Do Dipteryx alata Vogel seedlings recover the quality and the photosynthetic and antioxidant responses in the post-flooding? / Mudas de Dipteryx alata Vogel recuperam a qualidade e as respostas fotossintéticas e antioxidantes no pós-alagamento?

Dipteryx alata Vogel is a tree species widely found in Cerrado, settling preferentially in well drained soils. Studies related to ecophysiology of D. alata may contribute to the decision making about using seedlings of this species in projects aimed at the recovery of degraded areas where seasonal flooding happens. This study aimed to assess the effects of flooding on photosynthetic and antioxidant metabolism and quality of D. alata seedlings cultivated or not under flooding during four assessment periods (0, 20, 40, and 60 days), followed by 100 days after the end of each assessment period (0+100, 20+100, 40+100, and 60+100 days), allowing verifying the potential for post-flooding recovery. Flooded plants showed lower photosynthetic efficiency than non-flooded plants, regardless of the periods of exposure. However, this efficiency was recovered in the post-flooding, with values similar to that of the non-flooded seedlings. Moreover, the damage to FV/FM was evidenced by an increase in the period of exposure to flooding, but recovery was also observed at this stage of the photosynthetic metabolism. Seedling quality decreased under flooding, not varying between periods of exposure, but remained lower although the increase observed in the post-flooding period, with no recovery after flooding. The occurrence of hypertrophied lenticels associated with physiological changes and an efficient antioxidant enzyme system might have contributed to the survival and recovery of these seedlings. Thus, this species is sensitive to flooding stress but capable of adjusting and recovering metabolic characteristics at 100 days after the suspension of the water stress, but with no recovery in seedling quality. Thus, we suggested plasticity under the cultivation condition and determined that the time of 100 days is not enough for the complete resumption of growth.

Dipteryx alata Vogel é uma arbórea de ampla ocorrência no Cerrado, se estabelecendo preferencialmente em solos bem drenados. Estudos referentes à ecofisiologia de D. alata em podem contribuir para a tomada de decisão sobre o uso de mudas dessa espécie em programas de recuperação de áreas degradadas sujeitas a alagamento temporário. Objetivamos com essa pesquisa avaliar os efeitos do alagamento no metabolismo fotossintético e antioxidante, além da qualidade de mudas dessa espécie, cultivadas ou não sob alagamento durante quatro períodos de avaliação (0, 20, 40 e 60 dias) seguidos de 100 dias após o término de cada período (0+100, 20+100, 40+100, 60+100 dias), possibilitando verificar o potencial de recuperação pós-alagamento. Observamos que as plantas alagadas apresentaram menor eficiência fotossintética e danos em FV/FM entretanto houve recuperação dessas características no pós alagamento. A qualidade das mudas reduziu sob alagamento não variando entre os períodos de exposição e embora tenha aumentado no pós-alagamento manteve-se menor não se recuperando. A ocorrência de lenticelas hipertrofiadas associadas a alterações fisiológicas e um eficiente sistema enzimático antioxidante devem ter contribuído para a sobrevivência e recuperação metabólica dessas mudas. Diante disso, sugerimos que a espécie é sensível ao estresse por alagamento, mas capaz de se ajustar e recuperar as características metabólicas 100 dias após a suspensão deste estresse hídrico, no entanto a qualidade da mudas não apresentou recuperação, assim, sugerimos plasticidade diante da condição de cultivo e ressaltamos que o tempo de 100 dias não é suficiente para a completa retomada do crescimento.

Ecological consequences of primary and secondary seed dispersal on seed and seedling fate of Dipteryx oleifera (Fabaceae)

