Plant structure predicts leaf litter capture in the tropical montane bromeliad Tillandsia turneri

A estrutura da planta determina a folhagem interceptada pela bromelia Tillandsiaturneri

F. Ospina-Bautista J. V. Estévez Varón About the authors

Abstract

Leaves intercepted by bromeliads become an important energy and matter resource for invertebrate communities, bacteria, fungi, and the plant itself. The relationship between bromeliad structure, defined as its size and complexity, and accumulated leaf litter was studied in 55 bromeliads of Tillandsia turneri through multiple regression and the Akaike information criterion. Leaf litter accumulation in bromeliads was best explained by size and complexity variables such as plant cover, sheath length, and leaf number. In conclusion, plant structure determines the amount of litter that enters bromeliads, and changes in its structure could affect important processes within ecosystem functioning or species richness.

Keywords:
leaf litter; Bromeliaceae; plant structure; tropical montane forest

Resumo

As folhagens interceptadas pelas bromélias é um importante recurso para a comunidade de invertebrados, bactérias, fungos e para a própria planta. Estudou-se a relação entre a estrutura de 55 bromélias de Tillandsia tumeri, definida como o tamanho, a complexidade da planta, a folhagem acumulada por meio de regressão múltipla e o critério de informação de Akaike. Encontrou-se que as variáveis de tamanho, cobertura, comprimento da bainha e a variável de complexidade do número de folhas explicam a acumulação de folhas nas bromélias. Em conclusão, a estrutura do planta determina a quantidade de folhas armazenada na bromélia e os câmbios da estrutura da bromélia poderiam afetar importantes processos de funcionamento do ecossistema ou a riqueza de espécies.

Palavras-chave:
folhagens; Bromeliaceae; estrutura do planta; floresta tropical montana

1 Introduction

Leaf litter is the most significant energy and matter resource for detrital food webs (Anderson and Sedell, 1979Anderson, N.H. and Sedell, J.R., 1979. Detritus processing by macroinvertebrates in stream ecosystems. Annual Review of Entomology, vol. 24, no. 1, pp. 351-377. http://dx.doi.org/10.1146/annurev.en.24.010179.002031.
http://dx.doi.org/10.1146/annurev.en.24....
; Hattenschwiler et al., 2005Hattenschwiler, S., Tiunov, A.V. and Scheu, S., 2005. Biodiversity and litter decomposition in terrestrial ecosystems. Annual Review of Ecology Evolution and Systematics, vol. 36, no. 1, pp. 191-218. http://dx.doi.org/10.1146/annurev.ecolsys.36.112904.151932.
http://dx.doi.org/10.1146/annurev.ecolsy...
) as litter decomposition directs nutrient cycling through the conversion of organic material to its mineral form (Swift et al., 1979Swift, M.J., HEAL, O.W. and ANDERSON, J.M., 1979. Decomposition in terrestrial ecosystems. Oxford: Blackwell Scientific. 372 p. Studies in Ecology, no. 5.). Although most leaf litter in a forest falls directly to the soil, a part of it is intercepted by tree canopies, shrubs (Lodge, 1996Lodge, D.J., 1996. Microorganisms. In: D.P. REAGAN and R.B. WAIDE, eds. The food web of a tropical rain forest. Chicago: University of Chicago Press, pp. 53-108.), understory plants (Alvarez-Sanchez and Guevara, 1999Alvarez-Sanchez, J. and Guevara, S., 1999. Litter interception on Liebm. (Palmae) in a tropical rain forest. Astrocaryum mexicanumBiotropica, vol. 31, pp. 89-92. http://dx.doi.org/10.1111/j.1744-7429.1999.tb00119.x.
http://dx.doi.org/10.1111/j.1744-7429.19...
), and vascular epiphytes such as bromeliads (Lodge, 1996Lodge, D.J., 1996. Microorganisms. In: D.P. REAGAN and R.B. WAIDE, eds. The food web of a tropical rain forest. Chicago: University of Chicago Press, pp. 53-108.).

