RESUMO
Tropical forests are global biodiversity hotspots and are crucial in the global carbon (C) cycle. Understanding the drivers of aboveground carbon stock (AGC) in a heterogeneous and biodiverse system can shed light on the processes underlying the relationship between biodiversity and carbon accumulation. Here, we investigate how biodiversity, environment, and landscape structure affect AGC. We examined such associations in 349 plots comprising over 95,346 km2 the Atlantic Forest of southern Brazil, encompassing three forest types: Dense Ombrophylous Forest (DF), Mixed Ombrophylous Forest (MF), and Seasonal Deciduous Forest (SF). Each plot was described by environmental variables, landscape metrics, and biodiversity (species richness and functional diversity). We used diversity, environmental, and landscape variables to build generalized linear mixed models and understand which can affect the forest AGC. We found that species richness is associated positively with AGC in all forest types, combined and separately. Seasonal temperature and isothermality affect AGC in all forest types; additionally, stocks are positively influenced by annual precipitation in SF and isothermality in MF. Among landscape metrics, total fragment edge negatively affects carbon stocks in MF. Our results show the importance of species diversity for carbon stocks in subtropical forests. The climate effect was also relevant, showing the importance of these factors, especially in a world where climate change tends to affect forest stock capacity negatively.
Assuntos
Biodiversidade , Carbono , Florestas , Brasil , Carbono/análise , Mudança Climática , Clima Tropical , Ciclo do Carbono , ÁrvoresRESUMO
Globally, human activities impose threats to nature and the provision of ecosystem services, such as pollination. In this context, ecological restoration provides opportunities to create managed landscapes that maximize biodiversity conservation and sustainable agriculture, e.g., via provision of pollination services. Managing pollination services and restoration opportunities requires the engagement of distinct stakeholders embedded in diverse social institutions. Nevertheless, frameworks toward sustainable agriculture often overlook how stakeholders interact and access power in social arenas. We present a perspective integrating pollination services, ecological restoration, and public engagement for biodiversity conservation and agricultural production. We highlight the importance of a comprehensive assessment of pollination services, restoration opportunities identification, and a public engagement strategy anchored in institutional analysis of the social arenas involved in restoration efforts. Our perspective can therefore guide the implementation of practices from local to country scales to enhance biodiversity conservation and sustainable agriculture.
RESUMO
Crop pollination is one of Nature's Contributions to People (NCP) that reconciles biodiversity conservation and agricultural production. NCP benefits vary across space, including among distinct political-administrative levels within nations. Moreover, initiatives to restore ecosystems may enhance NCP provision, such as crop pollination delivered by native pollinators. We mapped crop pollination demand (PD), diversity of pollinator-dependent crops, and vegetation deficit (VD) (vis-a-vis Brazilian legal requirements) across all 5570 municipalities in Brazil. Pollinator-dependent crops represented â¼55% of the annual monetary value of agricultural production and â¼15% of the annual crop production. Municipalities with greater crop PD (i.e., higher degree of pollinator dependence of crop production) also had greater VD, associated with large properties and monocultures. In contrast, municipalities with a greater diversity of pollinator-dependent crops and predominantly small properties presented a smaller VD. Our results support that ecological restoration prompted by legal requirements offers great potential to promote crop productivity in larger properties. Moreover, conservation of vegetation remnants could support food security in small properties. We provided the first steps to identify spatial patterns linking biodiversity conservation and pollination service. Using Brazilian legal requirements as an example, we show that land-use management policies may be successfully used to ensure agricultural sustainability and crop production.
Assuntos
Ecossistema , Polinização , Agricultura , Abelhas , Biodiversidade , Brasil , Produtos Agrícolas , HumanosRESUMO
The Program for Biodiversity Research (PPBio) is an innovative program designed to integrate all biodiversity research stakeholders. Operating since 2004, it has installed long-term ecological research sites throughout Brazil and its logic has been applied in some other southern-hemisphere countries. The program supports all aspects of research necessary to understand biodiversity and the processes that affect it. There are presently 161 sampling sites (see some of them at Supplementary Appendix), most of which use a standardized methodology that allows comparisons across biomes and through time. To date, there are about 1200 publications associated with PPBio that cover topics ranging from natural history to genetics and species distributions. Most of the field data and metadata are available through PPBio web sites or DataONE. Metadata is available for researchers that intend to explore the different faces of Brazilian biodiversity spatio-temporal variation, as well as for managers intending to improve conservation strategies. The Program also fostered, directly and indirectly, local technical capacity building, and supported the training of hundreds of undergraduate and graduate students. The main challenge is maintaining the long-term funding necessary to understand biodiversity patterns and processes under pressure from global environmental changes.
