in any studied species. Intersexual difference in reproductive investment was only observed for B. concinna, with female individuals supporting higher inflorescence density than male individuals throughout the year. Gall abundance on the three Baccharis species was not influenced by plant sex. However, all plant traits evaluated here positively influenced the gall abundance on B. concinna, whereas only the number of fourth-level shoots positively influenced gall abundance on B. ramosissima and B. dracunculifolia. CONCLUSIONS/SIGNIFICANCE: The absence of differential reproductive allocation may have contributed to similar growth and shoot production between the sexes, with bottom-up effects resulting in gender similarities in gall abundance patterns. The number of fourth-level shoots, an indicator of meristem availability to herbivores, was the most important driver of the abundance of the galling insects regardless of host plant gender or species. Albeit the absence of intersexual variation in insect gall abundance is uncommon in the literature, the detailed study of the exceptions may bring more light to understand the mechanisms and processes behind such trend.

Ontogenetic and temporal variations in herbivory and defense of Handroanthus spongiosus (Bignoniaceae) in a Brazilian tropical dry forest.

We compared the richness and abundance of free-feeding herbivore insects (sap-sucking and leaf-chewing), leaf herbivory damage, leaf toughness and total phenolic content between two ontogenetic stages (juvenile and reproductive) of Handroanthus spongiosus (Rizzini) S. O. Grose (Bignoniaceae) throughout the rainy season in a Brazilian seasonally dry tropical forest. Twenty marked individuals of H. spongiosus were sampled per ontogenetic stage in each period of the rainy season (beginning, middle, and end). Herbivore richness and abundance did not differ between ontogenetic stages, but higher percentage of leaf damage, higher concentration of phenolic compounds, and lower leaf toughness were observed for juvenile individuals. The greatest morphospecies abundance was found at the beginning of the rainy season, but folivory increment was higher at the end, despite the fact that leaf toughness and total phenolic content increased in the same period. No significant relationships between leaf damage and both total phenolic content and leaf toughness were observed. These results suggest that insect richness and abundance do not track changes in foliage quality throughout plant ontogeny, but their decrease along rainy season confirms what was predicted for tropical dry forests. The general trends described in the current study corroborate those described in the literature about herbivores and plant ontogeny. However, the lack of relationship between herbivore damage and the two plant attributes considered here indicates that the analyses of multiple defensive traits (the defense syndrome) must be more enlightening to determine the mechanisms driving temporal and spatial patterns of herbivore attack.

An experimental test of rainfall as a control agent of Glycaspis brimblecombei Moore (Hemiptera, Psyllidae) on seedlings of Eucalyptus camaldulensis Dehn (Myrtaceae)

An experimental test of rainfall as a control agent of Glycaspis brimblecombei Moore (Hemiptera, Psyllidae) on seedlings of Eucalyptus camaldulensis Dehn (Myrtaceae). Glycaspis brimblecombei is one the greatest threats to eucalyptus plantations in Brazil. The effects of rainfall to reduce the abundance of lerp of Glycaspis brimblecombei on experimentally infested seedlings of Eucalyptus camaldulensis were assessed. The number of lerps on the adaxial and abaxial surfaces of every leaf of 60 seedlings was recorded, before and after submission to the following treatments: "artificial rain", "leaf wetting" and control. A drastic reduction in lerp abundance per plant was observed after the treatments "leaf wetting" and artificial rain (F = 53.630; p < 0.001), whereas lerp abundance remained roughly constant in the control treatment along the experiment (F = 1.450; p = 0.232). At the end of the experiment, lerp abundance was significantly lower in both the "artificial rain" and "leaf wetting" than in the control treatment. Two days of rainfall simulation were sufficient to decrease more than 50% of the lerp population, with almost 100% of effectiveness after 5 days of experiment. Our results indicate that lerp solubilization and mechanical removal by water are potential tools to the population regulation of G. brimblecombei on E. camaldulensis seedlings.