Leaves intercepted by bromeliads become an important energy and matter resource for invertebrate communities (Maloney and Lamberti, 1995Maloney, D.C. and Lamberti, G.A., 1995. Rapid decomposition of summer input leaves in a northern Michigan stream. American Midland Naturalist, vol. 133, no. 1, pp. 184-195. http://dx.doi.org/10.2307/2426360.
http://dx.doi.org/10.2307/2426360...
; Yanoviak, 1999Yanoviak, S.P., 1999. Effects of leaf litter species on macroinvertebrate community properties and mosquito yield in Neotropical tree hole microcosms. Oecologia, vol. 120, no. 1, pp. 147-155. http://dx.doi.org/10.1007/s004420050843.
http://dx.doi.org/10.1007/s004420050843...
) and the plant itself (Ngai and Srivastava, 2006Ngai, J.T. and Srivastava, D.S., 2006. Predators accelerate nutrient cycling in a bromeliad ecosystem. Science, vol. 314, no. 5801, pp. 963. http://dx.doi.org/10.1126/science.1132598. PMid:17095695.
http://dx.doi.org/10.1126/science.113259...
). Leaf litter intercepted by bromeliads provides microhabitat and nutrients to organisms such as bacteria and fungi, detritivores, and deposit feeders (Frank, 1983Frank, J.H., 1983. Bromeliad phytotelmata and their biota, especially mosquitos. In: H. Frank and P.L. Lounibos, eds. Phytotelmata: terrestrial plants as hosts of aquatic insects communities. New Jersey: Plexus, Inc., pp. 101-128.; Armbruster et al., 2002Armbruster, P., Hutchinson, R.A. and Cotgreave, P., 2002. Factors influencing community structure in a South American tank bromeliad fauna. Oikos, vol. 96, no. 2, pp. 225-234. http://dx.doi.org/10.1034/j.1600-0706.2002.960204.x.
http://dx.doi.org/10.1034/j.1600-0706.20...
). As a consequence, leaf litter affects the organisms associated with this micro-ecosystem, for example, invertebrate richness and abundance are related to the amount of litter in Guzmania spp. Ruíz and Pav. 1802 and Vriesia spp. Lindl. 1843 (Richardson et al., 2000Richardson, B., Rogers, C. and Richardson, M.J., 2000. Nutrients, diversity, and community structure of two phytotelm systems in a lower montane forest, Puerto Rico. Ecological Entomology, vol. 25, no. 3, pp. 348-356. http://dx.doi.org/10.1046/j.1365-2311.2000.00255.x.
http://dx.doi.org/10.1046/j.1365-2311.20...
), and the proportion of hunting spiders increases with greater litter depth in individuals of Aechmea distichantha Lem. 1853 (Montero et al., 2010Montero, G., Feruglio, C. and Barberis, I.M., 2010. The phytotelmata and foliage macrofauna assemblages of a bromeliad species in different habitats and seasons. Insect Conservation and Diversity, vol. 3, no. 2, pp. 92-102. http://dx.doi.org/10.1111/j.1752-4598.2009.00077.x.
http://dx.doi.org/10.1111/j.1752-4598.20...
). Additionally, bromeliads obtain nutrients from litter intercepted by rosettes, which are absorbed through specialized trichomes (Benzing and Renfrow, 1974Benzing, D.H. and Renfrow, A., 1974. The nutritional status of and on . Encyclia tampensisTillandsia circinata,Taxodium ascendens, and the availability of nutrients to epiphytes on this host in south FloridaBulletin of the Torrey Botanical Club, vol. 101, no. 4, pp. 191-197. http://dx.doi.org/10.2307/2484643.
http://dx.doi.org/10.2307/2484643...
; Benzing, 2000Benzing, D.H., 2000. Bromeliaceae: profile of an adaptive radiation. Cambridge: Cambridge University Press. 710 p.) and are important for reproduction, fitness, and growth (Benzing, 1990Benzing, D.H., 1990. Vascular epiphytes. Cambridge: Cambridge University Press. 354 p.; Lasso and Ackerman, 2013Lasso, E. and Ackerman, J.D., 2013. Nutrient limitation restricts growth and reproductive output in a tropical montane cloud forest bromeliad: findings from a long-term forest fertilization experiment. Oecologia, vol. 171, no. 1, pp. 165-174. http://dx.doi.org/10.1007/s00442-012-2403-z. PMid:22767363.
http://dx.doi.org/10.1007/s00442-012-240...
).

