Skip to main content

Advertisement

Log in

Seasonal and diel variations in the activity of canopy insect herbivores differ between deciduous and evergreen plant species in a tropical dry forest

  • ORIGINAL PAPER
  • Published:
Journal of Insect Conservation Aims and scope Submit manuscript

Abstract

This study evaluated whether herbivorous insects can be expected to have particular adaptations to withstand the harsh dry season in tropical dry forests (TDFs). We specifically investigated a possible escape in space, with herbivorous insects moving to the few evergreen trees that occur in this ecosystem; and escape in time, with herbivores presenting an increased nocturnal rather than diurnal activity during the dry season. We determined the variation in the free-feeding herbivorous insects (sap-sucking and leaf chewing) between seasons (beginning and middle of both rainy and dry seasons), plant phenological groups (deciduous and evergreen trees) and diel period (diurnal and nocturnal) in a Brazilian TDF. We sampled a total of 5827 insect herbivores in 72 flight-interception traps. Contrary to our expectations, we found a greater herbivore diversity during the dry season, with low species overlap among seasons. In the dry season, evergreen trees supported greater richness and abundance of herbivores as compared to deciduous trees. Insects were also more active at night during the dry season, but no diel differences in insect abundance were detected during the rainy season. These results indicate that the strategies used by insect herbivores to withstand the severe climatic conditions of TDFs during the dry season include both small-scale escape in space and time, with evergreen trees playing a key role in maintaining resident insect herbivore populations in TDFs. Relatively more nocturnal activity during the dry season may be related to the avoidance of harsh climatic conditions during the day. We suggest that the few evergreen tree species occurring in the TDF landscape should be especially targeted for protection in this threatened ecosystem, given their importance for insect conservation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Antunes FZ (1994) Caracterização Climática—Caatinga do Estado de Minas Gerais. Info Agro 17:15–19

    Google Scholar 

  • Basset Y, Springate ND (1992) Diel activity of arboreal artbropods associated with a rainforest tree. J Nat Hist 26:947–952

    Article  Google Scholar 

  • Basset Y, Aberlenc HR, Barrios H, Curletti G, Bérenger JM, Vesco JP, Causse P, Haug A, Hennion AS, Lesobre L, Marquès F, O’meara R (2001) Stratification and diel activity of arthropods in a lowland rainforest in Gabon. Biol J Linn Soc 72:585–607

    Article  Google Scholar 

  • Basset Y, Novotny V, Barrios H, Holloway JD, Miller E (2003) Vertical stratification of arthropod assemblages. In: Basset Y, Novotny V, Miller SE, Kitching RL (eds) Arthropods of tropical forests: spatio-temporal dynamics and resource use in the canopy. Cambridge University Press, Cambridge, pp 17–27

    Google Scholar 

  • Basset Y, Cizek L, Cuénoud P, Didham RK, Guilhaumon F, Missa O, Novotny V, Ødegaard F, Roslin T, Schmidl J, Tishechkin AK, Winchester NN, Roubik DW, Aberlenc HP, Bail J, Barrios H, Bridle JR, Castaño-Meneses G, Corbara B, Curletti G, Rocha WD, Bakker D, Delabie JHC, Dejean A, Fagan LL, Floren A, Kitching RL, Medianero E, Miller SE, Oliveira EG, Orivel J, Pollet M, Rapp M, Ribeiro SP, Roisin Y, Schmidt JB, Sørensen L, Leponce M (2012) Arthropod diversity in a Tropical Forest. Science 338:1481–1484

    Article  CAS  PubMed  Google Scholar 

  • Clarke KR (1993) Nonparametric analyses of changes in community structure. Aust J Ecol 18:117–143

    Article  Google Scholar 

  • Crawley MJ (2007) Statistical computing—an introduction to data analysis using S-Plus. Wiley, London

    Google Scholar 

  • Didham RK, Springate ND (2003) Determinants of temporal variation in community structure. In: Basset Y, Novotny V, Miller SE, Kitching RL (eds) Arthropods of tropical forests: spatio-temporal dynamics and resource use in the canopy. Cambridge University Press, Cambridge, pp 28–39

    Google Scholar 

  • Dirzo R, Domínguez CA (1995) Plant-herbivore interactions in Mesoamerican tropical dry forest. In: Bullock SH, Mooney A, Medina E (eds) Seasonally dry tropical forests. Cambridge University Press, Cambridge, pp 304–325

