Effects of bromeliad flowering event on the community structuring of aquatic insect larvae associated with phytotelmata of <i>Aechmea distichantha</i> Lem. (Bromeliaceae)

Amadeo, Felipe Emiliano; Dias, Juliana Déo; Segovia, Bianca Trevizan; Simões, Nadson Ressyé; Lansac-Tôha, Fábio Amodêo

doi:10.1590/S2179-975X3417

Abstracts

Abstract

Aim: We aimed to understand how aquatic insect larvae communities associated with bromeliad phytotelmata are affected by plant architecture, predators and resources (local factors), and by geographical distance (regional factors) in two different plant phenological phases. Bromeliad flowering results in plant structural changes, which favours insect dispersal. Considering that local and regional factors may affect the community of aquatic insect larvae, we expected that composition, beta diversity and the importance of those factors would differ in the vegetative growth and flowering phases.

Methods

We performed six samplings of the bromeliad associated fauna in 2010, three during the first semester - vegetative growth phase - and three during the second semester - flowering phase. In each sampling, we collected 12 plants along the rocky walls with similar location distribution, with a total of 72 bromeliads studied.

Results

Although beta diversity (PERMDISP) did not differ between vegetative growth and flowering, NMDS followed by ANOSIM showed that composition was significantly different in the distinct phenological phases. IndVal results showed that three Diptera morphospecies were discriminant of the vegetative growth phase. In addition, pRDA revealed differences in the relative contribution of local and regional factors to explain insect larvae community structure. During the flowering phase, local factors predominated, while during vegetative growth, regional factors were more important.

Conclusion

Differences in dispersal rates between the two phenological phases, likely due to adult insect pollination and further oviposition, influenced community structuring. Therefore, flowering events account for differences not only in the composition, but also in community structuring of aquatic insect larvae inhabiting the phytotelmata of Aechmea distichantha Lem. (Bromeliaceae).

Keywords:
assembly rules; environmental component; spatial component; inflorescence

Resumo

Objetivo: Esse estudo teve por objetivo entender como as comunidades de larvas de insetos aquáticas associadas aos fitotelmata são afetadas pela arquitetura da planta, presença de predadores e de recursos (fatores locais) e pela distância geográfica (fator regional) em duas fases fenológicas distintas. A floração de bromélias resulta em alterações estruturais nas plantas, que favorecem o aumento na dispersão de insetos. Considerando que tanto fatores locais quanto regionais podem afetar a comunidade de larvas de insetos aquáticas, nós esperamos que a composição, diversidade Beta e a importância desses fatores sejam diferentes entre as fases de crescimento vegetativo e de floração.

Métodos

Foram realizadas seis amostragens da fauna associada (insetos adultos e larvas) de bromélias em 2010, três durante o primeiro semestre - fase de crescimento vegetativo - e três durante o segundo semestre - fase de floração. Foram amostradas 12 plantas distribuídas de forma similar nos paredões rochosos por coleta, totalizando 72 bromélias.

Resultados

Embora a diversidade beta (PERMDISP) não tenha diferido entre as fases de crescimento vegetativo e de floração, a NMDS seguida pela ANOSIM demonstrou que a composição foi significativamente diferente entre as distintas fases fenológicas. Os resultados da IndVal mostraram que três espécies de Diptera foram discriminantes da fase de crescimento vegetativo. A pRDA revelou que diferenças na contribuição relativa dos fatores locais e regionais para explicar a estrutura da comunidade de larvas de insetos aquáticas. Na fase de floração, os fatores locais predominaram, enquanto que durante a fase de crescimento vegetativo, os fatores regionais foram os mais importantes.

Conclusão

Diferenças nas taxas de dispersão nas duas fases fenológicas, provavelmente em função da polinização e consequente oviposição, influenciaram a estruturação da comunidade. Assim, os eventos de floração não só influenciam na composição, mas também na estruturação da comunidade de larvas aquáticas presentes nos fitotelmata de Aechmea distichantha Lem. (Bromeliaceae).

Palavras-chave:
regras de montagem de comunidades; componente ambiental; componente espacial; inflorescência

1. Introduction

Natural communities may be regulated by local factors, such as competition, disturbances, biotic and abiotic variables, and regional factors, such as geographical distance among patches, dispersal capacity among habitats and climate conditions (Hillebrand & Blenckner, 2002HILLEBRAND, H. and BLENCKNER, T. Regional and local impact on species diversity - from pattern to processes. Oecologia, 2002, 132(4), 479-491. PMid:28547633. http://dx.doi.org/10.1007/s00442-002-0988-3.
http://dx.doi.org/10.1007/s00442-002-098... ; Cottenie et al., 2003COTTENIE, K., MICHELS, E., NUYTTEN, N. and DE MEESTER, L. Zooplankton Metacommunity structure: regional vs. local processes in highly interconnected ponds. Ecology, 2003, 84(4), 991-1000. http://dx.doi.org/10.1890/0012-9658(2003)084[0991:ZMSRVL]2.0.CO;2.
http://dx.doi.org/10.1890/0012-9658(2003... ; Paradise et al., 2008PARADISE, C.J., BLUE, J.D., BURKHART, J.Q., GOLDBERG, J., HARSHAW, L., HAWKINS, K.D., KEGAN, B., KRENTZ, T., SMITH, L. and VILLALPANDO, S. Local and regional factors influence the structure of treehole metacommunities. BMC Ecology, 2008, 8(1), 22. PMid:19099587. http://dx.doi.org/10.1186/1472-6785-8-22.
http://dx.doi.org/10.1186/1472-6785-8-22... ). These processes, acting in broad temporal and spatial scales, are important in determining diversity patterns and define the aspects of the regional species pool from where local communities are assembled (Caley & Schluter, 1997CALEY, M.J. and SCHLUTER, D. The relationship between local and regional diversity. Ecology, 1997, 78(1), 70-80. http://dx.doi.org/10.1890/0012-9658(1997)078[0070:TRBLAR]2.0.CO;2.
http://dx.doi.org/10.1890/0012-9658(1997... ).

The area in which the species pool is inserted has a fundamental role in the analysis of local and regional factors since it affects richness estimates (species-area relationship) and the scales in which species interact (ecological factors; Hillebrand & Blenckner, 2002HILLEBRAND, H. and BLENCKNER, T. Regional and local impact on species diversity - from pattern to processes. Oecologia, 2002, 132(4), 479-491. PMid:28547633. http://dx.doi.org/10.1007/s00442-002-0988-3.
http://dx.doi.org/10.1007/s00442-002-098... ). However, area extension is generally difficult to be determined (Srivastava, 1999SRIVASTAVA, D. Using local-regional richness plots to test for species saturation: pitfalls and potentials. Journal of Animal Ecology, 1999, 68(1), 1-16. http://dx.doi.org/10.1046/j.1365-2656.1999.00266.x.
http://dx.doi.org/10.1046/j.1365-2656.19... ), thus, most studies use a large randomly chosen area (Caley & Schluter, 1997CALEY, M.J. and SCHLUTER, D. The relationship between local and regional diversity. Ecology, 1997, 78(1), 70-80. http://dx.doi.org/10.1890/0012-9658(1997)078[0070:TRBLAR]2.0.CO;2.
http://dx.doi.org/10.1890/0012-9658(1997... ) or an area that is naturally delimited by landscape geography (Oberdorff et al., 1998OBERDORFF, T., HUGUENY, B., COMPIN, A. and BELKESSAM, D. Non-interactive fish communities in the coastal streams of Northwestern France. Journal of Animal Ecology, 1998, 67(3), 472-484. http://dx.doi.org/10.1046/j.1365-2656.1998.00211.x.
http://dx.doi.org/10.1046/j.1365-2656.19... ). Therefore, the difficulty in manipulating communities reduces the possibility of testing the predictions on the influence of local and regional factors on organismal diversity (Hillebrand & Blenckner, 2002HILLEBRAND, H. and BLENCKNER, T. Regional and local impact on species diversity - from pattern to processes. Oecologia, 2002, 132(4), 479-491. PMid:28547633. http://dx.doi.org/10.1007/s00442-002-0988-3.
http://dx.doi.org/10.1007/s00442-002-098... ).