Assuntos
Biodiversidade , Ecossistema , Brasil , Conservação dos Recursos Naturais , Humanos , ConhecimentoRESUMO
Analysis of the structure, diversity, and demographic dynamics of tree assemblages in tropical forests is especially important in order to evaluate local and regional successional trajectories.We conducted a long-term study to investigate how the structure, species richness, and diversity of secondary tropical forests change over time. Trees (DBH ≥ 5 cm) in the Atlantic Forest of southern Brazil were sampled twice during a 10-year period (2007 and 2017) in six stands (1 ha each) that varied in age from their last disturbance (25, 60, 75, 90, and more than 100 years). We compared forest structure (abundance and basal area), species richness, alpha diversity, demographic rates (mortality, recruitment, and loss or gain in basal area), species composition, spatial beta diversity, and temporal beta diversity (based on turnover and nestedness indices) among stand ages and study years.Demographic rates recorded in a 10-year interval indicate a rapid and dynamic process of species substitution and structural changes. Structural recovery occurred faster than beta diversity and species composition recovery. The successional gradient showed a pattern of species trade-off over time, with less spatial dissimilarity and faster demographic rates in younger stands. As stands grow older, they show larger spatial turnover of species than younger stands, making them more stochastic in relation to species composition. Stands appear to split chronologically to some extent, but not across a straightforward linear axis, reflecting stochastic changes, providing evidence for the formation of a nonequilibrium community. Policy implications. These results reiterate the complexity and variability in forest succession and serve as a reference for the evaluation and monitoring of local management and conservation actions and for defining regional strategies that consider the diversity of local successional trajectories to evaluate the effectiveness of restoration measures in secondary forests of the Atlantic Forest biome.
RESUMO
To reverse the effects of deforestation, tropical areas have expanded restoration efforts in recent years. As ecological restoration positively affects the structure and function of degraded ecosystems, understanding to what extent restoration recovers ecosystem services (ES) is an important step in directing large-scale restoration actions. We evaluated the effect of restoration in increasing the provision of ES in tropical forests. We performed a global meta-analysis of ecological indicators of the ES provided in restored areas, degraded areas and reference ecosystems. We tested for the effects of different restoration strategies, different types of degradation and for the effects of restoration over time. Overall, restoration actions contributed to a significant increase in levels of ecological indicators of ES (carbon pool, soil attributes and biodiversity protection) compared to disturbed areas. Among the restoration strategies, the natural regeneration was the most effective. Biodiversity protection and carbon recovered better than soil attributes. All other restoration strategies recovered ES to a substantially lesser degree, and reforestation with exotics decreased the ES of areas degraded by agriculture. In areas degraded by pasture, restoration was more effective in recovering the biodiversity protection, whereas in areas degraded by agriculture, the restoration recovered mainly the carbon pool. Our results show that by choosing the correct strategy, restoration can recover much of the ES lost by the degradation of tropical forests. These results should be considered for large-scale conservation and management efforts for this biome.
Assuntos
Ecossistema , Recuperação e Remediação Ambiental , Florestas , Carbono/química , Bases de Dados Factuais , Ecologia , Solo/química , Clima TropicalRESUMO
Trade-offs in ecosystem services (ES) have received increasing attention because provisioning services often come at the expense of biodiversity loss. When land-use patterns are not maximally efficient relative to productivity, provisioning services, such as crop production, can often be increased without losing biodiversity. The Atlantic Forest (AF) encompasses dense, mixed, and seasonal forests and has high levels of endemism and anthropogenic threat. We examined trade-offs between biodiversity and crop production in the AF to provide insights into land-use management decisions. We developed a biodiversity metric that combines information on tree species richness, evolutionary distinctiveness, and rarity at the local level. We examined the extent to which the nature of ES trade-offs differ among the 3 forest types. We assessed how annual deforestation rates and land management practices affect biodiversity and agricultural revenues. Finally, we tested whether it is possible to achieve the same total regional revenue without reducing biodiversity by improving local management practices. The 3 forest types had similar patterns in ES trade-offs, although within mixed forest patterns differed. Biodiversity appeared to be more sensitive to land-use change than crop revenues. Certain crops yielded up to 10 times higher values in some sites. Enhanced crop productivity may increase revenues without reducing biodiversity. Our results showed that to enhance human well-being without further conversion of AF, maximizing crop productivity is needed . Increasing efficiency of management outcomes by maintaining higher biodiversity and increasing provisioning services depends on knowledge of forest type, the comparative advantage of planting crops in the best places, and preserving species in a balanced manner across forests.