    Chapter  Google Scholar 

  • Freire-Jr G, Nascimento AR, Konstantinov IM, Diniz IR (2014) Temporal occurrence of two Morpho butterflies (Lepidoptera: Nymphalidae): influence of weather and food resources. Environ Entomol 43:274–282

    Article  Google Scholar 

  • Gonda-King L, Gómez S, Martin JL, Orians CM, Preisser EL (2014) Tree responses to an invasive sap-feeding insect. Plant Ecol 215:297–304

    Article  Google Scholar 

  • Grimbacher PS, Stork NE (2009) Seasonality of a diverse beetle assemblage inhabiting lowland tropical rain forest in Australia. Biotropica 41:328–337

    Article  Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) Past: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9

    Google Scholar 

  • Hasselquist NJ, Allen MF, Santiago LS (2010) Water relations of evergreen and drought-deciduous trees along a seasonally dry tropical forest chronosequence. Oecologia 164:881–890

    Article  PubMed  PubMed Central  Google Scholar 

  • Janzen DH (1973) Sweep samples of tropical foliage insects: effects of seasons, vegetation types, elevation, time of day, and insularity. Ecology 54:687–708

    Article  Google Scholar 

  • Janzen DH (1981) Patterns of herbivory in a tropical deciduous forest. Biotropica 13:271–282

    Article  Google Scholar 

  • Janzen DH (1983) Food webs: who eats what, why, how, and with what effects in a tropical forest. In: Golley FB (ed) Tropical rain forest ecosystems: structure and function. Elsevier, Amsterdam, pp 162–182

    Google Scholar 

  • Kishimoto-Yamada K, Itioka K (2015) How much have we learned about seasonality in tropical insect abundance since Wolda (1988)? Entomol Sci 18:407–419

    Article  Google Scholar 

  • Leal CRO, Fagundes M, Neves FS (2015) Change in herbivore insect communities from adjacent habitats in a transitional region. Arthropod-Plant Interact 9:311–320

    Article  Google Scholar 

  • Leal CRO, Silva JO, Sousa-Souto L, Neves FS (2016) Vegetation structure determines insect herbivore diversity in seasonally dry tropical forests. J Insect Conserv 20:979–988

    Article  Google Scholar 

  • Lebrija-Trejos E, Pérez García EA, Meave JA, Poorter L, Bongers F (2011) Environmental changes during secondary succession in a tropical dry forest in Mexico. J Trop Ecol 27:1–13

    Article  Google Scholar 

  • Losey JE, Vaughan M (2006) The economic value of ecological services provided by insects. Bioscience 56:311–323

    Article  Google Scholar 

  • Lott EJ, Atkinson TH (2002) Biodiversidad y fitogeografica de Chamela-Cuixmala Jalisco. In: Noguera F, Rivera JHV, Aldrete ANG, Quesada M (eds) Historia natural de Chamela. Instituto de Biologia UNAM, Mexico City, pp 83–97

    Google Scholar 

  • Madeira JÁ, Fernandes GW (1999) Reproductive phenology of sympatric taxa of Chamaecrista (Leguminosae) in Serra do Cipó, Brazil. J Trop Ecol 15:463–479

    Article  Google Scholar 

  • Madeira BG, Espírito-Santo MM, D’Angelo-Neto S, Nunes YRF, Sánchez-Azofeifa GA, Fernandes GW, Quesada M (2009) Changes in tree and liana communities along a successional gradient in a tropical dry forest in south-eastern Brazil. Plant Ecol 291:291–304

    Article  Google Scholar 

  • Miles L, Newton AC, Defries RS, Ravilious C, May I, Blyth S, Kapos V, Gordon JE (2006) A global overview of the conservation status of tropical dry forests. J Biogeogr 33:491–505

    Article  Google Scholar 

  • Moran CV, Southwood TRE (1982) The guild composition of arthropod communities in trees. J Anim Ecol 51:289–306

    Article  Google Scholar 

  • Murphy PG, Lugo AE (1986) Ecology of tropical dry forest. Annu Rev Ecol Syst 17:67–88

    Article  Google Scholar 

  • Neves FS, Silva JO, Espírito-Santo MM, Fernades GW (2014) Insect herbivores and leaf damage along successional and vertical gradients in a tropical dry forest. Biotropica 46:14–24