Phytotelmata are small aquatic habitats naturally formed in plants (i. e. bromeliads), which can contain associated organisms (Srivastava et al., 2004SRIVASTAVA, D.S., KOLASA, J., BENGTSSON, J., GONZALEZ, A., LAWLER, S.P., MILLER, T.E., MUNGUIA, P., ROMANUK, T., SCHNEIDER, D.C. and TRZCINSKI, M.K. Are natural microcosms useful model systems for ecology? Trends in Ecology & Evolution, 2004, 19(7), 379-384. PMid:16701289. http://dx.doi.org/10.1016/j.tree.2004.04.010.
http://dx.doi.org/10.1016/j.tree.2004.04... ; Williams, 2006WILLIAMS, D.D. The biology of temporary waters. Oxford: Oxford University Press, 2006.; Brouard et al., 2012BROUARD, O., CÉRÉGHINO, R., CORBARA, B., LEROY, C., PELOZUELO, L., DEJEAN, A. and CARRIAS, J.-F. Understorey environments influence functional diversity in tank-bromeliad ecosystems. Freshwater Biology, 2012, 57(4), 815-823. http://dx.doi.org/10.1111/j.1365-2427.2012.02749.x.
http://dx.doi.org/10.1111/j.1365-2427.20... ). Those habitats may be considered ideal model systems for the study of ecological processes affecting species diversity in natural communities (Srivastava, 2006SRIVASTAVA, D. Habitat structure, trophic structure and ecosystem function: interactive effects in a bromeliad–insect community. Oecologia, 2006, 149(3), 493-504. PMid:16896779. http://dx.doi.org/10.1007/s00442-006-0467-3.
http://dx.doi.org/10.1007/s00442-006-046... ), from community assembly rules (Céréghino et al., 2011CÉRÉGHINO, R., LEROY, C., CARRIAS, J.F., PELOZUELO, L., SÉGURA, C., BOSC, C., DEJEAN, A. and CORBARA, B. Ant-plant mutualisms promote functional diversity in phytotelm communities. Functional Ecology, 2011, 25(5), 954-963. http://dx.doi.org/10.1111/j.1365-2435.2011.01863.x.
http://dx.doi.org/10.1111/j.1365-2435.20... ; Dézerald et al., 2014DÉZERALD, O., TALAGA, S., LEROY, C., CARRIAS, J.F., CORBARA, B., DEJEAN, A. and CÉRÉGHINO, R. Environmental determinants of macroinvertebrate diversity in small water bodies: insights from tank-bromeliads. Hydrobiologia, 2014, 723(1), 77-86. http://dx.doi.org/10.1007/s10750-013-1464-2.
http://dx.doi.org/10.1007/s10750-013-146... ) to the relationships between diversity and ecosystem functioning (Srivastava & Bell, 2009SRIVASTAVA, D. and BELL, T. Reducing horizontal and vertical diversity in a food web triggers extinctions and impacts functions. Ecology Letters, 2009, 12(10), 1016-1028. PMid:19702635. http://dx.doi.org/10.1111/j.1461-0248.2009.01357.x.
http://dx.doi.org/10.1111/j.1461-0248.20... ; Romero & Srivastava, 2010ROMERO, G.Q. and SRIVASTAVA, D.S. Food-web composition affects cross-ecosystem interactions and subsidies. Journal of Animal Ecology, 2010, 79(5), 1122-1131. PMid:20584097. http://dx.doi.org/10.1111/j.1365-2656.2010.01716.x.
http://dx.doi.org/10.1111/j.1365-2656.20... ), since each phytotelmata can be considered as a unique small habitat with well-defined frontiers (Schulz et al., 2012SCHULZ, G., SIQUEIRA, T., STEFAN, G. and ROQUE, F.O. Passive and active dispersers respond similarly to environmental and spatial processes: an example from metacommunity dynamics of tree hole invertebrates. Fundamental and Applied Limnology, 2012, 181(4), 315-326. http://dx.doi.org/10.1127/1863-9135/2012/0365.
http://dx.doi.org/10.1127/1863-9135/2012... ), naturally replicated in the environment and composed by taxonomically diverse fauna with multiple trophic levels (Armbruster et al., 2002ARMBRUSTER, P., HUTCHINSON, R.A. and COTGREAVE, P. Factors influencing community structure in a South American tank bromeliad fauna. Oikos, 2002, 96(2), 225-234. http://dx.doi.org/10.1034/j.1600-0706.2002.960204.x.
http://dx.doi.org/10.1034/j.1600-0706.20... ).

Several species occupying phytotelmata are endemic, dominated by aquatic insect larvae which emerge from bromeliad tanks as terrestrial winged adults (Romero & Srivastava, 2010ROMERO, G.Q. and SRIVASTAVA, D.S. Food-web composition affects cross-ecosystem interactions and subsidies. Journal of Animal Ecology, 2010, 79(5), 1122-1131. PMid:20584097. http://dx.doi.org/10.1111/j.1365-2656.2010.01716.x.
http://dx.doi.org/10.1111/j.1365-2656.20... ). Rainfall water accumulated in bromeliad tanks throughout the year, together with leaf litter and other organic detritus, provide nutrients and spatial refuge to the associated community (Armbruster et al., 2002ARMBRUSTER, P., HUTCHINSON, R.A. and COTGREAVE, P. Factors influencing community structure in a South American tank bromeliad fauna. Oikos, 2002, 96(2), 225-234. http://dx.doi.org/10.1034/j.1600-0706.2002.960204.x.
http://dx.doi.org/10.1034/j.1600-0706.20... ; Torreias & Ferreira-Keppler, 2011TORREIAS, S.R.S. and FERREIRA-KEPPLER, R.L. Macroinvertebrates inhabiting the tank leaf terrestrial and epiphyte bromeliads at Reserva Adolpho Ducke, Manaus, Amazonas. Brazilian Archives of Biology and Technology, 2011, 54(6), 1193-1202. http://dx.doi.org/10.1590/S1516-89132011000600015.
http://dx.doi.org/10.1590/S1516-89132011... ).

In this way, communities inhabiting bromeliad tanks may be affected by several factors, such as resource availability and predation within those environments, geographical distance among plants and habitat conditions (Montero et al., 2010MONTERO, G., FERUGLIO, C. and BARBERIS, I.M. The phytotelmata and foliage macrofauna assemblages of a bromeliad species in different habitats and seasons. Insect Conservation and Diversity, 2010, 3(2), 92-102. http://dx.doi.org/10.1111/j.1752-4598.2009.00077.x.
http://dx.doi.org/10.1111/j.1752-4598.20... ). Habitat conditions are directly affected by plant development, since different ontogenetic phases (i. e. vegetative growth, flowering, and fruiting) leads to structural and physiological changes throughout bromeliad growth (Cavallero et al., 2009CAVALLERO, L., LÓPEZ, D. and BARBERIS, I.M. Morphological variation of Aechmea distichantha (Bromeliaceae) in a Chaco forest: habitat and size-related effects. Plant Biology, 2009, 11(3), 379-391. PMid:19470109. http://dx.doi.org/10.1111/j.1438-8677.2008.00123.x.
http://dx.doi.org/10.1111/j.1438-8677.20... ).

Flowering events are accompanied by structural modifications in the three-dimensional architecture of bromeliad leaf rosette, which fold back their leaves allowing pollinators a better access to the inflorescence (Romero & Vasconcellos-Neto, 2005bROMERO, G.Q. and VASCONCELLOS-NETO, J. Spatial distribution and microhabitat preference of Psecas chapoda (Peckham & Peckham) (Araneae, Salticidae). The Journal of Arachnology, 2005b, 33(1), 124-134. http://dx.doi.org/10.1636/M03-9.
http://dx.doi.org/10.1636/M03-9... ). Those modifications affect various characteristics of those microhabitats, such as the amount of water and organic matter accumulated and evapotranspiration rates (Zotz & Thomas, 1999ZOTZ, G. and THOMAS, V. How much water is in the tank? Model calculations for two epiphytic bromeliads. Annals of Botany, 1999, 83(2), 183-192. http://dx.doi.org/10.1006/anbo.1998.0809.
http://dx.doi.org/10.1006/anbo.1998.0809... ). Therefore, bromeliads become less suitable to some of the associated organisms (i.e. predators: spiders - Romero & Vasconcellos-Neto, 2005aROMERO, G.Q. and VASCONCELLOS-NETO, J. The effects of plant structure on the spatial and microspatial distribution of a bromeliad-living jumping spider (Salticidae). Journal of Animal Ecology, 2005a, 74(1), 12-21. http://dx.doi.org/10.1111/j.1365-2656.2004.00893.x.
http://dx.doi.org/10.1111/j.1365-2656.20... ), consequently altering community structure (Srivastava, 2006SRIVASTAVA, D. Habitat structure, trophic structure and ecosystem function: interactive effects in a bromeliad–insect community. Oecologia, 2006, 149(3), 493-504. PMid:16896779. http://dx.doi.org/10.1007/s00442-006-0467-3.
http://dx.doi.org/10.1007/s00442-006-046... ; Gonçalves-Souza, et al., 2010GONÇALVES-SOUZA, T., BRESCOVIT, A.D., ROSSA-FERES, D.C. and ROMERO, G.Q. Bromeliads as biodiversity amplifiers and habitat segregation of spider communities in a Neotropical rainforest. The Journal of Arachnology, 2010, 38(2), 270-279. http://dx.doi.org/10.1636/P09-58.1.
http://dx.doi.org/10.1636/P09-58.1... , 2011GONÇALVES-SOUZA, T., ALMEIDA-NETO, M. and ROMERO, G.Q. Bromeliad architectural complexity and vertical distribution predict spider abundance and richness. Austral Ecology, 2011, 36(4), 476-484. http://dx.doi.org/10.1111/j.1442-9993.2010.02177.x.
http://dx.doi.org/10.1111/j.1442-9993.20... ).

In addition, flowering events enhances insect visitation, which are pollinators or feed on floral nectar (Frank & Lounibos, 2009FRANK, J.H. and LOUNIBOS, L.P. Insects and allies associated with bromeliads: a review. Terrestrial Arthropod Reviews, 2009, 1(2), 125-153. PMid:20209047. http://dx.doi.org/10.1163/187498308X414742.
http://dx.doi.org/10.1163/187498308X4147... ). The presence of floral stimuli produced by the plants (floral volatiles) reach long distances attracting pollinators (Reisenman et al., 2010REISENMAN, C.E., RIFFELL, J.A., BERNAYS, E.A. and HILDEBRAND, J.G. Antagonistic effects of floral scent in an insect–plant interaction. Proceedings of the Royal Society of London. Series B, Biological Sciences, 2010, 277(1692), 2371-2379. PMid:20335210.) increasing dispersal rates and colonization among plants (Kneitel & Miller, 2003KNEITEL, J.M. and MILLER, T.E. Dispersal rates affect species composition in metacommunities of Sarracenia purpurea inquilines. American Naturalist, 2003, 162(2), 165-171. PMid:12858261. http://dx.doi.org/10.1086/376585.
http://dx.doi.org/10.1086/376585... ). During the flowering phase, these stimuli (i. e. floral volatiles and nectar) are critical for insects to choose suitable oviposition sites, leading to higher rates of oviposition in the plants (Reisenman et al., 2010REISENMAN, C.E., RIFFELL, J.A., BERNAYS, E.A. and HILDEBRAND, J.G. Antagonistic effects of floral scent in an insect–plant interaction. Proceedings of the Royal Society of London. Series B, Biological Sciences, 2010, 277(1692), 2371-2379. PMid:20335210.) and decreasing the influence of spatial distance on the structure of the aquatic larvae associated to phytotelmata (Paradise et al., 2008PARADISE, C.J., BLUE, J.D., BURKHART, J.Q., GOLDBERG, J., HARSHAW, L., HAWKINS, K.D., KEGAN, B., KRENTZ, T., SMITH, L. and VILLALPANDO, S. Local and regional factors influence the structure of treehole metacommunities. BMC Ecology, 2008, 8(1), 22. PMid:19099587. http://dx.doi.org/10.1186/1472-6785-8-22.
http://dx.doi.org/10.1186/1472-6785-8-22... ).