Assuntos
Ecossistema , Árvores , Biodiversidade , Conservação dos Recursos Naturais , Produção Agrícola , Florestas , HumanosRESUMO
Wetlands harbor an important compliment of regional plant diversity, but in many regions data on wetland diversity and composition is still lacking, thus hindering our understanding of the processes that control it. While patterns of broad-scale terrestrial diversity and composition typically correlate with contemporary climate it is not clear to what extent patterns in wetlands are complimentary, or conflicting. To elucidate this, we consolidate data from wetland forest inventories in Brazil and examine patterns of diversity and composition along temperature and rainfall gradients spanning five biomes. We collated 196 floristic inventories covering an area >220 ha and including >260,000 woody individuals. We detected a total of 2,453 tree species, with the Amazon alone accounting for nearly half. Compositional patterns indicated differences in freshwater wetland floras among Brazilian biomes, although biomes with drier, more seasonal climates tended to have a larger proportion of more widely distributed species. Maximal alpha diversity increased with annual temperature, rainfall, and decreasing seasonality, patterns broadly consistent with upland vegetation communities. However, alpha diversity-climate relationships were only revealed at higher diversity values associated with the uppermost quantiles, and in most sites diversity varied irrespective of climate. Likewise, mean biome-level differences in alpha-diversity were unexpectedly modest, even in comparisons of savanna-area wetlands to those of nearby forested regions. We describe attenuated wetland climate-diversity relationships as a shifting balance of local and regional effects on species recruitment. Locally, excessive waterlogging strongly filters species able to colonize from regional pools. On the other hand, increased water availability can accommodate a rich community of drought-sensitive immigrant species that are able to track buffered wetland microclimates. We argue that environmental conditions in many wetlands are not homogeneous with respect to regional climate, and that responses of wetland tree communities to future climate change may lag behind that of non-wetland, terrestrial habitat.
Assuntos
Clima , Água Doce , Árvores , Áreas Alagadas , Biodiversidade , Brasil , Análise por Conglomerados , Florestas , Chuva , Análise de Regressão , TemperaturaRESUMO
The Lowland Forest is one of the most disturbed and fragile ecosystems in the Atlantic Forest biome, yet little is known regarding its successional trajectory and resilience. We evaluated changes in species assemblages and forest structure of the canopy and understory along a successional gradient (young 21-yrs old forest, immature 34-yrs old forest and late successional 59-yrs old forest) aiming to assess changes in species composition and successional trajectory of different strata of secondary forests. A 0.1 ha plot (ten 10x10 m sub-plots) from each forest stand was surveyed for trees and shrubs with a diameter at breast height (DBH) ≥ 4.8 cm (canopy) and for individuals with heights ≥ 1 m and DBH < 4.8 cm (understory). A total of 3,619 individuals from 82 plant species were sampled. The successional gradient was marked by a unidirectional increase in species richness and a bidirectional pattern of density changes (increasing from young to immature forest and decreasing from immature to late successional forest). Community assemblages were distinct in the three forests and two strata; indicator species were only weakly shared among stands. Thus, each successional forest and stratum was observed to be a unique plant community. Our results suggest slight predictability of community assemblages in secondary forests, but a relatively fast recovery of forest structure.