    Article  Google Scholar 

  • Nichols E, Spector S, Louzada J, Larsen T, Amezquita S, Favila ME, Network TSR (2008) Ecological functions and ecosystem services provided by Scarabaeinae dung beetles. Biol Conserv 141:1461–1474

    Article  Google Scholar 

  • Novais SMA, Reis LEM, Rocha WD, Neves FS (2016) Effects of habitat management on different feeding guilds of herbivorous insects in cacao agroforestry systems. Rev Biol Trop 64:763–777

    Article  Google Scholar 

  • Novotny V, Basset Y (1998) Seasonality of sap-sucking insects (Auchenorrhyncha: Hemiptera) feeding on Ficus (Moraceae) in a lowland rain forest in New Guinea. Oecologia 115:514–522

    Article  PubMed  Google Scholar 

  • Novotny V, Basset Y (2005) Host specificity of insect herbivores in tropical forests. Proc R Soc Lond 272:1083–1090

    Article  Google Scholar 

  • Novotny V, Wilson MR (1997) Why are there no small species among xylem-sucking insects? Evol Ecol 11:419–437

    Article  Google Scholar 

  • Novotny V, Basset Y, Auga J, Boen W, Dal C, Drozd P, Kasbal M, Isua B, Kutil R, Manumbor M, Molem K (1999) Predation risk for herbivorous insects on tropical vegetation: a search for enemy-free space and time. Aust J Ecol 24:477–483

    Article  Google Scholar 

  • Novotny V, Basset Y, Kitching R (2003) Herbivore assemblages and their food resources. In: Basset Y, Novotny V, Miller S, Kitching R (eds) Arthropods of tropical forests: spatio-temporal dynamics and resource use in the canopy. Cambridge University Press, Cambridge, pp 40–53

    Google Scholar 

  • Pezzini FF (2008) Fenologia de comunidades arbóreas de mata seca em três estágios sucessionais. Master Dissertation. Universidade Federal de Minas Gerais, Belo Horizonte

  • Pezzini FF, Ranieri BD, Brandão D, Fernandes GW, Quesada M, Espírito-Santo MM, Jacobi CM (2014) Changes in tree phenology along natural regeneration in a seasonally dry tropical forest. Plant Biosyst 148:956–974

    Article  Google Scholar 

  • Pinheiro F, Diniz IR, Coelho D, Bandeira MSP (2002) Seasonal pattern of insect abundance in the Brazilian cerrado. Austral Ecol 27:132–136

    Article  Google Scholar 

  • Portillo-Quintero CA, Sánchez-Azofeifa GA (2010) Extent and conservation of tropical dry forests in the Americas. Biol Conserv 143:144–155

    Article  Google Scholar 

  • Price PW (2002) Resource-driven terrestrial interaction webs. Ecol Res 17:241–247

    Article  Google Scholar 

  • Quesada M, Sanchez-Azofeifa GA, Alvarez-Añorve M, Stoner KE, Avila-Cabadilla L, Calvo-Alvarado J, Castillo A, Espírito-Santo MM, Fagundes M, Fernandes GW, Gamon J, Lopezaraiza-Mikel M, Lawrence D, Morellato LPC, Powers JS, Neves F de S, Rosas-Guerrero V, Sayago R, Sanchez-Montoya G (2009) Succession and management of tropical dry forests in the Americas: review and new perspectives. For Ecol Manag 258:1014–1024

    Article  Google Scholar 

  • R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0. http://www.R-project.org

  • Rafael JA, Melo GAR, Carvalho CJB, Casari AS, Constantino R (2012) Os Insetos do Brasil: diversidade e taxonomia. Holos Editora, Ribeirão Preto

  • Ragusa-Netto JA, Silva RR (2007) Canopy phenology of a dry forest in western Brazil. Braz J Biol 67:569–575

    Article  CAS  PubMed  Google Scholar 

  • Rakitov RA (2000) Secretion of brochosomes during the ontogenesis of a leafhopper, Oncometopia orbona (F.) (Insecta:Homoptera:Cicadellidae). Tissue Cell 32:28–39

    Article  CAS  PubMed  Google Scholar 

  • Rakitov RA (2002) What are brochosomes for? An enigma of leafhoppers (Hemiptera, Cicadellidae). Denisia (Linz) 4:411–432

    Google Scholar 

  • Sanchez-Azofeifa GA, Quesada M, Rodríguez JP, Nassar JM, Stoner KE, Castillo A, Garvin T, Zent EL, Calvo-Alvarado JC, Kalacska MER, Fajardo L, Gamon JA, Cuevas-Reyes P (2005) Research priorities for Neotropical dry forests. Biotropica 37:477–485