The relative contributions of primary and secondary seed dispersal to plant demography have received little investigation. Evidence on these seed dispersal types, on seed fate and seedling recruitment of the tropical rain forest tree Dipteryx oleifera, is presented. The study was conducted in a 6.37ha permanent plot where seeds and seedlings were located and tagged for the 2007 cohort. A total of 2 814 seeds were threaded and their fate was followed one year after germination. Primary seed dispersal by bats protected seeds from insect larval predation below the adult tree. Bats congregated seeds in bat seed piles located at a mean distance of 40.94±1.48m from the nearest adult individual of D. oleifera. Terrestrial vertebrates congregated seeds in caches located 41.90±2.43m from the nearest adult individual of D. oleifera. The results of the fitted proportional hazard model suggested that primary seed dispersal decreased seed hazard probability by 1.12% for each meter from the adult conspecific (p<0.001) and that secondary seed dispersal decreased it by 23.97% (p<0.001). Besides, the odds ratio regression models results showed that the overall effect of unviable seeds was a reduction in viable seed predation rate. For each unviable seed deposited by bats into the seed piles, the rate of seed predation by terrestrial vertebrates decreased 6% (p<0.001). For each damaged seed by terrestrial vertebrates in the seed piles, the rate of germination decreased 4% (p<0.001). For each germinated seed in the seed piles, the rate of recruitment increased 16% (p=0.001). Seedling survival of seeds that emerged after secondary seed dispersal events, showed no statistically significant difference in arthropod herbivory, in relation to seedlings that came from seeds that were dispersed only primarily by bats (F=0.153, p=0.697, df=1.98). Thus both primary and secondary dispersal contributed to higher seedling survival away from the nearest adult D. oleifera (r2=0.713, n=578, p=0.004). The distribution of D. oleifera seedlings is consistent with the Janzen-Connell Hypothesis and depends on primary dispersal by bats, secondary dispersal by terrestrial vertebrates, a seed masking effect and, the constant threat of insect herbivores on seedlings. Rev. Biol. Trop. 58 (3): 991-1007. Epub 2010 September 01.

Presentamos evidencia de la contribución relativa de la dispersión primaria y secundaria de semillas en la suerte que corren las mismas y en el reclutamiento de plántulas de la especie de bosque húmedo tropical Dipteryx oleifera. Este estudio fue realizado en una parcela permanente de 6.37 ha en la que semillas y plántulas del cohorte del 2007 fueron localizadas y mapeadas. Etiquetamos 2 814 semillas para evaluar su suerte un año después de la germinación. Encontramos que la dispersión primaria por murciélagos libera a las semillas de la depredación bajo la copa del árbol adulto causada por la fase larval de un insecto. Los murciélagos dispersan semillas bajo la copa de palmas usadas como comederos, localizados a 40.94±1.48m del árbol de D. oleifera más cercano y vertebrados terrestres congregaran las semillas en caches localizados aproximadamente a 41.90±2.43m del árbol de D. oleifera. Un modelo proporcional de riesgos fue ajustado a los datos de semillas y los resultados sugieren que la dispersión decrece la probabilidad de mortalidad de las semillas 1.16% por cada metro del árbol conspecífico más cercano (p<0.001) y la dispersión secundaria de semillas decrece la probabilidad de mortalidad 23.94% por cada metro (p<0.001). Los modelos de regresión de quebrados muestran que las semillas inviables reducen la tasa de depredación de las viables. Por cada semilla inviable depositada por los murciélagos en las agrupaciones de semillas, la tasa de depredación por vertebrados terrestres decreció 6% (p<0.001). Por cada semilla dañada por vertebrados en las agrupaciones, la tasa de germinación decreció 4% (p<0.001). Por cada semilla germinada en las agrupaciones, la tasa de reclutamiento incrementó 16% (p=0.000). La sobrevivencia de plántulas con dispersión secundaria fue estadísticamente diferente a la de aquellas que únicamente tuvieron dispersión primaria (F=0.153, p=0.697, df=1.98). Ambos tipos de dispersión contribuyeron con una alta sobrevivencia de plántulas lejos del árbol congénere más cercano (r²=0.713, n=578, p=0.004). Concluimos que la distribución de las plántulas de D. oleifera es consistente con la Hipótesis de Janzen- Connell y depende de la dispersión primaria por murciélagos, dispersión secundaria por vertebrados terrestres, el efecto de enmascaramiento y el constante ataque de insectos herbívoros a las plántulas.

Beneficial effect of spider presence on seedling recruitment of the tropical rainforest tree Dipteryx oleifera (Fabaceae)

This research presents evidence showing that: (1) lower arthropod herbivory correlates with seedling survival, and (2) spider presence correlates with lower arthropod herbivory, seedling growth, and seedling survival of the tropical rainforest tree species Dipteryx oleifera in eastern Nicaragua. The study was conducted from January 2005 to January 2006 in a 6.37 ha permanent plot established in 2002. Seedling height, spider behavior and presence on seedlings, and percentage of leaf area lost due to arthropod herbivory were measured. Arthropod herbivory was assessed from digital photographs of each seedling within the permanent plot. Seedling fate was followed in order to determine its correlation with spider presence, initial seedling size, and arthropod herbivory. A GLM showed that seedling survival correlated negatively with lower levels of arthropod herbivory (<20%), while seedlings with higher levels of herbivore damage experienced mortalities close to 100%. Results from another GLM suggests that seedling mean height (aprox. 8 cm) would be increased by approximately 1.5 cm for each year that spiders were present on seedlings and would be decreased 0.75 cm in height for each percent unit of arthropod herbivory. We also report a trend toward lower arthropod herbivory in seedlings colonized by spiders with aggressive traits, presumably because more aggressive spiders better defended seedlings against herbivorous arthropods than less aggressive spiders. Rev. Biol. Trop. 57 (3): 837-846. Epub 2009 September 30.