Although leaf litter is relevant to associated organisms and the plant itself, little attention has been given to factors, such as bromeliad structure, that could determine the amount of leaf litter retained by the plant as well as its effect on the invertebrate community. Moreover, bromeliad structure has only been related to the invertebrate community associated with bromeliads (Richardson, 1999Richardson, B., 1999. The bromeliad microcosm and the assessment of faunal diversity in a Neotropical Forest. Biotropica, vol. 31, no. 2, pp. 321-336. http://dx.doi.org/10.1111/j.1744-7429.1999.tb00144.x.
http://dx.doi.org/10.1111/j.1744-7429.19...
; Armbruster et al., 2002Armbruster, P., Hutchinson, R.A. and Cotgreave, P., 2002. Factors influencing community structure in a South American tank bromeliad fauna. Oikos, vol. 96, no. 2, pp. 225-234. http://dx.doi.org/10.1034/j.1600-0706.2002.960204.x.
http://dx.doi.org/10.1034/j.1600-0706.20...
; Araújo et al., 2007Araújo, V.A., Melo, S.K., Araújo, A.P., Gomes, M.L. and Carneiro, M.A., 2007. Relationship between invertebrate fauna and bromeliad size. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 67, no. 4, pp. 611-617. http://dx.doi.org/10.1590/S1519-69842007000400004. PMid:18278311.
http://dx.doi.org/10.1590/S1519-69842007...
), vertebrate species (Cruz-Ruiz et al., 2012Cruz-Ruiz, G.I., Mondragón, D. and Santos-Moreno, A., 2012. The presence of Abronia oaxacae (Squamata: Anguidae) in tank bromeliads in temperate forests of Oaxaca, México. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 72, no. 2, pp. 337-341. http://dx.doi.org/10.1590/S1519-69842012000200015. PMid:22735142.
http://dx.doi.org/10.1590/S1519-69842012...
), the amount of water (Zotz and Vera, 1999Zotz, G. and Vera, T., 1999. How much water is in the tank? Model calculations for two epiphytic bromeliads. Annals of Botany, vol. 83, no. 2, pp. 183-192. http://dx.doi.org/10.1006/anbo.1998.0809.
http://dx.doi.org/10.1006/anbo.1998.0809...
), prey vulnerability (Saha et al., 2009Saha, N., Aditya, G. and Saha, G.K., 2009. Habitat complexity reduces prey vulnerability: an experimental analysis using aquatic insect predators and immature dipteran prey. Journal of Asia-Pacific Entomology, vol. 12, no. 4, pp. 233-239. http://dx.doi.org/10.1016/j.aspen.2009.06.005.
http://dx.doi.org/10.1016/j.aspen.2009.0...
), and detrital processing (Srivastava, 2006Srivastava, D., 2006. Habitat structure, trophic structure and ecosystem function: interactive effects in a bromeliad–insect community. Oecologia, vol. 149, no. 3, pp. 493-504. http://dx.doi.org/10.1007/s00442-006-0467-3. PMid:16896779.
http://dx.doi.org/10.1007/s00442-006-046...
). In this study, we evaluated the relationship between bromeliad structure and the amount of litter retained, and built a model to predict leaf litter capture using measures of plant structure in Tillandsia turneri Baker 1888.

2 Material and Methods

The study was conducted in a tropical montane forest (Holdridge, 1967Holdridge, L.R., 1967. Life zone ecology. San José, Costa Rica: Tropical Science Center. 216 p.) at 3000 m and 3100 m of elevation. This forest is a 70 years old mature forest located in El Santuario ranch (Cundinamarca, Colombia), near El Sisga dam (5° 01’ N, 73° 42’ W). The mean annual rainfall is 924.7 mm. The precipitation regimen is unimodal with the dry season from September to April; the mean annual temperature is 11.9 ºC and the annual sunshine is 1264.1 hours. Average canopy height is 18 m, with some trees growing up to 30 m; the basal area is 51.35 m2/ha and the number of plant individuals per hectare is 3510. The most common of 27 tree species at the site were: Weinmannia tomentosa L f. 1781, Drymis granadensis L f., and Myrsine ferruginea (Ruíz and Pav. 1802) Spreng 1825. The bromeliads in this forest included T. turneri Baker 1888, Guzmania gloriosa (Andre’) Andre’ ex Mez. 1897, Racinaea tetrantha (Ruíz and Pav.1802) M.A. Spencer and L.B. Sm., T. biflora Ruíz and Pav.1802, T. complanata Benth 1846, and T. fendleri Griseb. 1865. Litterfall is 5264.31 kg/ha in a year and is unrelated to the monthly precipitation, air temperature, and evaporation (Estevez Varón and Viña, 1999Estevez Varon, J.V. and Viña, A., 1999. Producción y Descomposición de hojarasca en Tres Estadios sucesionales de un Bosque de montaña en el Municipio de Chocontá, Cundinamarca, Colombia. Bogotá: Fondo FEN. 65 p. Informe.).