Beta diversity (Whittaker, 1960WHITTAKER, R.H. Vegetation of the Siskiyou Mountains, Oregon and California. Ecological Monographs, 1960, 30(3), 279-338. http://dx.doi.org/10.2307/1943563.
http://dx.doi.org/10.2307/1943563... ; 1972WHITTAKER, R.H. Evolution and measurement of species diversity. Taxon, 1972, 21(2/3), 213-251. http://dx.doi.org/10.2307/1218190.
http://dx.doi.org/10.2307/1218190... ) can be defined as the variation in species composition among sampling units within a region (Anderson et al., 2006ANDERSON, M.J., ELLINGSEN, K.E. and MCARDLE, B.H. Multivariate dispersion as a measure of beta diversity. Ecology Letters, 2006, 9(6), 683-693. PMid:16706913. http://dx.doi.org/10.1111/j.1461-0248.2006.00926.x.
http://dx.doi.org/10.1111/j.1461-0248.20... ; Hill et al., 2017HILL, M.J., HEINO, J., THORNHILL, I., RYVES, D.B. and WOOD, P.J. Effects of dispersal mode on the environmental and spatial correlates of nestedness and species turnover in pond communities. Oikos, 2017. In press. http://dx.doi.org/10.1111/oik.04266.
http://dx.doi.org/10.1111/oik.04266... ). Several factors such as the habitat structure, degree of isolation, and the dispersal capacity of the organisms may affect beta diversity (Gering & Crist, 2002GERING, J.C. and CRIST, T.O. The alpha-beta-regional relationship: providing new insights into local–regional patterns of species richness and scale dependence of diversity components. Ecology Letters, 2002, 5(3), 433-444. http://dx.doi.org/10.1046/j.1461-0248.2002.00335.x.
http://dx.doi.org/10.1046/j.1461-0248.20... ). In bromeliads, habitat structure influences the available niche space and offers a wide range of essential elements for the animals, such as reproduction, shelter, and foraging sites (Romero & Vasconcellos-Neto, 2005aROMERO, G.Q. and VASCONCELLOS-NETO, J. The effects of plant structure on the spatial and microspatial distribution of a bromeliad-living jumping spider (Salticidae). Journal of Animal Ecology, 2005a, 74(1), 12-21. http://dx.doi.org/10.1111/j.1365-2656.2004.00893.x.
http://dx.doi.org/10.1111/j.1365-2656.20... ; Romero, 2006). Although the three-dimensional vegetation structure is recognized for altering the patterns of beta diversity, how this influence occurs remains poorly understood (Zellweger et al., 2017ZELLWEGER, F., ROTH, T., BUGMANN, H. and BOLLMANN, K. Beta diversity of plants, birds and butterflies is closely associated with climate and habitat structure. Global Ecology and Biogeography, 2017, 26(8), 898-906. http://dx.doi.org/10.1111/geb.12598.
http://dx.doi.org/10.1111/geb.12598... ). Dispersal among habitats may affect species composition and diversity in different manners, at both local and regional scales (Kneitel & Miller, 2003KNEITEL, J.M. and MILLER, T.E. Dispersal rates affect species composition in metacommunities of Sarracenia purpurea inquilines. American Naturalist, 2003, 162(2), 165-171. PMid:12858261. http://dx.doi.org/10.1086/376585.
http://dx.doi.org/10.1086/376585... ). High dispersal rates assure a constant input of new colonizers in new areas (Winegardner et al., 2012WINEGARDNER, A.K., JONES, B.K., NG, I.S.Y., SIQUEIRA, T. and COTTENIE, K. The terminology of metacommunity ecology. Trends in Ecology & Evolution, 2012, 27(5), 253-254. PMid:22325446. http://dx.doi.org/10.1016/j.tree.2012.01.007.
http://dx.doi.org/10.1016/j.tree.2012.01... ; Heino et al., 2015HEINO, J., MELO, A.S. and BINI, L.M. Reconceptualising the beta diversity‐environmental heterogeneity relationship in running water systems. Freshwater Biology, 2015, 60(2), 223-235. http://dx.doi.org/10.1111/fwb.12502.
http://dx.doi.org/10.1111/fwb.12502... ), leading to the homogenization of community structure at a local scale, and consequently, to a decrease in beta diversity (Cadotte & Fukami, 2005CADOTTE, M.W. and FUKAMI, T. Dispersal, spatial scale, and species diversity in a hierarchically structured experimental landscape. Ecology Letters, 2005, 8(5), 548-557. PMid:21352459. http://dx.doi.org/10.1111/j.1461-0248.2005.00750.x.
http://dx.doi.org/10.1111/j.1461-0248.20... ). On the other hand, low dispersal rates prevent species to reach all habitats, even the ones suitable for their development (Winegardner et al., 2012WINEGARDNER, A.K., JONES, B.K., NG, I.S.Y., SIQUEIRA, T. and COTTENIE, K. The terminology of metacommunity ecology. Trends in Ecology & Evolution, 2012, 27(5), 253-254. PMid:22325446. http://dx.doi.org/10.1016/j.tree.2012.01.007.
http://dx.doi.org/10.1016/j.tree.2012.01... ; Heino et al., 2015HEINO, J., MELO, A.S. and BINI, L.M. Reconceptualising the beta diversity‐environmental heterogeneity relationship in running water systems. Freshwater Biology, 2015, 60(2), 223-235. http://dx.doi.org/10.1111/fwb.12502.
http://dx.doi.org/10.1111/fwb.12502... ), increasing beta diversity.

Considering that plant architecture, the presence of predators and resources (local factors) and geographical distance (regional factors) may affect the community structure of aquatic insect larvae in bromeliads, we expect that composition, β-diversity and the relative importance of local and regional factors would be different between vegetative growth and flowering phases. We tested the hypotheses that I) insect larvae composition is different between vegetative growth and flowering phases; II) β-diversity (dissimilarity) is lower during flowering, since this event increases dispersal of insects among plants and consequently enhances oviposition, leading to more homogeneous larvae communities; III) during flowering, local factors would be more important for the community structuring of aquatic insect larvae, since dispersal rates would be sufficient to allow an environmental control based on niche differentiation, while in the vegetative growth phase regional factors would be more influential, considering that dispersal limitation would result in spatially structured communities within the bromeliad phytotelmata.

2. Methods

2.1. Study area

The study area is located in the Paraná River basin, between the mouths of Paranapanema and Baia rivers. Sampling was performed at the left bank of the Paraná River (Porto Rico, PR, Brazil - 22°45’53.5”S 53°15’27.2”W and 22°43’11.5”S 53°10’46”W; Figure 1). The region is characterized by the asymmetry of both sides of the valley, with an elevated left bank marked by rocky walls and sparse flooded areas (Souza Filho & Stevaux, 2004SOUZA FILHO, E.E. and STEVAUX, J.C. Geomorphology of the Paraná River Floodplain in the reach between the Paranapanema and Ivaí Rivers. In: A.A. AGOSTINHO, L. RODRIGUES, L.C. GOMES, S.M. THOMAZ and L.E. MIRANDA, eds. Structure and functioning of the Paraná River and its flooplain. Maringá: Eduem, 2004, pp. 9-13.). These rocky walls provide a suitable habitat for the development of several epiphytic plants, such as the bromeliads.

Figure 1
Map showing the sampling sites at the left bank of the Paraná River.

Vegetation of the Upper Paraná River basin is inserted in the Atlantic Forest biome in fragments of semideciduous forests forming strings of riparian vegetation near the border of the Paraná River (Campos & Souza, 1997CAMPOS, J.B. and SOUZA, M.C. Vegetação. In: A.E.A.M. VAZZOLER, A.A. AGOSTINHO and N.S. HAHN, eds. A planície de inundação do alto rio Paraná: aspectos físicos, biológicos e socioeconômicos. Maringá: Eduem, 1997, pp. 331-342.; Souza & Kita, 2002SOUZA, M.C. and KITA, K.K. Formações vegetais ripárias da planície alagável do alto rio Paraná e Mato Grosso do Sul, Brasil. In: A.A. AGOSTINHO, S.M. THOMAZ, L. RODRIGUES and L.C. GOMES, eds. A planície de inundação do alto rio Paraná: Site 6. Maringá: Nupélia/PELD/CNPq, 2002, pp. 197-201.). Precipitation varies from 1400 to 1600 mm/year (maximum rainfall during summer), relative annual humidity is approximately 70% and the average temperature is 24 °C (IBGE, 1990INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA – IBGE. Geografia do Brasil: região sul. Rio de Janeiro: IBGE, 1990. vol. 2.; IAPAR, 2000INSTITUTO AGRONÔMICO DO PARANÁ – IAPAR. Cartas climáticas do Estado do Paraná. Londrina: IAPAR, 2000.).

2.2. Sampling

Aechmea distichantha Lem. (Bromeliaceae) was chosen because of the high density of this plant in the region. This facultative epiphytic bromeliad is widely distributed in South America, occurring from the sea level to 2,400 m altitude (Smith & Downs, 1979SMITH, L.B. and DOWNS, R.J. Bromelioideae (Bromeliaceae). Flora Neotropica, 1979, 14(3), 1493-2142.). According to Reitz (1983)REITZ, R. Bromeliáceas e a malária-bromélia endêmica. In: R. REITZ, ed. Flora Ilustrada Catarinense. Itajaí: BROM, 1983. 559 p., this Bromeliaceae is 40-100 cm height with few leaves (15 to 25) which grow in a rosette, forming water-collecting cisterns. The foliage has margins covered with thorns, with an acute ending. Water volume contained in the bromeliad tanks are on average 200 cm³. Flowering usually occurs between June and September, a period in which the plant exhibits a densely flowered inflorescence (70 to 330 flowers), lasting for 20 to 30 days (Scrok & Varassin, 2011SCROK, G.J. and VARASSIN, I.G. Reproductive biology and pollination of Aechmea distichantha Lem. (Bromeliaceae). Acta Botanica Brasílica, 2011, 25(3), 571-576. http://dx.doi.org/10.1590/S0102-33062011000300009.
http://dx.doi.org/10.1590/S0102-33062011... ).

We performed six samplings in 2010, three during the first semester - vegetative growth phase - and three during the second semester - flowering phase. In each sampling, we took 12 plants along the rocky walls with similar location distribution, with a total of 72 bromeliads studied. For each plant, geographical coordinates were taken. Using these data, a distance matrix was constructed, considering the distance (meters) from each plant in relation to the others (Spatial component). Measurements were taken using Google Earth.