As Florestas de Terras Baixas constituem um dos ecossistemas mais perturbados e frágeis no bioma Mata Atlântica, mas ainda pouco se sabe sobre sua trajetória sucessional e resiliência. Foram avaliadas alterações na composição de espécies e a estrutura florestal do dossel e sub-bosque ao longo de um gradiente sucessional (floresta jovem-21 anos, floresta imatura-34 anos, floresta madura-59 anos) com o objetivo de verificar as mudanças na composição de espécies e a trajetória sucessional de diferentes estratos destas florestas secundárias. Uma parcela de 0,1 ha (dez sub-parcelas de 10x10 m) foi estabelecida em cada floresta, amostrando-se árvores e arbustos com um diâmetro è altura do peito (DAP) ≥ 4,8 cm (dossel) e para indivíduos com altura > 1 m e DAP < 4,8 cm (sub-bosque). Um total de 3.619 indivíduos de 82 espécies de plantas foram amostrados. O gradiente sucessional foi marcado por um aumento unidirecional na riqueza de espécies com o tempo, e um padrão bidirecional de mudanças de densidade (aumentando da floresta jovem para a imatura e diminuindo da imatura para a madura). As assembléias de plantas eram distintas nas três florestas e nos dois estratos; espécies indicadoras foram pouco compartilhadas entre as florestas. Portanto, cada estádio da cronosequência e cada estrato representam uma comunidade única de plantas. Nossos resultados sugerem pouca previsibilidade das assembleias de plantas destas florestas secundárias, mas uma recuperação relativamente rápida da estrutura da floresta.
RESUMO
Animal-plant interactions are important for the recovery of diversity and processes in secondary forests, which increasingly dominate the tropical landscape. We used a combination of observational and experimental approaches to study the interactions of ants with diaspores across a successional gradient of forests in Southern Brazil, from August 2007 to April 2008. In addition to diaspore removal rates, we assessed the species richness, diversity and behaviour of ants interacting with diaspores, in three replicated sites of four successional stages of forests. We recorded 22 ant species interacting with diaspores (an estimated 15% of the total species pool in the region). Species richness and diversity did not differ among successional stages but the behaviour of ants towards diaspores changed with the age of secondary forests. In old successional stages the removal of entire diaspores was more common than in young successional stages of forests. Concordantly, diaspore removal rates were lowest in the youngest successional stage of secondary forests and increased with the age of forests. These results indicate that ant-diaspore interactions in secondary forests are disturbed and lower removal rates in secondary forests are likely to constrain the recruitment of plant populations during secondary succession. Rev. Biol. Trop. 60 (2): 933-942. Epub 2012 June 01.
Las interacciones entre animales y plantas son importantes para la recuperación de la diversidad y los procesos en los bosques secundarios, los cuales cada vez más tienden a dominar el paisaje tropical. Nosotros utilizamos una combinación de métodos experimentales y observaciones para estudiar las interacciones entre hormigas y diásporas a través de un gradiente de sucesión en los bosques del sur de Brasil, entre agosto 2007 y abril 2008. Además de las tasas de eliminación de diásporas, evaluamos la riqueza de especies, la diversidad y el comportamiento de las hormigas que interactúan con las diásporas, con tres repeticiones por sitio de cuatro estadios de sucesión del bosque. Se registraron 22 especies de hormigas que interactúan con diásporas (se estima un 15% del total de especies en la región). La riqueza y diversidad de especies no varió entre las etapas de sucesión, pero el comportamiento de las hormigas hacia las diásporas cambio con la edad de los bosques secundarios. En las etapas sucesionales avanzadas del bosque la eliminación de diásporas fue más común que en las etapas tempranas. En concordancia, las tasas de eliminación de diásporas fueron menores en la etapa más temprana de la sucesión de bosques secundarios y aumenta con la edad de los mismos. Estos resultados indican que las interacciones hormigasdiásporas en los bosques secundarios son alteradas y las menores tasas de extracción en los bosques secundarios es probable que limiten el reclutamiento de las poblaciones de plantas durante la sucesión secundaria.
Assuntos
Animais , Formigas/fisiologia , Biodiversidade , Comportamento Animal/fisiologia , Árvores , Formigas/classificação , Brasil , Ecossistema , Dinâmica PopulacionalRESUMO
Animal-plant interactions are important for the recovery of diversity and processes in secondary forests, which increasingly dominate the tropical landscape. We used a combination of observational and experimental approaches to study the interactions of ants with diaspores across a successional gradient of forests in Southern Brazil, from August 2007 to April 2008. In addition to diaspore removal rates, we assessed the species richness, diversity and behaviour of ants interacting with diaspores, in three replicated sites of four successional stages of forests. We recorded 22 ant species interacting with diaspores (an estimated 15% of the total species pool in the region). Species richness and diversity did not differ among successional stages but the behaviour of ants towards diaspores changed with the age of secondary forests. In old successional stages the removal of entire diaspores was more common than in young successional stages of forests. Concordantly, diaspore removal rates were lowest in the youngest successional stage of secondary forests and increased with the age of forests. These results indicate that ant-diaspore interactions in secondary forests are disturbed and lower removal rates in secondary forests are likely to constrain the recruitment of plant populations during secondary succession.