Tillandsia turneri is the most abundant tank bromeliad in this ecosystem (Isaza et al., 2004Isaza, C., Betancur, J. and Estévez Varón, J.V., 2004. Vertical distribution of bromeliads in a montane forest in the Eastern cordillera of the colombian Andes. Selbyana, vol. 25, no. 1, pp. 126-137.); the fauna associated with T. turneri is well known (Ospina et al., 2004Ospina, M.F., Estevez Varon, J.V., Betancur, J. and Realpe, E., 2004. Macroinvertebrados acuáticos asociados a la bromelia en un bosque altoandino. Tillandsia turneriRevista Acta Zoológica Mexicana, vol. 20, no. 1, pp. 153-166., 2008Ospina, M.F., Estevez Varon, J.V., Realpe, E. and Gast, F., 2008. Diversidad de invertebrados acuáticos asociados a Bromeliaceae en un bosque de montaña. Revista Colombiana de Entomologia, vol. 34, no. 2, pp. 224-229.). In order to estimate leaf litter weight inside 53 adult T. turneri individuals in the forest, bromeliads were collected from January to May of 2000. For this study, leaf litter only included leaves from the canopy. The samples were packed in labeled bags and then taken to the laboratory where they were dried at 80°C for 72 hours. The dry mass of the fallen leaves was determined using an analytical scale to the nearest 0.01g.

Bromeliad structure is defined by its size and complexity. Bromeliad size was measured through plant height (determined as the vertical distance between the plant base and the tip of the highest leaf), plant cover, which was calculated as the area of a circle with the same diameter as the plant diameter (plant diameter measured as the average between the distance between the most external leaves of the bromeliad and the diameter perpendicular to this first axis) (Richardson, 1999Richardson, B., 1999. The bromeliad microcosm and the assessment of faunal diversity in a Neotropical Forest. Biotropica, vol. 31, no. 2, pp. 321-336. http://dx.doi.org/10.1111/j.1744-7429.1999.tb00144.x.
http://dx.doi.org/10.1111/j.1744-7429.19...
), leaf length and width, and sheath length and width of the four longest leaves of each plant. Complexity was measured through leaf number.

We performed regression models with bromeliad variables in order to investigate the relationship between litter amount on the phytotelmata and bromeliad size and complexity. The litter amount was transformed as y^0.5 and the assumptions of normality, collinearity, linearity and homoscedasticity were tested. We did not consider interaction terms among variables. We calculated the AICc (Akaike information criterion corrected) value through the formula: AICc = nLog(RSS/n)2 + 2K (n/(n-K-1)); where n is the number of observations, RSS is the residual sums of squares, and K is the number of parameters (Anderson, 2008Anderson, D.R., 2008. Model based inference in the life sciences: a primer on evidence. New York: Springer Science. 208 p.). The best model was determined by examining the differences relative to smallest AIC, Δi = AICi – min AIC; where Δiis the difference between the AIC of the best fitting model and that of model i, AICiis the AIC for the model i, and min AIC is the minimum AIC value of all models.

Model probability was found with the formula: wi= exp (- 0.5*Δi) / ∑Rr=1exp (- 0.5*Δr); where wiis the Akaike weightfor model i, the numerator is the relative likelihood, given the data, for model i, and the denominator is the sum of the relative likelihoods for all candidate models. Furthermore, we found the evidence of each model with the formula: E min,i = wmin / wi.

We calculated the composite or averaged model with its unconditional standard errors (SE) through the formula: SE = ((se2 + MSV) * w) ½ where MSV is calculated as (model average estimate – raw parameter estimate)2 and (se2) is the square of the standard error of regression. The SE values allow us to determine the precision of the estimated model and variables; therefore, if the SE value is two times greater than the estimated parameter, then we can conclude that this parameter is not a good estimator of the response variable (Anderson, 2008Anderson, D.R., 2008. Model based inference in the life sciences: a primer on evidence. New York: Springer Science. 208 p.). In order to evaluate the relative importance of each variable, we established the weight of each explanatory variable using the function to calculate relative importance metrics for linear models (calc.relimp) with R^2 contribution averaged over orderings among regressors (Chevan and Sutherland, 1991Chevan, A. and Sutherland, M., 1991. Hierarchical partitioning. The American Statistician, vol. 45, no. 2, pp. 90-96. http://dx.doi.org/10.2307/2684366.
http://dx.doi.org/10.2307/2684366...
). The statistical analyses were done using the R statistic program (R Development Core Team R, 2013R DEVELOPMENT CORE TEAM2013R: a language and environment for statistical computingViennaR Foundation Statistical Computing).

3 Results

The T. turneri individuals selected in the study presented high variability in the structure variables, for instance, plant cover varied from 483 to 6249 cm2 and leaf number from 32 to 93 (see Table 1). Moreover, the T. turneri individuals contained 38.54 g +/-20.36 of litter.