Plants were manually removed from the rocky walls, wrapped in plastic bags and taken to Nupelia/University of Maringá Field Station, where the following measurements of the morphometric parameters were taken: height and width of the plant, perimeter, and height of the bromeliad tank and leaf number. Assuming that bromeliads approximated a geometric shape of a cone, we calculated the plant total volume (V_plant) and bromeliad tank total volume (V_tank) as cone volume, according to Armbruster et al. (2002)ARMBRUSTER, P., HUTCHINSON, R.A. and COTGREAVE, P. Factors influencing community structure in a South American tank bromeliad fauna. Oikos, 2002, 96(2), 225-234. http://dx.doi.org/10.1034/j.1600-0706.2002.960204.x.
http://dx.doi.org/10.1034/j.1600-0706.20... (Equation 1):

V = 1 / 3 π r^{2} h

(1)

where to calculate the total volume of the plant (V_plant), the radius of the plant (r_plant) was obtained by dividing plant width by two, and h_plant is the height from the base to the top of the central leave. To calculate bromeliad tank total volume (V_tank), bromeliad tank height (h_tank) was measured from the plant base to the interlocking of the more internal leaves. Bromeliad tank radius (r_tank) was calculated using the perimeter (plant perimeter/2 × π) (Figure 2).

Figure 2
Morphometric parameters measured in the plants (A) and bromeliad tank (B). Dashed lines represent plant measures used in our study.

Leaf number in each plant was considered a proxy of its complexity, since each leaf axil constitutes a discrete water body, compartmentalizing the internal space inside the bromeliad (Armbruster et al., 2002ARMBRUSTER, P., HUTCHINSON, R.A. and COTGREAVE, P. Factors influencing community structure in a South American tank bromeliad fauna. Oikos, 2002, 96(2), 225-234. http://dx.doi.org/10.1034/j.1600-0706.2002.960204.x.
http://dx.doi.org/10.1034/j.1600-0706.20... ). Water contained within each plant was carefully removed and inspected for macroinvertebrates (including aquatic insect larvae, spiders, ants, among others). Water volume from each bromeliad was further measured with graduated cylinder.

Sampling of the associated bromeliad fauna followed the protocol described by Armbruster et al. (2002)ARMBRUSTER, P., HUTCHINSON, R.A. and COTGREAVE, P. Factors influencing community structure in a South American tank bromeliad fauna. Oikos, 2002, 96(2), 225-234. http://dx.doi.org/10.1034/j.1600-0706.2002.960204.x.
http://dx.doi.org/10.1034/j.1600-0706.20... : leaves were cut near the base of the plant, removed, individually checked for more macroinvertebrates and then washed with distilled water inside a white tray. Associated fauna was fixed with 70% alcohol. Insects were sorted, counted and identified to larval and adult morphospecies in the zoology laboratory at Maringá State University. Diagnostic features used for assigning morphospecies were wing venation, structure of mouth parts, chaetotaxy, antennal segmentation and structure, tarsal structure and overall body form, according to Armbruster et al. (2002)ARMBRUSTER, P., HUTCHINSON, R.A. and COTGREAVE, P. Factors influencing community structure in a South American tank bromeliad fauna. Oikos, 2002, 96(2), 225-234. http://dx.doi.org/10.1034/j.1600-0706.2002.960204.x.
http://dx.doi.org/10.1034/j.1600-0706.20... . The classification of insect morphospecies into each order was based on Borror et al. (1989)BORROR, D.J., TRIPLEHORN, C.A. and JOHNSON, N.F. An introduction to the study of insects. New York: Harcodrt Brace Jobanovich Colleg Publishers, 1989.. Although the identification to morphospecies is common in studies on macroinvertebrate fauna associated with phytotelmata, there are some problems related to its use. For example, the adult and larvae of the same species are usually classified as different morphospecies. However, these different development stages may have different ecological niche, which justifies the identification of different development stages as different morphospecies to better comprehend the functional role of these organisms within phytotelmata (Armbruster et al., 2002ARMBRUSTER, P., HUTCHINSON, R.A. and COTGREAVE, P. Factors influencing community structure in a South American tank bromeliad fauna. Oikos, 2002, 96(2), 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.A., GOMES, M.L.M. and CARNEIRO, M.A.A. Relationship between invertebrate fauna and bromeliad size. Brazilian Journal of Microbiology, 2007, 67(4), 611-617. PMid:18278311.; Jabiol et al., 2009JABIOL, J., CORBARA, B., DEJEAN, A. and CÉRÉGHINO, R. Structure of aquatic insect communities in tank-bromeliads in a East-Amazonian rainforest in French Guiana. Forest Ecology and Management, 2009, 257(1), 351-360. http://dx.doi.org/10.1016/j.foreco.2008.09.010.
http://dx.doi.org/10.1016/j.foreco.2008.... ; Montero et al., 2010MONTERO, G., FERUGLIO, C. and BARBERIS, I.M. The phytotelmata and foliage macrofauna assemblages of a bromeliad species in different habitats and seasons. Insect Conservation and Diversity, 2010, 3(2), 92-102. http://dx.doi.org/10.1111/j.1752-4598.2009.00077.x.
http://dx.doi.org/10.1111/j.1752-4598.20... ).

Spiders (predators) were counted and identified at the family level in the Arachnology laboratory of Museu Paraense Emilio Goeldi (Belém, PA). Spiders were identified to morphospecies and identification was primarily based on the shape of adult female reproductive organs - epigyne. When spider families were composed only by juveniles, we considered those families to be composed of at least one taxon, and this criterion was used in all statistical analyses. Based on ecological characteristics of each family, spiders were grouped in “web weavers” and “hunters”.

To estimate ciliate density, water samples from each plant were analysed in vivo using an optic microscope (for more details, see Buosi et al., 2015BUOSI, P.R.B., CABRAL, A.F., UTZ, L.R.P., VIEIRA, L.C.G. and VELHO, L.F.M. Effects of Seasonality and Dispersal on the Ciliate Community Inhabiting Bromeliad Phytotelmata in Riparian Vegetation of a Large Tropical River. The Journal of Eukaryotic Microbiology, 2015, 62(6), 737-749. PMid:25963550. http://dx.doi.org/10.1111/jeu.12232.
http://dx.doi.org/10.1111/jeu.12232... ).

2.3. Study system

Spiders and ants are among the most commonly arthropods found foraging on Bromeliaceae leaves (Montero et al., 2010MONTERO, G., FERUGLIO, C. and BARBERIS, I.M. The phytotelmata and foliage macrofauna assemblages of a bromeliad species in different habitats and seasons. Insect Conservation and Diversity, 2010, 3(2), 92-102. http://dx.doi.org/10.1111/j.1752-4598.2009.00077.x.
http://dx.doi.org/10.1111/j.1752-4598.20... ; Hénaut et al., 2014HÉNAUT, Y., CORBARA, B., PÉLOZUELO, L., AZÉMAR, F., CÉRÉGHINO, R., HERAULT, B. and DEJEAN, A. A tank bromeliad favors spider presence in a neotropical inundated forest. PLoS One, 2014, 9(12), e114592. PMid:25494055. http://dx.doi.org/10.1371/journal.pone.0114592.
http://dx.doi.org/10.1371/journal.pone.0... ) and may play an important role in structuring phytotelmata communities (Romero & Srivastava, 2010ROMERO, G.Q. and SRIVASTAVA, D.S. Food-web composition affects cross-ecosystem interactions and subsidies. Journal of Animal Ecology, 2010, 79(5), 1122-1131. PMid:20584097. http://dx.doi.org/10.1111/j.1365-2656.2010.01716.x.
http://dx.doi.org/10.1111/j.1365-2656.20... ; Céréghino et al., 2011CÉRÉGHINO, R., LEROY, C., CARRIAS, J.F., PELOZUELO, L., SÉGURA, C., BOSC, C., DEJEAN, A. and CORBARA, B. Ant-plant mutualisms promote functional diversity in phytotelm communities. Functional Ecology, 2011, 25(5), 954-963. http://dx.doi.org/10.1111/j.1365-2435.2011.01863.x.
http://dx.doi.org/10.1111/j.1365-2435.20... ). Considered as predators in these microhabitats (Romero & Srivastava, 2010ROMERO, G.Q. and SRIVASTAVA, D.S. Food-web composition affects cross-ecosystem interactions and subsidies. Journal of Animal Ecology, 2010, 79(5), 1122-1131. PMid:20584097. http://dx.doi.org/10.1111/j.1365-2656.2010.01716.x.
http://dx.doi.org/10.1111/j.1365-2656.20... ; Gonçalves et al., 2017GONÇALVES, A.Z., SRIVASTAVA, D.S., OLIVEIRA, P.S. and ROMERO, G.Q. Effects of predatory ants within and across ecosystems in bromeliad food webs. Journal of Animal Ecology, 2017, 86(4), 790-799. PMid:28342283. http://dx.doi.org/10.1111/1365-2656.12671.
http://dx.doi.org/10.1111/1365-2656.1267... ), spiders and ants may affect communities associated with bromeliad leaves and tanks, through the direct reduction in the abundance of prey (consumptive effects), or by altering the behaviour and use of these habitats by these organisms (non-consumptive effects) (Werner & Peacor, 2003WERNER, E. and PEACOR, S. A review of trait-mediated indirect interactions in ecological communities. Ecology, 2003, 84(5), 1083-1100. http://dx.doi.org/10.1890/0012-9658(2003)084[1083:AROTII]2.0.CO;2.
http://dx.doi.org/10.1890/0012-9658(2003... ; Hill & Weissburg, 2013HILL, J.M. and WEISSBURG, M.J. Predator biomass determines the magnitude of non-consumptive effects (NCEs) in both laboratory and field environments. Oecologia, 2013, 172(1), 79-91. PMid:23250631. http://dx.doi.org/10.1007/s00442-012-2488-4.
http://dx.doi.org/10.1007/s00442-012-248... ).

