Hostname: page-component-54dcc4c588-scsgl Total loading time: 0 Render date: 2025-10-08T02:17:33.230Z Has data issue: false hasContentIssue false
  • English
  • Français

Avian use of honeydew (Hemiptera: Coccoidea) in the Atlantic Forest of Southeastern Brazil

Published online by Cambridge University Press:  18 September 2025

Raissa Sequini Capelão Open the ORCID record for Raissa Sequini Capelão [Opens in a new window]  and
Augusto João Piratelli Open the ORCID record for Augusto João Piratelli [Opens in a new window]
Raissa Sequini Capelão
Affiliation:
Programa de Pós-Graduação em Ecologia e Recursos Naturais, Universidade Federal de São Carlos, São Carlos, SP, Brazil
Augusto João Piratelli*
Affiliation:
Departamento de Ciências Ambientais, CCTS, Universidade Federal de São Carlos, Sorocaba, São Paulo, Brazil
*
Corresponding author: Augusto João Piratelli; Email: piratelli@ufscar.br
Get access Rights & Permissions [Opens in a new window]

Abstract

Honeydew is a carbohydrate-rich exudate produced by scale insects (Hemiptera) that feed on phloem sap and excrete surplus sugars. Although its consumption by birds has been documented in a few tropical and temperate systems, its ecological relevance remains underexplored. Here, we describe the use of honeydew produced by Stigmacoccus paranaenses (Stigmacoccidae) on Inga trees (Fabaceae) by birds in the Atlantic Forest of southeastern Brazil. From March to October 2017, we conducted 359 hours of full-day observations and recorded 2599 visits from 25 bird species. Visitation was dominated by nectarivorous and frugivorous species, especially Coereba flaveola, Thalurania glaucopis, and Thraupis ornata, which together accounted for over 75% of visits. Generalised linear mixed models indicated strong seasonal variation in visitation rates, with peaks during the dry season (April–July) and a decline during wetter months. In contrast, no significant effects were found for time of day, honeydew sugar concentration, or air temperature. Species richness of visitors was also higher during the dry season. These findings suggest that honeydew may serve as a seasonal fallback resource for birds with high energetic demands, reinforcing its potential ecological role in fragmented tropical landscapes. From a restoration perspective, the presence of native plant species that host honeydew-producing insects, such as Inga, may enhance trophic complexity and support bird foraging during periods of resource scarcity, contributing to the ecological resilience of restored Atlantic Forest landscapes.