Assuntos
Formigas/fisiologia , Comportamento Animal/fisiologia , Biodiversidade , Árvores , Animais , Formigas/classificação , Brasil , Ecossistema , Dinâmica PopulacionalRESUMO
Planting seedlings is a common technique for abandoned pastures restoration in the tropics, supposedly by increasing the seedling recruitment and accelerating succession. In this study we evaluated the role of a young restored forest (one year old) in enhancing seedling establishment from two sources (seed rain and seed bank), in the Atlantic Rainforest region in Southern Brazil. We compared abandoned pasture, young restored forest and old-growth forest with respect to the seedlings recruited from different sources, by monitoring 40 permanent plots (0.5mx0.5m) over 20 months. From the three studied areas a total of 392 seedlings of 53 species were recruited. Species were mainly herbaceous (85%), pioneers (88%), zoochorous (51%) and small-seeded species (60%). Seedling recruitment from the seed bank (density and species richness) was higher and dominated by herbaceous species in the abandoned pasture and in the young restored forest; on the other hand, the recruitment of woody species from seed rain was more pronounced in the old-growth forest. The young restored forest increased the species richness of woody seedlings recruitment from the seed bank (two-fold) and from seed rain (three-fold) compared to the abandoned pasture. Also, the seedling density in young restored forest was still higher than abandoned pastures (seed bank: four times; seed rain: ten times). Our results show that even young restored areas enhance the establishment of woody species and should be considered an important step for pasture restoration. Rev. Biol. Trop. 58 (4): 1271-1282. Epub 2010 December 01.
La introducción de plántulas en pastizales abandonados es una técnica común de restauración de los bosques en los trópicos, debido a que incrementa el reclutamiento de plántulas y acelera la sucesión. En este estudio se evaluó el papel de un bosque restaurado joven (un año) en el reclutamiento de plántulas a través de dos fuentes (lluvia y banco de semillas) en la región del Bosque Atlántico en el sur de Brasil. Se comparó un pastizal abandonado, un bosque restaurado joven y un bosque secundario maduro en cuanto al reclutamiento de plántulas de diferentes fuentes, mediante el monitoreo permanente de 40 parcelas (0.5mx0.5m) durante 20 meses. En las tres áreas estudiadas se reclutaron 392 plántulas de 53 especies, principalmente herbáceas (85%), pioneras (88%), zoocoras (51%) y de semilla pequeña (60%). El reclutamiento de plántulas en el banco de semillas (densidad y riqueza de especies) fue el más alto y dominado por especies herbáceas en el pasto abandonado y en el bosque restaurado joven, el reclutamiento de especies leñosas por la lluvia de semillas fue más pronunciado en los bosques secundarios maduros. Cuando se compara con el pastizal abandonado, el bosque restaurado joven presentó una mayor riqueza de plántulas de especies leñosas reclutadas, tanto del banco (el doble) como de la lluvia de semillas (tres veces más); la densidad de plántulas en el bosque restaurado joven fue más alta que en los pastizales abandonados (cuatro veces en el banco y diez veces en la lluvia de semillas). Nuestros resultados muestran que las áreas restauradas aún jóvenes pueden aumentar el reclutamiento de especies leñosas y deben considerarse como un paso importante para la restauración de pastizales.
Assuntos
Plântula/crescimento & desenvolvimento , Sementes/crescimento & desenvolvimento , Árvores/crescimento & desenvolvimento , Biomassa , Brasil , Conservação dos Recursos Naturais , Monitoramento Ambiental , Fatores de TempoRESUMO
The expectations that shade-tolerant forest species show 1) a population structure composed by a high amount of small individuals, and 2) biomass allocation for diameter higher than for height growth, were tested for Rudgea parquioides, a typical shrub in Southern Brazil. We described the size structure (height and stem diameter) and allometrical relations of a R. parquioides population by counting and measuring all the individuals in a 725m² area in the municipality of Curitiba (25"25'S; 49"19'W). A total of 916 individuals (12,634 ind.ha-1) were recorded in the area. The firstexpectation was supported, since distribution by height and diameter classes showed a predominance of small individuals (skewness coefficients > 1). On the other hand, the regression between height and stem base diameter showed slope β < 1, which indicates that growth in height is higher than in diameter, not supporting the second expectation. These results show that life strategies in shade-tolerant species may imply in more trade-off combinations than previously described.