Associations between spiders and bromeliads are common in Neotropical regions (Romero, 2006) and the presence of these predators on the plants may repel pollinators, reducing bromeliad fitness (Gonçalves-Souza et al., 2008GONÇALVES-SOUZA, T., OMENA, P.M., SOUZA, J.C. and ROMERO, G.Q. Trait-mediated effects on flowers: artificial spiders deceive pollinators and decrease plant fitness. Ecology, 2008, 89(9), 2407-2413. PMid:18831161. http://dx.doi.org/10.1890/07-1881.1.
http://dx.doi.org/10.1890/07-1881.1... ). The presence of spiders in bromeliads could lead to a reduction in invertebrate diversity and abundance, changing the composition of the associated fauna, from a community dominated by aquatic insect larvae to a community dominated by other aquatic invertebrates (i.e. ostracods and oligochaete; Romero & Srivastava, 2010ROMERO, G.Q. and SRIVASTAVA, D.S. Food-web composition affects cross-ecosystem interactions and subsidies. Journal of Animal Ecology, 2010, 79(5), 1122-1131. PMid:20584097. http://dx.doi.org/10.1111/j.1365-2656.2010.01716.x.
http://dx.doi.org/10.1111/j.1365-2656.20... ). Therefore, the presence of these predators may affect not only aquatic organisms with complex life cycles (i. e. insects), but also those spending their whole life inside phytotelmata (Romero & Srivastava, 2010ROMERO, G.Q. and SRIVASTAVA, D.S. Food-web composition affects cross-ecosystem interactions and subsidies. Journal of Animal Ecology, 2010, 79(5), 1122-1131. PMid:20584097. http://dx.doi.org/10.1111/j.1365-2656.2010.01716.x.
http://dx.doi.org/10.1111/j.1365-2656.20... ).

Several ant species use bromeliads as shelter and sites for nest construction, and the interaction between the ants and these plants may be species-specific (Céréghino et al., 2011CÉRÉGHINO, R., LEROY, C., CARRIAS, J.F., PELOZUELO, L., SÉGURA, C., BOSC, C., DEJEAN, A. and CORBARA, B. Ant-plant mutualisms promote functional diversity in phytotelm communities. Functional Ecology, 2011, 25(5), 954-963. http://dx.doi.org/10.1111/j.1365-2435.2011.01863.x.
http://dx.doi.org/10.1111/j.1365-2435.20... ; Leroy et al., 2012LEROY, C., CORBARA, B., PÉLOZUELO, L., CARRIAS, J.-F., DEJEAN, A. and CÉRÉGHINO, R. Ant species identity mediates reproductive traits and allocation in an ant-garden bromeliad. Annals of Botany, 2012, 109(1), 145-152. PMid:21984729. http://dx.doi.org/10.1093/aob/mcr253.
http://dx.doi.org/10.1093/aob/mcr253... ; Talaga et al., 2015TALAGA, S., DÉZERALD, O., CARTERON, A., PETITCLERC, F., LEROY, C., CÉRÉGHINO, R. and DEJEAN, A. Tank bromeliads as natural microcosms: a facultative association with ants influences the aquatic invertebrate community structure. Comptes Rendus Biologies, 2015, 338(10), 696-700. PMid:26302833. http://dx.doi.org/10.1016/j.crvi.2015.05.006.
http://dx.doi.org/10.1016/j.crvi.2015.05... ; Gonçalves et al., 2017GONÇALVES, A.Z., SRIVASTAVA, D.S., OLIVEIRA, P.S. and ROMERO, G.Q. Effects of predatory ants within and across ecosystems in bromeliad food webs. Journal of Animal Ecology, 2017, 86(4), 790-799. PMid:28342283. http://dx.doi.org/10.1111/1365-2656.12671.
http://dx.doi.org/10.1111/1365-2656.1267... ). Although the presence of these organisms in bromeliads may result in some advantage for these plants, such as protection against herbivory or seed dispersal (Leroy et al., 2012LEROY, C., CORBARA, B., PÉLOZUELO, L., CARRIAS, J.-F., DEJEAN, A. and CÉRÉGHINO, R. Ant species identity mediates reproductive traits and allocation in an ant-garden bromeliad. Annals of Botany, 2012, 109(1), 145-152. PMid:21984729. http://dx.doi.org/10.1093/aob/mcr253.
http://dx.doi.org/10.1093/aob/mcr253... ), the predatory behaviour that ants exert on potential pollinators and colonizers may alter the structure of the associated aquatic and terrestrial communities (Gonçalves et al., 2017GONÇALVES, A.Z., SRIVASTAVA, D.S., OLIVEIRA, P.S. and ROMERO, G.Q. Effects of predatory ants within and across ecosystems in bromeliad food webs. Journal of Animal Ecology, 2017, 86(4), 790-799. PMid:28342283. http://dx.doi.org/10.1111/1365-2656.12671.
http://dx.doi.org/10.1111/1365-2656.1267... ).

Ciliates have a key role in the flow of energy and matter within bromeliad phytotelmata, being more efficient than metazoans in the nutrient remineralization in the water column (Carrias et al., 2001CARRIAS, J.F., CUSSAC, M.E. and CORBARA, B. A preliminary study of freshwater protozoa in tank bromeliads. Journal of Tropical Ecology, 2001, 17(4), 611-617. http://dx.doi.org/10.1017/S0266467401001456.
http://dx.doi.org/10.1017/S0266467401001... ). In this environment, ciliates can be considered as a proxy of organic matter (Carrias et al., 2001CARRIAS, J.F., CUSSAC, M.E. and CORBARA, B. A preliminary study of freshwater protozoa in tank bromeliads. Journal of Tropical Ecology, 2001, 17(4), 611-617. http://dx.doi.org/10.1017/S0266467401001456.
http://dx.doi.org/10.1017/S0266467401001... ; Petermann et al., 2015bPETERMANN, J.S., KRATINA, P., MARINO, N.A.C., MACDONALD, A.A.M. and SRIVASTAVA, D.S. Resources alter the structure and increase stochasticity in bromeliad microfauna communities. PLoS One, 2015b, 10(3), e0118952. PMid:25775464. http://dx.doi.org/10.1371/journal.pone.0118952.
http://dx.doi.org/10.1371/journal.pone.0... ), due to their efficiency in decomposing detritus (Kneitel & Miller, 2002KNEITEL, J.M. and MILLER, T.E. Resource and top predator regulation in the pitcher plant (Sarracenia purpurea) inquiline community. Ecology, 2002, 83(3), 680-688. http://dx.doi.org/10.1890/0012-9658(2002)083[0680:RATPRI]2.0.CO;2.
http://dx.doi.org/10.1890/0012-9658(2002... , 2003KNEITEL, J.M. and MILLER, T.E. Dispersal rates affect species composition in metacommunities of Sarracenia purpurea inquilines. American Naturalist, 2003, 162(2), 165-171. PMid:12858261. http://dx.doi.org/10.1086/376585.
http://dx.doi.org/10.1086/376585... ). Moreover, ciliates are in the intermediate trophic levels of phytotelmata food webs, being grazed by aquatic insect larvae (Kneitel & Miller, 2002KNEITEL, J.M. and MILLER, T.E. Resource and top predator regulation in the pitcher plant (Sarracenia purpurea) inquiline community. Ecology, 2002, 83(3), 680-688. http://dx.doi.org/10.1890/0012-9658(2002)083[0680:RATPRI]2.0.CO;2.
http://dx.doi.org/10.1890/0012-9658(2002... ).

Considering the importance of the several factors above mentioned for the community structuring of aquatic insect larvae in phytotelmata, spider and ant abundances (predators), ciliate density (resources) and plant morphometric parameters (plant height, plant total volume, leaf number, bromeliad tank height, bromeliad tank total volume and water volume) were considered as local factors (Environmental component) in this study.

2.4. Data analysis

To observe the effect of flowering events on the composition of insect larvae associated with A. distichantha (hypothesis I), we performed non-metric multi-dimensional scaling (NMDS; Clarke, 1993CLARKE, K.R. Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology, 1993, 18(1), 117-143. http://dx.doi.org/10.1111/j.1442-9993.1993.tb00438.x.
http://dx.doi.org/10.1111/j.1442-9993.19... ) using Jaccard distance (presence/absence data). NMDS rearranges objects in a space with a particular number of dimensions, reproducing the observed distances. Distortion of the two-dimension resolution is expressed by S value (stress): the nearer this value is to zero, the better is the adjustment among original distances and the configuration obtained by the analysis (Legendre & Legendre, 1998LEGENDRE, P. and LEGENDRE, L. Numerical ecology. Amsterdam: Elsevier, 1998.). Analysis of similarities (ANOSIM; Clarke, 1993CLARKE, K.R. Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology, 1993, 18(1), 117-143. http://dx.doi.org/10.1111/j.1442-9993.1993.tb00438.x.
http://dx.doi.org/10.1111/j.1442-9993.19... ) with 9,999 permutations was performed to verify statistical differences in the composition patterns observed in NMDS. ANOSIM is a procedure of non-parametric permutations based on the ranking of the dissimilarity matrix generated by NMDS, comparing the degree of separation within and between sample groups using R statistics. If R=0 there are no differences in community composition between groups, while R=1 indicates complete distinction between communities (Quinn & Keough, 2002QUINN, G. and KEOUGH, M. Experimental design and data analysis for biologists. Cambridge: Cambridge University Press, 2002.). These analyses were performed using PAST 2.17 (Paleontological Statistics Software Package for Education and Data Analysis - Hammer et al., 2001HAMMER, Ø., HARPER, D.A.T. and RYAN, P.D. PAST: paleontological statistics software package for education and data analysis [software]. Palaeontological Association, 2001. 9 p. [viewed 4 July 2016]. Available from: http://palaeo-electronica.org/2001_1/past/issue1_01.htm
http://palaeo-electronica.org/2001_1/pas... ).

Indicator morphospecies of vegetative growth and flowering phases were identified using Indicator Species Analysis (IndVal; Dufrêne & Legendre, 1997DUFRÊNE, M. and LEGENDRE, P. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecological Monographs, 1997, 67(3), 345-366.). This analysis combines relative abundance and frequency occurrence of each species, generating an indicator value varying between zero and one. The value is near one when all individuals of a species occur in all plants in a certain phenological phase. Significance (P<0.05) was tested by 1,000 random permutations.