Teste experimental da chuva como agente de controle de Glycaspis brimblecombei Moore (Hemiptera, Psyllidae) em mudas de Eucalyptus camaldulensis Dehn (Myrtaceae). Glycaspis brimblecombei é uma das maiores ameaças das plantações de eucalipto do Brasil. Foram avaliados os efeitos da água na redução da abundância de conchas desse inseto em mudas de Eucalyptus camaldulensis infestadas experimentalmente. Foi quantificado o número de conchas nas superfícies adaxial e abaxial de todas as folhas de 60 mudas, antes e após a aplicação dos seguintes tratamentos: "chuva artificial", "molhamento das folhas" e controle. Foi observada uma drástica redução na abundância de conchas nos tratamentos "chuva artificial" e "molhamento das folhas" (F = 53,630; p < 0,001), o que não ocorreu para o tratamento controle ao longo do experimento (F = 1,450; p = 0,232). Ao final do experimento, a abundância de conchas foi significativamente menor no tratamento "chuva artificial" e "molhamento das folhas" do que no tratamento controle. Dessa forma, dois dias de chuva mostraram ser eficientes para diminuir mais que 50% da população de conchas, com quase 100% de eficiência após 5 dias de experimento. Nossos resultados indicam que a solubilização das conchas e a remoção mecânica pela água são potenciais ferramentas para regulação populacional de G. brimblecombei em mudas de E. camaldulensis.

[Effects of landscape structure and Eucalyptus genotype on the abundance and biological control of Glycaspis brimblecombei Moore (Hemiptera: Psyllidae)]. / Efeito da estrutura da paisagem e do genótipo de Eucalyptus na abundância e controle biológico de Glycaspis brimblecombei Moore (Hemiptera: Psyllidae).

Glycaspis brimblecombei Moore is an Australian native pest of Eucalyptus detected in Brazil in 2003. Since then, it has spread fast and colonized plantations in several states of the country. This study aimed to investigate the influence of cerrado remnants on the abundance and biological control of G. brimblecombei. We placed yellow sticky card traps to capture insects in four plantations of hybrid clones of Eucalyptus urophylla x Eucalyptus grandis ('Urograndis') and four plantations of E. urophylla x Eucalyptus camaldulensis ('Urocam'). Traps were placed in three areas of these plantations: center, border with cerrado and border without cerrado. We also collected leaves from the same clones to estimate psyllid egg and lerp abundance. The abundance of G. brimblecombei was lower in the plantation-cerrado border, and the inverse pattern was observed for microhymenopterans. The leaf abaxial surface showed a higher abundance of eggs and nymphs, probably as a consequence of a lower parasitism rate and mechanical removal by wind and rain. Egg number was higher on Urograndis than in Urocam clones, but the number of psyllid lerps was higher in the latter. Thus, the establishment of first instars is probably a critical event to psyllid infestation, and these differences may be caused by morphological, anatomical and biochemical leaf features of distinct clones. Our results suggest that the maintenance of native vegetation around plantations is a promising management practice to promote the natural biological control of G.brimblecombei, a strategy that would also enhance the preservation of cerrado remnants.

Efeito da estrutura da paisagem e do genótipo de Eucalyptus na abundância e controle biológico de Glycaspis brimblecombei Moore (Hemiptera: Psyllidae) / Effects of landscape structure and Eucalyptus genotype on the abundance and biological control of Glycaspis brimblecombei Moore (Hemiptera: Psyllidae)

Glycaspis brimblecombei Moore is an Australian native pest of Eucalyptus detected in Brazil in 2003. Since then, it has spread fast and colonized plantations in several states of the country. This study aimed to investigate the influence of cerrado remnants on the abundance and biological control of G. brimblecombei. We placed yellow sticky card traps to capture insects in four plantations of hybrid clones of Eucalyptus urophylla x Eucalyptus grandis ("Urograndis") and four plantations of E. urophylla x Eucalyptus camaldulensis ("Urocam"). Traps were placed in three areas of these plantations: center, border with cerrado and border without cerrado. We also collected leaves from the same clones to estimate psyllid egg and lerp abundance. The abundance of G. brimblecombei was lower in the plantation-cerrado border, and the inverse pattern was observed for microhymenopterans. The leaf abaxial surface showed a higher abundance of eggs and nymphs, probably as a consequence of a lower parasitism rate and mechanical removal by wind and rain. Egg number was higher on Urograndis than in Urocam clones, but the number of psyllid lerps was higher in the latter. Thus, the establishment of first instars is probably a critical event to psyllid infestation, and these differences may be caused by morphological, anatomical and biochemical leaf features of distinct clones. Our results suggest that the maintenance of native vegetation around plantations is a promising management practice to promote the natural biological control of G.brimblecombei, a strategy that would also enhance the preservation of cerrado remnants.