Foram testadas duas hipóteses relativas a espécies florestaistolerantes à sombra em uma população de Rudgea parquioides, um arbusto característico do sul do Brasil: 1) espécies tolerantes à sombra possuem uma estrutura populacional composta por um grande número de indivíduos pequenos e 2) a alocação de biomassa para o crescimento em diâmetro é maior que para o crescimento em altura. Foram descritas as estruturas de tamanho (altura e diâmetro do tronco) e relações alométricas através da contagem e medição de todos os indivíduos de R. parquioides em uma área de 725m² no município de Curitiba (25"25'S; 49"19'W). Um total de 916 indivíduos(12.634 ind.ha-1) foi medido nesta área. A primeira hipótese foi aceita, uma vez que a distribuição em classes de altura e de diâmetro mostrou um predomínio de indivíduos pequenos (coeficiente de assimetria > 1). Por outro lado, a regressão entre altura e diâmetro na base do caule mostrou inclinação β < 1, o que indica que o crescimento em altura é maior que em diâmetro, não suportando a segunda hipótese. Esses resultados mostram que as estratégias de crescimento em espécies tolerantes à sombra podem implicar em outras relações ecológicas além das já descritas.
Assuntos
Ecossistema , Rubiaceae/classificação , Árvores , Biomassa , Brasil , Rubiaceae/anatomia & histologia , Rubiaceae/crescimento & desenvolvimentoRESUMO
Planting seedlings is a common technique for abandoned pastures restoration in the tropics, supposedly by increasing the seedling recruitment and accelerating succession. In this study we evaluated the role of a young restored forest (one year old) in enhancing seedling establishment from two sources (seed rain and seed bank), in the Atlantic Rainforest region in Southern Brazil. We compared abandoned pasture, young restored forest and old-growth forest with respect to the seedlings recruited from different sources, by monitoring 40 permanent plots (0.5 m x 0.5 m) over 20 months. From the three studied areas a total of 392 seedlings of 53 species were recruited. Species were mainly herbaceous (85%), pioneers (88%), zoochorous (51%) and small-seeded species (60%). Seedling recruitment from the seed bank (density and species richness) was higher and dominated by herbaceous species in the abandoned pasture and in the young restored forest; on the other hand, the recruitment of woody species from seed rain was more pronounced in the old-growth forest. The young restored forest increased the species richness of woody seedlings recruitment from the seed bank (two-fold) and from seed rain (three-fold) compared to the abandoned pasture. Also, the seedling density in young restored forest was still higher than abandoned pastures (seed bank: four times; seed rain: ten times). Our results show that even young restored areas enhance the establishment of woody species and should be considered an important step for pasture restoration.
Assuntos
Plântula/crescimento & desenvolvimento , Sementes/crescimento & desenvolvimento , Árvores/crescimento & desenvolvimento , Biomassa , Brasil , Conservação dos Recursos Naturais , Monitoramento Ambiental , Fatores de TempoRESUMO
The expectations that shade-tolerant forest species show 1) a population structure composed by a high amount of small individuals, and 2) biomass allocation for diameter higher than for height growth, were tested for Rudgea parquioides, a typical shrub in Southern Brazil. We described the size structure (height and stem diameter) and allometrical relations of a R. parquioides population by counting and measuring all the individuals in a 725m(2) area in the municipality of Curitiba (25°25'S; 49°19'W). A total of 916 individuals (12,634 ind.ha(-1)) were recorded in the area. The first expectation was supported, since distribution by height and diameter classes showed a predominance of small individuals (skewness coefficients > 1). On the other hand, the regression between height and stem base diameter showed slope ß < 1, which indicates that growth in height is higher than in diameter, not supporting the second expectation. These results show that life strategies in shade-tolerant species may imply in more trade-off combinations than previously described.