Beta diversity of insect larvae associated with phytotelmata was measured through permutation test of multivariate homogeneity of groups dispersions (PERMIDISP, Anderson et al., 2006ANDERSON, M.J., ELLINGSEN, K.E. and MCARDLE, B.H. Multivariate dispersion as a measure of beta diversity. Ecology Letters, 2006, 9(6), 683-693. PMid:16706913. http://dx.doi.org/10.1111/j.1461-0248.2006.00926.x.
http://dx.doi.org/10.1111/j.1461-0248.20... ). The biological matrix with presence/absence data of insect larvae was transformed into a distance matrix based on Jaccard distance. In this analysis, beta diversity is measured as the mean dissimilarity of a sample in relation to the group centroid (Anderson et al., 2006ANDERSON, M.J., ELLINGSEN, K.E. and MCARDLE, B.H. Multivariate dispersion as a measure of beta diversity. Ecology Letters, 2006, 9(6), 683-693. PMid:16706913. http://dx.doi.org/10.1111/j.1461-0248.2006.00926.x.
http://dx.doi.org/10.1111/j.1461-0248.20... ), in our case, flowering and vegetative growth phases of A. distichantha (hypothesis II).

The relative importance of local and regional factors in the diversity of aquatic insect larvae associated with A. distichantha (hypothesis III) was evaluated through Partial Redundancy Analysis (pRDA; Legendre & Legendre, 1998LEGENDRE, P. and LEGENDRE, L. Numerical ecology. Amsterdam: Elsevier, 1998.; Legendre et al., 2005LEGENDRE, P., BORCARD, D. and PERES-NETO, P.R. Analyzing beta diversity: partitioning the spatial variation of community composition data. Ecological Monographs, 2005, 75(4), 435-450. http://dx.doi.org/10.1890/05-0549.
http://dx.doi.org/10.1890/05-0549... ). RDA is an extension of multiple regression analysis, with a dependent variable (insect larvae composition) and different explanatory matrices: local factors (environmental component using morphometric parameters, ciliate density and the abundances of ants, hunter spiders and web weaver spiders) and regional factors (spatial component using geographical distances). A Principal Coordinates of Neighbour Matrices (PCNM - Borcard & Legendre, 2002BORCARD, D. and LEGENDRE, P. All-scale spatial analysis of ecological data by means of principal coordinates of neighbour matrices. Ecological Modelling, 2002, 153(1-2), 51-68. http://dx.doi.org/10.1016/S0304-3800(01)00501-4.
http://dx.doi.org/10.1016/S0304-3800(01)... ; Borcard et al., 2004BORCARD, D., LEGENDRE, P., AVOIS-JACQUET, C. and TUOMISTO, H. Dissecting the spatial structure of ecological data at multiple scales. Ecology, 2004, 85(7), 1826-1832. http://dx.doi.org/10.1890/03-3111.
http://dx.doi.org/10.1890/03-3111... ; Diniz-Filho & Bini, 2005DINIZ-FILHO, J.A.F. and BINI, L.M. Modelling geographical patterns in species richness using eigenvector based spatial filters. Global Ecology and Biogeography, 2005, 14(2), 177-185. http://dx.doi.org/10.1111/j.1466-822X.2005.00147.x.
http://dx.doi.org/10.1111/j.1466-822X.20... ; Dray et al., 2006DRAY, S., LEGENDRE, P. and PERES-NETO, P.R. Spatial modelling: a comprehensive framework for principal coordinate analysis of neighbour matrices (PCNM). Ecological Modelling, 2006, 196(3-4), 483-493. http://dx.doi.org/10.1016/j.ecolmodel.2006.02.015.
http://dx.doi.org/10.1016/j.ecolmodel.20... ; Griffith & Peres-Neto, 2006GRIFFITH, D.A. and PERES-NETO, P.R. 2006 Spatial Modeling in Ecology: The Flexibility of Eigenfunction Spatial Analyses. Ecology, 2006, 87(10), 2603-2613. PMid:17089668. http://dx.doi.org/10.1890/0012-9658(2006)87[2603:SMIETF]2.0.CO;2.
http://dx.doi.org/10.1890/0012-9658(2006... ) was applied to a distance matrix (meters) and scores were used as explanatory variables of the spatial component. Abundance data was Hellinger transformed (Legendre & Gallagher, 2001LEGENDRE, P. and GALLAGHER, E.D. Ecologically meaningful transformations for ordination of species data. Oecologia, 2001, 129(2), 271-280. PMid:28547606. http://dx.doi.org/10.1007/s004420100716.
http://dx.doi.org/10.1007/s004420100716... ). The significance of the components was tested through 9,999 Monte Carlo randomizations (Borcard et al., 1992BORCARD, D., LEGENDRE, P. and DRAPEAU, P. Partialling out the spatial component of ecological variation. Ecology, 1992, 73(3), 1045-1055. http://dx.doi.org/10.2307/1940179.
http://dx.doi.org/10.2307/1940179... ) and R² adjusted values were considered. IndVal analysis, PERMDISP, PCNM and pRDA were performed in R software (R Development Core Team, 2013R DEVELOPMENT CORE TEAM. R: a language and environment for statistical computing [software]. Vienna: R Foundation for Statistical Computing, 2013 [viewed 4 July 2016]. Available from: http://www.r-project.org
http://www.r-project.org... ).

3. Results

Considering both phenological phases, we collected 3,481 insect larvae associated with A. distichantha, distributed in four orders and 16 morphospecies (Table 1). Diptera and Lepidoptera were the most representative orders, with seven morphospecies each. Coleoptera and Neuroptera showed only one morphospecies. Out of all the morphospecies registered, we verified that nine were common to both phenological phases (vegetative growth and flowering). Flowering showed the highest number of morphospecies (n=13), out of which four were exclusive. During vegetative growth, three morphospecies were exclusive, with a total of 12 morphospecies in this phase.

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Table 1
Morphospecies occurrence of aquatic insect larvae found in A. distichantha of the rocky walls at the left bank of the Paraná River (PR, Brazil) during both phenological phases.

Regarding the contribution of each order to total abundance, Coleoptera was the most representative, with around 96% total abundance registered (3,349 individuals), consisting of the Scirtidae family (vegetative growth: 1,446 ind.; flowering: 1,903 ind.). Highest values of abundance of the aquatic larvae community were registered in the flowering phase, with 1,959 individuals (56% of abundance). In the vegetative growth phase, 1,522 individuals were collected (44% of abundance).

NMDS results indicated a separation of morphospecies of aquatic insect larvae between vegetative growth and flowering phases (Figure 3; NMDS stress: 0.25). ANOSIM results confirmed significant differences in community composition between the phenological phases (R=0.12; p<0.001).

Figure 3
Non-metric multi-dimensional scaling (NMDS) ordination for phenological phases (vegetative growth and flowering), based on composition of insect larvae associated with A. distichantha in rocky walls.

According to IndVal results, only three morphospecies were considered discriminant and only in the vegetative growth phase: Diptera01 (IndVal: 0.49; p<0.01), Diptera02 (IndVal: 0.31 p=0.01) and Diptera05 (Indval: 0.22; p=0.01).

PERMDISP results showed no significant differences in beta diversity of insect larvae between the phenological phases (Figure 4), indicating that the variation in taxa composition is similar between flowering and vegetative growth phases.

Figure 4
Distances to centroid in vegetative growth and flowering phases.

pRDA revealed that different components affected insect larvae diversity in phytotelmata during vegetative growth and flowering phases (Table 2). As expected, local factors (environmental component) were more important for larvae community during flowering (19%), with the contribution of plant morphometric parameters (plant height and total volume) together with ciliate density as the main responsible for community structuring in this phenological phase (Table 3), whereas regional factors (spatial component) were not significant.

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Table 2
Variance partitioning showing the relative contribution of [a] pure spatial component, [b] shared component, and [c] pure environmental component. Residuals: non explained variation. X1= Spatial model and X2= Environmental model.

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Table 3
Environmental and spatial variables selected in pRDA analysis during each phenological phase (vegetative growth and flowering) of A. distichantha.

During vegetative growth, abundance of web weaver spiders and bromeliad tank total volume (environmental component), together with PCNMs 6 and 9 (spatial component) were selected to explain community variation (Table 3). However, only the spatial component (regional factors; 6%) was significant and explained community structuring of aquatic insect larvae during this phenological phase (Table 2).

4. Discussion

Throughout the study, we found 3,481 aquatic insect larvae in the phytotelmata, distributed in four orders and 16 morphospecies. Species composition was significant different between vegetative growth and flowering (hypothesis I), whereas beta diversity was not significant different between the two phenological phases (hypothesis II). The relative contribution of local and regional factors in structuring the insect larvae community (hypothesis III) was different between vegetative growth and flowering phases. During flowering, local factors predominated, whereas during vegetative growth, regional factors were more important.

Significant differences regarding insect larvae composition between vegetative growth and flowering phases may be explained by the differences in plant architecture and insect dispersal among bromeliads in the two phenological phases. During flowering, the structure of leaf rosette in bromeliads is modified to offer better access to pollinators (Romero & Vasconcellos-Neto, 2005aROMERO, G.Q. and VASCONCELLOS-NETO, J. The effects of plant structure on the spatial and microspatial distribution of a bromeliad-living jumping spider (Salticidae). Journal of Animal Ecology, 2005a, 74(1), 12-21. http://dx.doi.org/10.1111/j.1365-2656.2004.00893.x.
http://dx.doi.org/10.1111/j.1365-2656.20... , bROMERO, G.Q. and VASCONCELLOS-NETO, J. Spatial distribution and microhabitat preference of Psecas chapoda (Peckham & Peckham) (Araneae, Salticidae). The Journal of Arachnology, 2005b, 33(1), 124-134. http://dx.doi.org/10.1636/M03-9.
http://dx.doi.org/10.1636/M03-9... ). These modifications alter several plant morphological parameters (Zotz & Thomas, 1999ZOTZ, G. and THOMAS, V. How much water is in the tank? Model calculations for two epiphytic bromeliads. Annals of Botany, 1999, 83(2), 183-192. http://dx.doi.org/10.1006/anbo.1998.0809.
http://dx.doi.org/10.1006/anbo.1998.0809... ), influencing the attributes of the insect larvae community and their predators in phytotelmata (Armbruster et al., 2002ARMBRUSTER, P., HUTCHINSON, R.A. and COTGREAVE, P. Factors influencing community structure in a South American tank bromeliad fauna. Oikos, 2002, 96(2), 225-234. http://dx.doi.org/10.1034/j.1600-0706.2002.960204.x.
http://dx.doi.org/10.1034/j.1600-0706.20... ). In addition, insect dispersal enhanced by pollination during flowering, which leads to an increase in oviposition rates (Reisenman et al., 2010REISENMAN, C.E., RIFFELL, J.A., BERNAYS, E.A. and HILDEBRAND, J.G. Antagonistic effects of floral scent in an insect–plant interaction. Proceedings of the Royal Society of London. Series B, Biological Sciences, 2010, 277(1692), 2371-2379. PMid:20335210.), counteracts the limited dispersal during vegetative growth, constituting another factor responsible for differences in species composition between phases. However, those factors do not seem to influence beta diversity patterns which, contrary to expected, were not different between the phenological phases.