Table 1
Mean, Standard error, Minimal and Maximal of structure variables of Tillandsia turneri.

The model with the lowest AICc and the highest m

odel probability included plant cover, leaf number, and sheath length variables was the best model to explain the variation in leaf litter amount present in the bromeliads (Table 2). The model was statistically significant and explained 29.82% of variation in leaf litter amount present in the bromeliads (F3,49= 8.36, p= 0.0001, R2= 0.30; litter= 0.37 + 0.0005 plant cover + 0.035 leaf number + 0.12 sheath length). In this model, plant cover and leaf number were the variables that most contributed to explaining litter weight in bromeliads (plant cover: t=3.02, df=49, p=0.004, leaf number: t=2.44, df=49, p=0.018) (see Figure 1). Moreover, this model is 1.22 times more likely to be the best explanation for litter amount compared to the second model, which included plant cover, leaf number, and plant height variables (see Table 2). According to the evidence, the most probable models are those that include plant cover, leaf number, and sheath length combined with plant height, because their evidence values are less than four (Anderson 2008Anderson, D.R., 2008. Model based inference in the life sciences: a primer on evidence. New York: Springer Science. 208 p.). The weight of each variable was: sheath length 0.16, plant cover 0.52, and leaf number 0.32; therefore, leaf number and plant cover are highly plausible explanations for leaf litter amount, but, given the data and the group of candidate models, plant cover is 0.2 times more plausible or probable than leaf number, and 0.36 times more probable than sheath length.

Table 2
Model tested to evaluate the effect of bromeliad structure parameters on leaf litter amount.
Figure 1
Relation between bromeliad variables and leaf litter amount. (a). Leaf number. (b). Plant cover.

4 Discussion

Bromeliads are a relevant component of Neotropical forests where bromeliads have high abundance and richness (Lugo and Scatena, 1992Lugo, A.E. and SCATENA, F.N., 1992. Epiphytes and climate change research in the caribbean: a proposal. Selbyana, vol. 13, pp. 123-130.). Our study sought to determinate the relation between litter intercepted by bromeliads and bromeliad size and complexity. We found a relationship between leaf litter amount on Tillandsia turneri, which is the most abundant bromeliad in the study area, and bromeliad plant structure, measured through bromeliad leaf number, sheath length, and plant cover.

Plant leaf number is a measure of habitat complexity, which is the spatial subdivision of a habitat at a scale smaller than the mobility of individuals (Srivastava, 2006Srivastava, D., 2006. Habitat structure, trophic structure and ecosystem function: interactive effects in a bromeliad–insect community. Oecologia, vol. 149, no. 3, pp. 493-504. http://dx.doi.org/10.1007/s00442-006-0467-3. PMid:16896779.
http://dx.doi.org/10.1007/s00442-006-046...
). The rosette dispositions of bromeliad leaves allow the creation of small tanks, where the plant can reserve rain water and leaf litter from the canopy (Benzing, 1980Benzing, D.H., 1980. The biology of bromeliads. California: Mad River Press, Eureka. 305 p.). The complexity of this micro-ecosystem increases with higher bromeliad leaf numbers, leading to more litter retention on the bromeliad and, as a result, increasing the diversity of associated organisms.

Plant cover and sheath length are related to bromeliad size. Plant cover refers to estimates of the bromeliad’s area for interception of water and canopy leaf litter; accordingly, plants with high plant cover values will have greater amounts of resources, thereby increasing the probability of associated organisms (Lawton and Schroder, 1977Lawton, J.H. and Schröder, D., 1977. Effects of plant type, size of geographical range and taxonomic isolation on number of insect species with British plants. Nature, vol. 265, no. 5590, pp. 137-140. http://dx.doi.org/10.1038/265137a0.
http://dx.doi.org/10.1038/265137a0...
; Araújo et al., 2007Araújo, V.A., Melo, S.K., Araújo, A.P., Gomes, M.L. and Carneiro, M.A., 2007. Relationship between invertebrate fauna and bromeliad size. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 67, no. 4, pp. 611-617. http://dx.doi.org/10.1590/S1519-69842007000400004. PMid:18278311.
http://dx.doi.org/10.1590/S1519-69842007...
). Studies of Guzmania spp. and Vriesia spp. have reported a linear relationship between leaf litter and plant cover (Richardson, 1999Richardson, B., 1999. The bromeliad microcosm and the assessment of faunal diversity in a Neotropical Forest. Biotropica, vol. 31, no. 2, pp. 321-336. http://dx.doi.org/10.1111/j.1744-7429.1999.tb00144.x.
http://dx.doi.org/10.1111/j.1744-7429.19...
). The sheath, which is the basal portion of the leaf, is the space in which the bromeliad retains water and litter received from the canopy; hence, an increase in sheath length leads to a greater tank size and a higher probability of retaining more leaf litter.