Se presenta evidencia que sugiere (1) que los niveles bajos de herbivoría de artrópodos se correlacionan con la supervivencia de plántulas y, (2) que la presencia de arañas se correlaciona con los niveles bajos de herbivoría de artrópodos, crecimiento y supervivencia de plántulas de la especie de bosque húmedo tropical Dipteryx oleifera en el este de Nicaragua. El estudio se realizó entre enero del 2005 y enero del 2006 en una parcela de 6.37 ha establecida en 2002. Se midió altura de plántulas, presencia de arañas en plántulas, comportamiento de arañas, y porcentaje de herbivoría de artrópodos. La suerte de las plántulas fue monitoreada con el objetivo de determinar su correlación con la presencia de arañas, el tamaño inicial de las plántulas y herbivoría de artrópodos. Un GLM mostró que las plántulas con bajo nivel de daño de herbivoría (<20%) sobrevivieron más que las plántulas con niveles mayores de daño por herbivoría, las cuales experimentaron mortalidades cercanas al 100 por ciento. Los resultados de otro GLM sugieren que la altura media de plántulas (aprox. 8 cm) incrementó aproximadamente 1.5 cm por cada año en el cual las arañas se encontraron presente en las plántulas, y decrecieron 0.75 cm en altura por cada unidad de herbivoría. También se reporta menor herbivoría en plántulas colonizadas por arañas de comportamiento agresivo.

Recruitment dynamics of the tropical rainforest tree Dipteryx oleifera (Fabaceae) in eastern Nicaragua

Seed production, seed dispersal and recruitment are critical processes in population dynamics, because they are almost never completely successful. We recorded the recruitment dynamics for the population of Dipteryx oleifera in a tropical rainforest in eastern Nicaragua (12°05’ N., 83°55’ W.) from March 2002 to August 2006. Seeds and seedlings had highly clumped distributions, while sapling distributions appeared to be random. Seedling survival increased away from the nearest conspecifc adult tree, where seedling density is lower. Since relative growth rates of seedlings are not correlated with the distance to the nearest conspecific adult, seedling survival appears to be independent of seedling growth. Seedling density is inversely correlated with seedling insect herbivory damage. Seedling survival correlated negatively with the number of saplings per sub-plot (10x10m), suggesting that insect herbivore may also cue in on saplings rather than only on adult D. oleifera trees in order to locate seedlings. Seedling establishment is significantly clumped with respect to the nearest adult tree. Larger clumps of seedlings seems more ephemeral than isolated smaller clumps located away from the nearest D. oleifera tree. These results support current empirical evidence presented earlier for the Janzen-Connell hypothesis for Dipteryx oleifera at seed and seedling stages and, the Recruitment Limitation hypothesis at the sapling stage, because sapling individuals might have recruited after random light-gap formation. Rev. Biol. Trop. 57 (1-2): 321-338. Epub 2009 June 30.

Resumen Estudiamos la dinámica de regeneración de la población de Dipteryx oleifera en un bosque húmedo tropical del este de Nicaragua. Semillas y plántulas se encuentran altamente agregadas, pero la distribución de vástagos podría ser al azar. La supervivencia de plántulas aumenta con la distancia al congéner más cercano, donde la densidad de plántulas es más baja. Como las tasas de crecimiento relativo de plántulas no se correlacionan con la distancia al congénere más cercano, la supervivencia de las plantas pareciera no estar determinada por el crecimiento de plántulas. La densidad de plántulas está inversamente correlacionada con los niveles de daño de herbivoría insectívora. La supervivencia de plántulas se correlaciona negativamente con el número de vástagos, lo cuál sugiere que los insectos herbívoros podrían estar localizando vástagos y árboles y de allí, las plántulas. La supervivencia de plántulas presentó una distribución significativamente agrupada lejos de los congéneres más cercanos. Los parches de plántulas más grandes fueron más efímeros que los parches pequeños y aislados ubicados lejos de los árboles adultos. Los resultados coinciden con la hipótesis de Janzen-Connell sobre estados de semilla y plántula. Además, ofrecen evidencia en favor de la hipótesis de Limitación de Reclutamiento para los vástagos, ya que los vástagos podrían estar estableciéndose en claros de luz pequeños que se forman al azar.