Although phytotelmata may harbour many of the main aquatic insect orders, Diptera is considered the most common, with over 20 families present (Williams, 2006WILLIAMS, D.D. The biology of temporary waters. Oxford: Oxford University Press, 2006.). Indeed, we found that three Diptera morphospecies were discriminant in the vegetative growth phase. Several morphological and behavioural traits of this insect order suggest long term association with phytotelmata (Williams, 2006WILLIAMS, D.D. The biology of temporary waters. Oxford: Oxford University Press, 2006.). Diptera larvae are very abundant in bromeliads (Araújo et al., 2007ARAÚJO, V.A., MELO, S.K., ARAÚJO, A.P.A., GOMES, M.L.M. and CARNEIRO, M.A.A. Relationship between invertebrate fauna and bromeliad size. Brazilian Journal of Microbiology, 2007, 67(4), 611-617. PMid:18278311.), pitcher plants (Baiser et al., 2011BAISER, B., ARDESHIRI, R.S. and ELLISON, A.M. Species richness and trophic diversity increase decomposition in a co-evolved food Web. PLoS One, 2011, 6(5), e20672. PMid:21673992. http://dx.doi.org/10.1371/journal.pone.0020672.
http://dx.doi.org/10.1371/journal.pone.0... ) and tree-holes (Blakely et al., 2012BLAKELY, T.J., HARDING, J.S. and DIDHAM, R.K. Distinctive aquatic assemblages in water-filled tree holes: a novel component of freshwater biodiversity in New Zealand temperate rainforests. Insect Conservation and Diversity, 2012, 5(3), 202-212. http://dx.doi.org/10.1111/j.1752-4598.2011.00155.x.
http://dx.doi.org/10.1111/j.1752-4598.20... ), and are considered the main predators in the phytotelmata of several bromeliad species, where they exert a great influence on microorganisms (Walker et al., 2010WALKER, E.D., KAUFMAN, M.G. and MERRITT, R.W. An acute trophic cascade among microorganisms in the tree hole ecosystem following removal of omnivorous mosquito larvae. Community Ecology, 2010, 11(2), 171-178. PMid:25342946. http://dx.doi.org/10.1556/ComEc.11.2010.2.5.
http://dx.doi.org/10.1556/ComEc.11.2010.... ; Baiser et al., 2011BAISER, B., ARDESHIRI, R.S. and ELLISON, A.M. Species richness and trophic diversity increase decomposition in a co-evolved food Web. PLoS One, 2011, 6(5), e20672. PMid:21673992. http://dx.doi.org/10.1371/journal.pone.0020672.
http://dx.doi.org/10.1371/journal.pone.0... ). Although several studies show that zygoptera larvae are the main aquatic predators within phytotelmata (Petermann et al., 2015aPETERMANN, J.S., FARJALLA, V.F., JOCQUE, M., KRATINA, P., MACDONALD, A.A.M., MARINO, N.A., DE OMENA, P.M., PICCOLI, G.C., RICHARDSON, B.A., RICHARDSON, M.J., ROMERO, G.Q., VIDELA, M. and SRIVASTAVA, D.S. Dominant predators mediate the impact of habitat size on trophic structure in bromeliad invertebrate communities. Ecology, 2015a, 96(2), 428-439. PMid:26240864. http://dx.doi.org/10.1890/14-0304.1.
http://dx.doi.org/10.1890/14-0304.1... ; Romero et al., 2016ROMERO, G.Q., PICCOLI, G.C., DE OMENA, P.M. and GONÇALVES-SOUZA, T. Food web structure shaped by habitat size and climate across a latitudinal gradient. Ecology, 2016, 97(10), 2705-2715. PMid:27859108. http://dx.doi.org/10.1002/ecy.1496.
http://dx.doi.org/10.1002/ecy.1496... ), in the bromeliads used in our study no larval forms of these organisms were observed. Paradise (2000)PARADISE, C.J. Effects of pH and resources on a processing chain interaction in simulated treeholes. Journal of Animal Ecology, 2000, 69(4), 651-658. http://dx.doi.org/10.1046/j.1365-2656.2000.00423.x.
http://dx.doi.org/10.1046/j.1365-2656.20... suggest that alterations in pH due to the decomposition of organic matter by Scirtidae larvae (Coleoptera) within phytotelmata may lead to a reduction in the mortality and an increase in the abundance of Diptera larvae in this habitat. In fact, we found very high abundances of Scirtidae larvae in A. distichantha phytotelmata.

Insect larvae community structuring was influenced by different factors in the two phenological phases. During flowering, ciliate density (proxy of resource availability) and the morphometric parameters plant height and plant total volume were the most important local factors. Plant parameters are directly related to plant architecture and habitat complexity - the main predictor of arthropod distribution in vegetation (Gonçalves-Souza et al., 2011GONÇALVES-SOUZA, T., ALMEIDA-NETO, M. and ROMERO, G.Q. Bromeliad architectural complexity and vertical distribution predict spider abundance and richness. Austral Ecology, 2011, 36(4), 476-484. http://dx.doi.org/10.1111/j.1442-9993.2010.02177.x.
http://dx.doi.org/10.1111/j.1442-9993.20... ). According to Lawton (1983)LAWTON, J.H. Plant architecture and the diversity of phytophagous insects. Annual Review of Entomology, 1983, 28(1), 23-39. http://dx.doi.org/10.1146/annurev.en.28.010183.000323.
http://dx.doi.org/10.1146/annurev.en.28.... , seasonal changes may considerably affect plant architecture. In bromeliads, flowering events cause profound alterations in the three-dimensional leaf rosette structure, which opens to guarantee better access of pollinators to plant inflorescence (Romero & Vasconcellos-Neto, 2005aROMERO, G.Q. and VASCONCELLOS-NETO, J. The effects of plant structure on the spatial and microspatial distribution of a bromeliad-living jumping spider (Salticidae). Journal of Animal Ecology, 2005a, 74(1), 12-21. http://dx.doi.org/10.1111/j.1365-2656.2004.00893.x.
http://dx.doi.org/10.1111/j.1365-2656.20... , bROMERO, G.Q. and VASCONCELLOS-NETO, J. Spatial distribution and microhabitat preference of Psecas chapoda (Peckham & Peckham) (Araneae, Salticidae). The Journal of Arachnology, 2005b, 33(1), 124-134. http://dx.doi.org/10.1636/M03-9.
http://dx.doi.org/10.1636/M03-9... ). These modifications alter habitat conditions, such as water availability, resource capture (Zotz & Thomas, 1999ZOTZ, G. and THOMAS, V. How much water is in the tank? Model calculations for two epiphytic bromeliads. Annals of Botany, 1999, 83(2), 183-192. http://dx.doi.org/10.1006/anbo.1998.0809.
http://dx.doi.org/10.1006/anbo.1998.0809... ) and the presence of predators (Romero & Vasconcellos-Neto, 2005bROMERO, G.Q. and VASCONCELLOS-NETO, J. Spatial distribution and microhabitat preference of Psecas chapoda (Peckham & Peckham) (Araneae, Salticidae). The Journal of Arachnology, 2005b, 33(1), 124-134. http://dx.doi.org/10.1636/M03-9.
http://dx.doi.org/10.1636/M03-9... ).

By actively participating in nutrient cycling and bacterial population control in aquatic environments, ciliates are considered important components within food webs in those ecosystems (Sherr & Sherr, 2002SHERR, E.B. and SHERR, B.F. Significance of predation by protists in aquatic microbial food webs. Antonie van Leeuwenhoek Journal of Microbiology, 2002, 81(1-4), 293-308. PMid:12448728. http://dx.doi.org/10.1023/A:1020591307260.
http://dx.doi.org/10.1023/A:102059130726... ; Durán-Ramírez et al., 2015DURÁN-RAMÍREZ, C.A., GARCÍA-FRANCO, J.G., FOISSNER, W. and MAYÉN-ESTRADA, R. Free-living ciliates from epiphytic tank bromeliads in Mexico. European Journal of Protistology, 2015, 51(1), 15-33. PMid:25497463. http://dx.doi.org/10.1016/j.ejop.2014.09.002.
http://dx.doi.org/10.1016/j.ejop.2014.09... ). Carrias et al. (2001)CARRIAS, J.F., CUSSAC, M.E. and CORBARA, B. A preliminary study of freshwater protozoa in tank bromeliads. Journal of Tropical Ecology, 2001, 17(4), 611-617. http://dx.doi.org/10.1017/S0266467401001456.
http://dx.doi.org/10.1017/S0266467401001... point out that these organisms are key components to phytotelmata metabolism, since they are more efficient than metazoan in nutrient remineralization, that are released in the water column of this microhabitat and may be absorbed by the plants during development. This efficiency in organic matter degradation leads to an increase in the abundance of those microorganisms with the large amount of detritus input in phytotelmata (Kneitel & Miller, 2002KNEITEL, J.M. and MILLER, T.E. Resource and top predator regulation in the pitcher plant (Sarracenia purpurea) inquiline community. Ecology, 2002, 83(3), 680-688. http://dx.doi.org/10.1890/0012-9658(2002)083[0680:RATPRI]2.0.CO;2.
http://dx.doi.org/10.1890/0012-9658(2002... ; 2003KNEITEL, J.M. and MILLER, T.E. Dispersal rates affect species composition in metacommunities of Sarracenia purpurea inquilines. American Naturalist, 2003, 162(2), 165-171. PMid:12858261. http://dx.doi.org/10.1086/376585.
http://dx.doi.org/10.1086/376585... ), thus they are considered as a proxy of organic matter in this habitat (Carrias et al., 2001CARRIAS, J.F., CUSSAC, M.E. and CORBARA, B. A preliminary study of freshwater protozoa in tank bromeliads. Journal of Tropical Ecology, 2001, 17(4), 611-617. http://dx.doi.org/10.1017/S0266467401001456.
http://dx.doi.org/10.1017/S0266467401001... ; Petermann et al., 2015bPETERMANN, J.S., KRATINA, P., MARINO, N.A.C., MACDONALD, A.A.M. and SRIVASTAVA, D.S. Resources alter the structure and increase stochasticity in bromeliad microfauna communities. PLoS One, 2015b, 10(3), e0118952. PMid:25775464. http://dx.doi.org/10.1371/journal.pone.0118952.
http://dx.doi.org/10.1371/journal.pone.0... ). Furthermore, since they are in the intermediate level of food webs in those ecosystems, ciliates serve as a resource to insect larvae in phytotelmata (Kneitel & Miller, 2002KNEITEL, J.M. and MILLER, T.E. Resource and top predator regulation in the pitcher plant (Sarracenia purpurea) inquiline community. Ecology, 2002, 83(3), 680-688. http://dx.doi.org/10.1890/0012-9658(2002)083[0680:RATPRI]2.0.CO;2.
http://dx.doi.org/10.1890/0012-9658(2002... ).