Bromeliads species vary in their traits associated with plant structure, such as diameter, leaf number, tank number, leaf length, and leaf width (e.g. Gonçalves-Souza et al., 2011Gonçalves-Souza, T., Almeida-Neto, M. and Romero, G.Q., 2011. Bromeliad architectural complexity and vertical distribution predict spider abundance and richness. Austral Ecology, vol. 36, no. 4, pp. 476-484. http://dx.doi.org/10.1111/j.1442-9993.2010.02177.x.
http://dx.doi.org/10.1111/j.1442-9993.20...
; Marino et al., 2013Marino, N.A.C., Srivastava, D.S. and Farjalla, V.F., 2013. Aquatic macroinvertebrate community composition in tank-bromeliads is determined by bromeliad species and its constrained characteristics. Insect Conservation and Diversity, vol. 6, no. 3, pp. 372-380. http://dx.doi.org/10.1111/j.1752-4598.2012.00224.x.
http://dx.doi.org/10.1111/j.1752-4598.20...
); moreover, these variations occur within-species (Zytynska et al., 2012Zytynska, S.E., Khudr, M.S., Harris, E. and Preziosi, R.F., 2012. Genetic effects of tank-forming bromeliads on the associated invertebrate community in a tropical forest ecosystem. Oecologia, vol. 170, no. 2, pp. 467-475. http://dx.doi.org/10.1007/s00442-012-2310-3. PMid:22466862.
http://dx.doi.org/10.1007/s00442-012-231...
). According to our results, bromeliads with differences in plant cover, leaf number, and sheath length would differ in the amount of intercepted litter, leading to a shift in bromeliad contribution to nutrient cycling and the spatial heterogeneity of litter distribution.

Overall, the variables that we found relevant to determine leaf litter amount in Tillandsia turneri are related to the area available for receiving leaf litter from the canopy, as well as to the number and size of tanks available for retaining the leaf litter. These models can be used to predict the energy input into the aquatic micro-ecosystem, which is known to affect community richness, complexity, and ecosystem functioning.

  • (With 1 figure)