    Google Scholar 

  • Santos MG, Oliveira MT, Figueiredo KV, Falcão HM, Arruda EP, Almeida-Cortez JS, Sampaio EVSB, Ometto JPHB, Menezes RSC, Oliveira AFM, Pompelli MF, Antonino ACD (2014) Caatinga, the Brazilian dry tropical forest: can it tolerate climate changes? Theor Exp Plant Physiol 26:83–99

    Article  Google Scholar 

  • Silva JO, Neves FS (2014) Insect herbivores associated with an evergreen tree Goniorrhachis marginata Taub. (Leguminosae: Caesalpinioideae) in a tropical dry forest. Braz J Biol 74:623–631

    Article  CAS  PubMed  Google Scholar 

  • Silva JO, Espírito-Santo MM, Melo GA (2012) Herbivory on Handroanthus ochraceus (Bignoniaceae) along a successional gradient in a tropical dry forest. Arthropod-Plant Interact 6:45–57

    Article  Google Scholar 

  • Silva JO, Espírito-Santo MM, Morais HC (2015) Leaf traits and herbivory on deciduous and evergreen trees in a tropical dry forest. Basic Appl Ecol 16:210–219

    Article  Google Scholar 

  • Silva JO, Espírito-Santo MM, Fernandes GW (2016) Galling insect species richness and leaf herbivory in an abrupt transition between Cerrado and Tropical Dry Forest. Ann Entomol Soc Am 109:705–712

    Article  Google Scholar 

  • Springate ND, Basset Y (1996) Diel activity of arboreal arthropods associated with Papua New Guinean trees. J Nat Hist 30:101–112

    Article  Google Scholar 

  • Vasconcellos A, Andreazze R, Almeida AM, Araujo HFP, Oliveira ES, Oliveira U (2010) Seasonality of insects in the semi-arid Caatinga of northeastern Brazil. Rev Bras Entomol 54: 471–476

    Article  Google Scholar 

  • Villalobos SC, González-Carcacía JA, Rodríguez JP, Nassar J (2013) Interspecific and interannual variation in foliar phenological patterns in a successional mosaic of a dry forest in the central llanos of Venezuela. In: Sánchez-Azofeifa GA, Powers JS, Fernandes GW, Quesada M (eds) Tropical dry forests in the Americas. CRC Press, Boca Raton, pp 301–324

    Chapter  Google Scholar 

  • Walter J, Hein H, Auge H, Beierkuhnlein C, Löffler S, Reifenrath K, Schädler M, Weber M, Jentsch A (2012) How do extreme drought and plant community composition affect host plant metabolites and herbivore performance? Arthropod-Plant Interact 6:15–25

    Article  Google Scholar 

  • Wardhaugh CW (2014) The spatial and temporal distributions of arthropods in forest canopies: uniting disparate patterns with hypotheses for specialization. Biol Rev 89:1021–1041

    Article  PubMed  Google Scholar 

  • Warton DI, Wright ST, Wang Y (2012) Distance-based multivariate analyses confound location and dispersion effects. Methods Ecol Evol 3:89–101

    Article  Google Scholar 

Download references

Acknowledgements

We are very grateful to A Scariot, J Hay and M Almeida-Neto for their valuable suggestions on early versions of the manuscript, and to TG Silva, JC Santos, A Mendes and SFM Silva for field assistance. We also thank the logistical support provided by the Instituto Estadual de Florestas (IEF), and the financial by Fundação de Amparo à Pesquisa de Minas Gerais-FAPEMIG, Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq 563304/2010-3), the Inter-American Institute for Global Change Research (IAI-CRN II-021), and Decanato de Pesquisa e Pós-Graduação of the Universidade de Brasília (UnB). We gratefully acknowledge a scholarship of the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) to Jhonathan O. Silva and Mário M. Espírito-Santo.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jhonathan O. Silva.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 16671 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Silva, J.O., Leal, C.R.O., Espírito-Santo, M.M. et al. Seasonal and diel variations in the activity of canopy insect herbivores differ between deciduous and evergreen plant species in a tropical dry forest. J Insect Conserv 21, 667–676 (2017). https://doi.org/10.1007/s10841-017-0009-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10841-017-0009-9

Keywords

Navigation