[Influence of Atlantic Rain Forest remnants on the biological control of Euselasia apisaon (Dahman) (Lepidoptera: Riodinidae) by Trichogramma maxacalii (Voegelé e Pointel) (Hymenoptera: Trichogrammatidae)]. / Efeitos de remanescentes de Mata Atlântica no controle biológico de Euselasia apisaon (Dahman) (Lepidoptera: Riodinidae) por Trichogramma maxacalii (Voegelé e Pointel) (Hymenoptera: Trichogrammatidae).

This study evaluated the effects of Atlantic Rain Forest remnants on the natural biological control of Euselasia apisaon (Dahman) by the parasitoid Trichogramma maxacalii (Voegelé e Pointel) in Eucalyptus plantations. The number of E. apisaon eggs/leaf was higher in the center than in the edge of the plantations (23.5 +/- 7.61 vs. 14.8 +/- 3.14), but parasitism showed the reversed pattern (72.4% in the center and 80.5% in the edge). The results indicated that natural regulation exerted by T. maxacalii on populations of E. apisaon may be enhanced by the preservation of fragments of native vegetation surrounding Eucalyptus plantations.

Efeitos de remanescentes de Mata Atlântica no controle biológico de Euselasia apisaon (Dahman) (Lepidoptera: Riodinidae) por Trichogramma maxacalii (Voegelé e Pointel) (Hymenoptera: Trichogrammatidae) / Influence of Atlantic Rain Forest remnants on the biological control of Euselasia apisaon (Dahman) (Lepidoptera: Riodinidae) by Trichogramma maxacalii (Voegelé e Pointel) (Hymenoptera: Trichogrammatidae)

Este estudo avaliou os efeitos de remanescentes de Mata Atlântica no controle biológico natural de Euselasia apisaon (Dahman) pelo parasitóide Trichogramma maxacalii (Voegelé e Pointel) em plantios de Eucalyptus. O número de ovos de E. apisaon por folha foi maior no centro que nas bordas dos talhões (23,5 ± 7,61 versus 14,8 ± 3,14), mas o padrão inverso foi observado para as taxas de parasitismo (72,4 por cento no centro e 80,5 por cento na borda). Os resultados sugerem que a regulação natural de E. apisaon por T. maxacalii pode ser aumentada com a preservação de fragmentos de vegetação nativa no entorno de plantios de eucalipto.

This study evaluated the effects of Atlantic Rain Forest remnants on the natural biological control of Euselasia apisaon (Dahman) by the parasitoid Trichogramma maxacalii (Voegelé e Pointel) in Eucalyptus plantations. The number of E. apisaon eggs/leaf was higher in the center than in the edge of the plantations (23.5 ± 7.61 vs. 14.8 ± 3.14), but parasitism showed the reversed pattern (72.4 percent in the center and 80.5 percent in the edge). The results indicated that natural regulation exerted by T. maxacalii on populations of E. apisaon may be enhanced by the preservation of fragments of native vegetation surrounding Eucalyptus plantations.

Plant architecture and meristem dynamics as the mechanisms determining the diversity of gall-inducing insects.

Plant architecture is considered to affect herbivory intensity, but it is one of the least studied factors in plant-insect interactions, especially for gall-inducing insects. This study aimed to investigate the influence of plant architecture on the speciose fauna of gall-inducing insects associated with 17 species of Baccharis. Five architectural variables were evaluated: plant height, number of fourth-level shoots, biomass, average level and number of ramifications. The number of galling species associated with each host plant species was also determined. To test the effects of plant architecture on gall richness at the individual level, we used another data set where the number of fourth-level shoots and gall richness were determined for B. concinna, B. dracunculifolia, and B. ramosissima every 3 weeks during 1 year. The average similarity between host species based on gall fauna was low (9%), but plants with the same architectural pattern tended to support similar gall communities. The most important architectural trait influencing gall richness at the species level was the number of fourth-level shoots, which is indicative of the availability of plant meristems, a fundamental tissue for gall induction and development. This variable also showed a positive correlation with gall richness at the individual level. We propose that variations in gall richness among host species are driven by interspecific differences in plant architecture via availability of young, undifferentiated tissue, which is genetically controlled by the strength of the apical dominance. Plant architecture should have evolutionary consequences for gall communities, promoting insect radiation among architecturally similar plants through host shift and sympatric speciation. We also discuss the role of plant architecture in the global biogeography of gall-inducing insects.