Therefore, insect larvae community structuring during flowering may be explained by the alterations in plant structure in response to the flowering event itself, which changes the physical characteristics of the plants, besides enhancing the capture of organic matter by the bromeliad, increasing ciliate abundance. Thus, the combined effects of those factors lead to modifications in the community of insect larvae in this phenological phase.

In contrast to the flowering phase, aquatic insect larvae during the vegetative growth phase were structured by regional factors (spatial component). Spatial distribution of plants in the environment may affect the community attributes of associated arthropods (i. e. species richness: Gonçalves-Souza et al., 2011GONÇALVES-SOUZA, T., ALMEIDA-NETO, M. and ROMERO, G.Q. Bromeliad architectural complexity and vertical distribution predict spider abundance and richness. Austral Ecology, 2011, 36(4), 476-484. http://dx.doi.org/10.1111/j.1442-9993.2010.02177.x.
http://dx.doi.org/10.1111/j.1442-9993.20... ; and abundance: Hanski, 1982HANSKI, I. Dynamics of regional distribution: the core and satellite species hypothesis. Oikos, 1982, 38(2), 210-221. http://dx.doi.org/10.2307/3544021.
http://dx.doi.org/10.2307/3544021... ), since this distribution directly influences plant exposure to organisms, consequently enhancing colonization (Neuvonen & Niemelä, 1983NEUVONEN, S. and NIEMELÄ, P. Species richness and faunal similarity of arboreal insect herbivores. Oikos, 1983, 40(3), 452-459. http://dx.doi.org/10.2307/3544318.
http://dx.doi.org/10.2307/3544318... ) and dispersal of associated fauna.

According to Kneitel & Miller (2003)KNEITEL, J.M. and MILLER, T.E. Dispersal rates affect species composition in metacommunities of Sarracenia purpurea inquilines. American Naturalist, 2003, 162(2), 165-171. PMid:12858261. http://dx.doi.org/10.1086/376585.
http://dx.doi.org/10.1086/376585... , dispersal among local communities may have a variety of effects on species diversity and composition. For instance, an increase in dispersal rates - as we expected during flowering - may lead to an increase in the richness and abundance of the organisms, while decreasing variation among communities in a certain area (Kneitel & Miller, 2003KNEITEL, J.M. and MILLER, T.E. Dispersal rates affect species composition in metacommunities of Sarracenia purpurea inquilines. American Naturalist, 2003, 162(2), 165-171. PMid:12858261. http://dx.doi.org/10.1086/376585.
http://dx.doi.org/10.1086/376585... ). On the other hand, during vegetative growth, reduced dispersal may lead to an increase in the importance of the spatial component in community structuring.

Differences in dispersal rates between vegetative growth and flowering phases could be explained by the increase in resource availability for adult insects, due to bromeliad inflorescence. During the reproductive phase, plants produce floral stimuli (floral volatiles - Reisenman et al., 2010REISENMAN, C.E., RIFFELL, J.A., BERNAYS, E.A. and HILDEBRAND, J.G. Antagonistic effects of floral scent in an insect–plant interaction. Proceedings of the Royal Society of London. Series B, Biological Sciences, 2010, 277(1692), 2371-2379. PMid:20335210.) and offer rewards to pollinators (Nicholls & Altieri, 2013NICHOLLS, C.I. and ALTIERI, M.A. Plant biodiversity enhances bees and other insect pollinators in agroecosystems: a review. Agronomy for Sustainable Development, 2013, 33(2), 257-274. http://dx.doi.org/10.1007/s13593-012-0092-y.
http://dx.doi.org/10.1007/s13593-012-009... ), generally nectar or pollen (Labandeira, 2011LABANDEIRA, C.C. Pollination mutualisms by insects before the evolution of flowers. In J. TREFIL, ed. McGraw Hill Encyclopedia of Science & Technology. New York: McGraw-Hill Education, 2011, pp. 250-252.). Concerning the interactions between bromeliads and insects, other resources may be offered, such as resin and other material for nests, shelter, foraging, mating and oviposition sites (Kevan & Baker, 1983KEVAN, P.G. and BAKER, H.G. Insects as flower visitors and pollinators. Annual Review of Entomology, 1983, 28(1), 407-453. http://dx.doi.org/10.1146/annurev.en.28.010183.002203.
http://dx.doi.org/10.1146/annurev.en.28.... ; Labandeira, 2011LABANDEIRA, C.C. Pollination mutualisms by insects before the evolution of flowers. In J. TREFIL, ed. McGraw Hill Encyclopedia of Science & Technology. New York: McGraw-Hill Education, 2011, pp. 250-252.). Accordingly, this wide range of resources during flowering becomes a decisive factor for insect larvae fitness, in part due to the choice of oviposition sites by adult insects - active dispersers of this community (Basset & Novotny, 1999BASSET, Y. and NOVOTNY, V. Species richness of insect herbivore communities on Ficus in Papua New Guinea. Biological Journal of the Linnean Society, 1999, 67(4), 477-499. http://dx.doi.org/10.1111/j.1095-8312.1999.tb01943.x.
http://dx.doi.org/10.1111/j.1095-8312.19... ; Gonçalves-Souza et al., 2014GONÇALVES-SOUZA, T., ROMERO, G.Q. and COTTENIE, K. Metacommunity versus Biogeography: A Case Study of Two Groups of Neotropical Vegetation-Dwelling Arthropods. PLoS One, 2014, 9(12), e115137. PMid:25549332. http://dx.doi.org/10.1371/journal.pone.0115137.
http://dx.doi.org/10.1371/journal.pone.0... ). During vegetative growth, the absence of those rewards results in a decline of insect movement among plants and oviposition. Thus, we suggest that insect behaviour as a function of bromeliad flowering determines aquatic larvae community structuring in both phenological phases. However, since our samplings were performed in distinct seasons, further experimental studies are necessary to disentangle the effects of seasonal fluctuation and the phenological phase of plants on invertebrate fauna.

5. Conclusion

The hypothesis that community composition of aquatic insect larvae is different between the phenological phases was corroborated. Variation in this attribute could be attributed to differences in bromeliad architecture, insect dispersal and higher rates of oviposition among plants in the phenological phases, which is likely the result of rewards offered by the plants during the flowering phase. However, those factors may not seem to affect beta diversity patterns, which were not different between vegetative growth and flowering phases, contrary to expected in hypothesis II. Finally, our third hypothesis regarding the relative importance of local and regional factors in structuring the community of aquatic insect larvae was corroborated. During flowering, local factors were more important in community structuring, whereas during vegetative growth, regional factors predominated in explaining community variation.

Acknowledgements

The authors would like to thank the post-graduate course in Ecology of Continental Aquatic Habitats (PEA, Maringá State University) and NUPELIA for financial support, material, equipment and facilities during the samplings. This study was supported by the Brazilian Research Council (CNPq) and the Brazilian Federal Agency for the Support and Evaluation of Graduate Education (CAPES).

Cite as: Amadeo, F.E. et al. Effects of bromeliad flowering event on the community structuring of aquatic insect larvae associated with phytotelmata of Aechmea distichantha Lem. (Bromeliaceae). Acta Limnologica Brasiliensia, 2017, vol. 29, e111.

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Publication Dates

Publication in this collection
2017

History

Received
26 Mar 2017
Accepted
16 Oct 2017

This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

[1] Cite as: Amadeo, F.E. et al. Effects of bromeliad flowering event on the community structuring of aquatic insect larvae associated with phytotelmata of Aechmea distichantha Lem. (Bromeliaceae). Acta Limnologica Brasiliensia, 2017, vol. 29, e111.

Order	Morphospecies	Phenological Phase
Order	Morphospecies	Vegetative Growth	Flowering
Coleoptera
	Scirtidae	+	+
Diptera
	Diptera01	+	+
	Diptera02	+	+
	Diptera03	+	+
	Diptera04	+	+
	Diptera05	+	+
	Diptera06	+
	Diptera07	+
Lepidoptera
	Lepidoptera01	+	+
	Lepidoptera02	+	+
	Lepidoptera03	+	+
	Lepidoptera04	+
	Lepidoptera05		+
	Lepidoptera06		+
	Lepidoptera07		+
Neuroptera
	Neuroptera01		+

Phenological phases
	Vegetative Growth		Flowering
	R² Adj	P	R² Adj	P
[a] = X1\|X2	0.06197	0.031	0.00233	0.384
[b]	0.03792		-0.02366
[c] = X2\|X1	0.04186	0.066	0.19755	0.004
Residual	0.85824		0.82378

Phenological Phase	Environmental Variables	Spatial Variables
Vegetative Growth	bromeliad tank total volume, “web weaver” spiders	PCNM 6, 9
Flowering	plant height, plant total volume, ciliate density	PCNM 6, 9

Brasil

Brasil

Effects of bromeliad flowering event on the community structuring of aquatic insect larvae associated with phytotelmata of Aechmea distichantha Lem. (Bromeliaceae)

Efeito de um evento de floração na estruturação da comunidade de larvas de insetos aquáticos associados aos fitotelmata de Aechmea distichantha Lem. (Bromeliaceae)

Abstracts

Abstract

Methods

Results

Conclusion

Resumo

Métodos

Resultados

Conclusão

1. Introduction

2. Methods

2.1. Study area

2.2. Sampling

2.3. Study system

2.4. Data analysis

3. Results

4. Discussion

5. Conclusion

Acknowledgements

References

Publication Dates

History