References

  • Alvarez-Sanchez, J. and Guevara, S., 1999. Litter interception on Liebm. (Palmae) in a tropical rain forest. Astrocaryum mexicanumBiotropica, vol. 31, pp. 89-92. http://dx.doi.org/10.1111/j.1744-7429.1999.tb00119.x
    » http://dx.doi.org/10.1111/j.1744-7429.1999.tb00119.x
  • Anderson, D.R., 2008. Model based inference in the life sciences: a primer on evidence. New York: Springer Science. 208 p.
  • Anderson, N.H. and Sedell, J.R., 1979. Detritus processing by macroinvertebrates in stream ecosystems. Annual Review of Entomology, vol. 24, no. 1, pp. 351-377. http://dx.doi.org/10.1146/annurev.en.24.010179.002031
    » http://dx.doi.org/10.1146/annurev.en.24.010179.002031
  • Araújo, V.A., Melo, S.K., Araújo, A.P., Gomes, M.L. and Carneiro, M.A., 2007. Relationship between invertebrate fauna and bromeliad size. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 67, no. 4, pp. 611-617. http://dx.doi.org/10.1590/S1519-69842007000400004 PMid:18278311.
    » http://dx.doi.org/10.1590/S1519-69842007000400004
  • Armbruster, P., Hutchinson, R.A. and Cotgreave, P., 2002. Factors influencing community structure in a South American tank bromeliad fauna. Oikos, vol. 96, no. 2, pp. 225-234. http://dx.doi.org/10.1034/j.1600-0706.2002.960204.x
    » http://dx.doi.org/10.1034/j.1600-0706.2002.960204.x
  • Benzing, D.H. and Renfrow, A., 1974. The nutritional status of and on . Encyclia tampensisTillandsia circinata,Taxodium ascendens, and the availability of nutrients to epiphytes on this host in south FloridaBulletin of the Torrey Botanical Club, vol. 101, no. 4, pp. 191-197. http://dx.doi.org/10.2307/2484643
    » http://dx.doi.org/10.2307/2484643
  • Benzing, D.H., 1980. The biology of bromeliads. California: Mad River Press, Eureka. 305 p.
  • Benzing, D.H., 1990. Vascular epiphytes. Cambridge: Cambridge University Press. 354 p.
  • Benzing, D.H., 2000. Bromeliaceae: profile of an adaptive radiation. Cambridge: Cambridge University Press. 710 p.
  • Chevan, A. and Sutherland, M., 1991. Hierarchical partitioning. The American Statistician, vol. 45, no. 2, pp. 90-96. http://dx.doi.org/10.2307/2684366
    » http://dx.doi.org/10.2307/2684366
  • Cruz-Ruiz, G.I., Mondragón, D. and Santos-Moreno, A., 2012. The presence of Abronia oaxacae (Squamata: Anguidae) in tank bromeliads in temperate forests of Oaxaca, México. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 72, no. 2, pp. 337-341. http://dx.doi.org/10.1590/S1519-69842012000200015 PMid:22735142.
    » http://dx.doi.org/10.1590/S1519-69842012000200015
  • Estevez Varon, J.V. and Viña, A., 1999. Producción y Descomposición de hojarasca en Tres Estadios sucesionales de un Bosque de montaña en el Municipio de Chocontá, Cundinamarca, Colombia. Bogotá: Fondo FEN. 65 p. Informe.
  • Frank, J.H., 1983. Bromeliad phytotelmata and their biota, especially mosquitos. In: H. Frank and P.L. Lounibos, eds. Phytotelmata: terrestrial plants as hosts of aquatic insects communities. New Jersey: Plexus, Inc., pp. 101-128.
  • Gonçalves-Souza, T., Almeida-Neto, M. and Romero, G.Q., 2011. Bromeliad architectural complexity and vertical distribution predict spider abundance and richness. Austral Ecology, vol. 36, no. 4, pp. 476-484. http://dx.doi.org/10.1111/j.1442-9993.2010.02177.x
    » http://dx.doi.org/10.1111/j.1442-9993.2010.02177.x
  • Hattenschwiler, S., Tiunov, A.V. and Scheu, S., 2005. Biodiversity and litter decomposition in terrestrial ecosystems. Annual Review of Ecology Evolution and Systematics, vol. 36, no. 1, pp. 191-218. http://dx.doi.org/10.1146/annurev.ecolsys.36.112904.151932
    » http://dx.doi.org/10.1146/annurev.ecolsys.36.112904.151932
  • Holdridge, L.R., 1967. Life zone ecology. San José, Costa Rica: Tropical Science Center. 216 p.
  • Isaza, C., Betancur, J. and Estévez Varón, J.V., 2004. Vertical distribution of bromeliads in a montane forest in the Eastern cordillera of the colombian Andes. Selbyana, vol. 25, no. 1, pp. 126-137.
  • Lasso, E. and Ackerman, J.D., 2013. Nutrient limitation restricts growth and reproductive output in a tropical montane cloud forest bromeliad: findings from a long-term forest fertilization experiment. Oecologia, vol. 171, no. 1, pp. 165-174. http://dx.doi.org/10.1007/s00442-012-2403-z PMid:22767363.
    » http://dx.doi.org/10.1007/s00442-012-2403-z
  • Lawton, J.H. and Schröder, D., 1977. Effects of plant type, size of geographical range and taxonomic isolation on number of insect species with British plants. Nature, vol. 265, no. 5590, pp. 137-140. http://dx.doi.org/10.1038/265137a0
    » http://dx.doi.org/10.1038/265137a0
  • Lodge, D.J., 1996. Microorganisms. In: D.P. REAGAN and R.B. WAIDE, eds. The food web of a tropical rain forest. Chicago: University of Chicago Press, pp. 53-108.
  • Lugo, A.E. and SCATENA, F.N., 1992. Epiphytes and climate change research in the caribbean: a proposal. Selbyana, vol. 13, pp. 123-130.
  • Maloney, D.C. and Lamberti, G.A., 1995. Rapid decomposition of summer input leaves in a northern Michigan stream. American Midland Naturalist, vol. 133, no. 1, pp. 184-195. http://dx.doi.org/10.2307/2426360
    » http://dx.doi.org/10.2307/2426360
  • Marino, N.A.C., Srivastava, D.S. and Farjalla, V.F., 2013. Aquatic macroinvertebrate community composition in tank-bromeliads is determined by bromeliad species and its constrained characteristics. Insect Conservation and Diversity, vol. 6, no. 3, pp. 372-380. http://dx.doi.org/10.1111/j.1752-4598.2012.00224.x
    » http://dx.doi.org/10.1111/j.1752-4598.2012.00224.x
  • Montero, G., Feruglio, C. and Barberis, I.M., 2010. The phytotelmata and foliage macrofauna assemblages of a bromeliad species in different habitats and seasons. Insect Conservation and Diversity, vol. 3, no. 2, pp. 92-102. http://dx.doi.org/10.1111/j.1752-4598.2009.00077.x
    » http://dx.doi.org/10.1111/j.1752-4598.2009.00077.x
  • Ngai, J.T. and Srivastava, D.S., 2006. Predators accelerate nutrient cycling in a bromeliad ecosystem. Science, vol. 314, no. 5801, pp. 963. http://dx.doi.org/10.1126/science.1132598 PMid:17095695.
    » http://dx.doi.org/10.1126/science.1132598
  • Ospina, M.F., Estevez Varon, J.V., Betancur, J. and Realpe, E., 2004. Macroinvertebrados acuáticos asociados a la bromelia en un bosque altoandino. Tillandsia turneriRevista Acta Zoológica Mexicana, vol. 20, no. 1, pp. 153-166.
  • Ospina, M.F., Estevez Varon, J.V., Realpe, E. and Gast, F., 2008. Diversidad de invertebrados acuáticos asociados a Bromeliaceae en un bosque de montaña. Revista Colombiana de Entomologia, vol. 34, no. 2, pp. 224-229.
  • R DEVELOPMENT CORE TEAM2013R: a language and environment for statistical computingViennaR Foundation Statistical Computing
  • Richardson, B., 1999. The bromeliad microcosm and the assessment of faunal diversity in a Neotropical Forest. Biotropica, vol. 31, no. 2, pp. 321-336. http://dx.doi.org/10.1111/j.1744-7429.1999.tb00144.x
    » http://dx.doi.org/10.1111/j.1744-7429.1999.tb00144.x
  • Richardson, B., Rogers, C. and Richardson, M.J., 2000. Nutrients, diversity, and community structure of two phytotelm systems in a lower montane forest, Puerto Rico. Ecological Entomology, vol. 25, no. 3, pp. 348-356. http://dx.doi.org/10.1046/j.1365-2311.2000.00255.x
    » http://dx.doi.org/10.1046/j.1365-2311.2000.00255.x
  • Saha, N., Aditya, G. and Saha, G.K., 2009. Habitat complexity reduces prey vulnerability: an experimental analysis using aquatic insect predators and immature dipteran prey. Journal of Asia-Pacific Entomology, vol. 12, no. 4, pp. 233-239. http://dx.doi.org/10.1016/j.aspen.2009.06.005
    » http://dx.doi.org/10.1016/j.aspen.2009.06.005
  • Srivastava, D., 2006. Habitat structure, trophic structure and ecosystem function: interactive effects in a bromeliad–insect community. Oecologia, vol. 149, no. 3, pp. 493-504. http://dx.doi.org/10.1007/s00442-006-0467-3 PMid:16896779.
    » http://dx.doi.org/10.1007/s00442-006-0467-3
  • Swift, M.J., HEAL, O.W. and ANDERSON, J.M., 1979. Decomposition in terrestrial ecosystems. Oxford: Blackwell Scientific. 372 p. Studies in Ecology, no. 5.
  • Yanoviak, S.P., 1999. Effects of leaf litter species on macroinvertebrate community properties and mosquito yield in Neotropical tree hole microcosms. Oecologia, vol. 120, no. 1, pp. 147-155. http://dx.doi.org/10.1007/s004420050843
    » http://dx.doi.org/10.1007/s004420050843
  • Zotz, G. and Vera, T., 1999. How much water is in the tank? Model calculations for two epiphytic bromeliads. Annals of Botany, vol. 83, no. 2, pp. 183-192. http://dx.doi.org/10.1006/anbo.1998.0809
    » http://dx.doi.org/10.1006/anbo.1998.0809
  • Zytynska, S.E., Khudr, M.S., Harris, E. and Preziosi, R.F., 2012. Genetic effects of tank-forming bromeliads on the associated invertebrate community in a tropical forest ecosystem. Oecologia, vol. 170, no. 2, pp. 467-475. http://dx.doi.org/10.1007/s00442-012-2310-3 PMid:22466862.
    » http://dx.doi.org/10.1007/s00442-012-2310-3

Publication Dates

  • Publication in this collection
    03 May 2016
  • Date of issue
    Jul-Sep 2016

History

  • Received
    12 Dec 2014
  • Accepted
    17 June 2015
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