Keywords

feeding behaviourIngaresource partitioningscale insectstrophic interactions

Information

Type
Research Article
Information
Journal of Tropical Ecology , Volume 41 , 2025 , e27
Check for updates
Copyright
© The Author(s), 2025. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Antunes, AZ, Silva, BG, Matsukuma, CK, Eston, MR and Santos, AMR (2013) Aves do Parque Estadual Carlos Botelho. Biota Neotropica 13, 124–140. https://doi.org/10.1590/S1676-06032013000200012 CrossRefGoogle Scholar
Bach, CE (1991) Direct and indirect interactions between ants (Pheidole megacephala), scales (Coccus viridis), and plants (Pluchea indica). Oecologia 87, 233–239. https://doi.org/10.1007/BF00325261 CrossRefGoogle ScholarPubMed
Baker, HG (1975) Sugar concentrations in nectars from hummingbird flowers. Biotropica 7, 37–41. https://www.jstor.org/stable/2989798 10.2307/2989798CrossRefGoogle Scholar
Beggs, JR and Wardle, DA (2006) Keystone species: competition for honeydew among exotic and indigenous species. In: Allen, RB and Lee, WG (eds) Biological Invasions in New Zealand. Ecological Studies 186, 281–294. https://doi.org/10.1007/3-540-30023-6_18 CrossRefGoogle Scholar
Clayton, NS, Dickinson, A (1998) Episodic-like memory during cache recovery by scrub jays. Nature 395, 272–274. https://doi.org/10.1038/26216 CrossRefGoogle ScholarPubMed
Cortés, I, Igua-Muñoz, J and Morales, I (2024) Biology of Stigmacoccus asper (Hemiptera: Stigmacoccidae) in Colombian High-Andean Oak Forests. Entomology and Applied Science Letters 11, 1–8. https://doi.org/10.51847/M6zomiHue3 CrossRefGoogle Scholar
Dungan, RJ and Kelly, D (2003) Effect of host-tree and environmental variables on honeydew production by scale insects (Ultracoelostoma sp.) in a high elevation Nothofagus solandri forest. New Zealand Journal of Ecology 27, 169–177. https://newzealandecology.org/nzje/2196 Google Scholar
Farine, DR and Lang, SDJ (2013) The early bird gets the worm: foraging strategies of wild songbirds lead to the early discovery of food sources. Biology Letters 9, 20130578. https://doi.org/10.1098/rsbl.2013.0578 CrossRefGoogle Scholar
Feinsinger, P (1976) Organization of a tropical guild of nectarivorous birds. Ecological Monographs 46, 257–291. https://doi.org/10.2307/1942255 Google Scholar
Florestal, Fundação (2008) Inventário Florestal da Vegetação Natural do Estado de São Paulo. São Paulo: Secretaria do Meio Ambiente/Instituto Florestal/Imprensa Oficial. https://www.infraestruturameioambiente.sp.gov.br/institutoflorestal/2005/03/inventario-florestal-da-vegetacao-natural-do-estado-de-sao-paulo/ Google Scholar
Gamper, HA and Koptur, S (2010) Honeydew foraging by birds in tropical montane forests and pastures of Mexico. Journal of Tropical Ecology 26, 335–341. https://doi.org/10.1017/S0266467409990654 CrossRefGoogle Scholar
Gaze, PD and Clout, MN (1983) Honeydew and its importance to birds in beech forests of South Island New Zealand. New Zealand Journal of Ecology 6, 33–37. https://newzealandecology.org/nzje/1569 Google Scholar
Grant, WD and Beggs, JR (1989) Carbohydrate analysis of beech honeydew. New Zealand Journal of Zoology 16, 283–288. https://doi.org/10.1080/03014223.1989.10422893 CrossRefGoogle Scholar
Gullan, PJ (1997) Relationships with ants. In: Ben-Dov, Y and Hodgson, CJ (eds) Soft scale insects: their biology, natural enemies and control. Elsevier, pp. 351–374.Google Scholar
Hartig, F (2022) DHARMa: residual diagnostics for hierarchical (multi-level/mixed) regression models. R package version 0.4.6. https://CRAN.R-project.org/package=DHARMa Google Scholar
Herrera, C (1990) Daily patterns of pollinator activity differential pollinating effectiveness and floral resource availability in a summer-flowering Mediterranean shrub. Oikos 58, 277–288. https://doi.org/10.2307/3545218 CrossRefGoogle Scholar
INMET – Instituto Nacional de Meteorologia (2023) Banco de Dados Meteorológicos para Ensino e Pesquisa (BDMEP). Ministério da Agricultura e Pecuária Governo Federal do Brasil. https://bdmep.inmet.gov.br Google Scholar
Jiron, LF and Salas, S (1975) Simbioses entre cochinillas de cola Coccoidea (Margarodidae) y otros insectos. Brenesia 5, 67–71. https://agris.fao.org/search/en/providers/123819/records/64735e6f2c1d629bc97d7104 Google Scholar
Koster, F and Stoewesand, H (1973) Schildläuse als Honigtaulieferanten für Kolibris und Insekten. Bonner Zoologische Beiträge 24, 15–23. https://archive.org/details/bonner-zoologische-beitraege-24-0015-0023/page/22/mode/2up Google Scholar
Kronka, FJN, Nalon, MA and Matsukuma, CK (2005) Inventário florestal da vegetação natural do Estado de São Paulo. Secretaria do Meio Ambiente/Instituto Florestal/Imprensa Oficial São Paulo. https://www.infraestruturameioambiente.sp.gov.br/institutoflorestal/2005/03/inventario-florestal-da-vegetacao-natural-do-estado-de-sao-paulo/ Google Scholar
Lara, C, Martínez-García, V, Ortiz-Pulido, R, Bravo-Cadena, J and Córdoba-Aguilar, A (2011) Temporal-spatial segregation among hummingbirds foraging on honeydew in a temperate forest in Mexico. Current Zoology 57, 56–62. https://doi.org/10.1093/czoolo/57.1.56 CrossRefGoogle Scholar
Latta, SC, Gamper, HA and Tietz, JR (2001) Revising the convergence hypothesis of avian use of honeydew: evidence from Dominican subtropical dry forest. Oikos 93, 250–259. https://doi.org/10.1034/j.1600-0706.2001.930208.x CrossRefGoogle Scholar
Leighton, G.M, Drury, JP, Small, J. et al. (2024) Unfamiliarity generates costly aggression in interspecific avian dominance hierarchies. Nature Communications 15, 335. https://doi.org/10.1038/s41467-023-44613-0 CrossRefGoogle ScholarPubMed
Lima, RAF, Dittrich, VAO, Souza, VC, Salino, A, Breier, TB and Aguiar, OT (2011) Flora vascular do Parque Estadual Carlos Botelho São Paulo Brasil. Biota Neotropica 11, 173–214. https://doi.org/10.1590/S1676-06032011000400018 CrossRefGoogle Scholar
Mallon, JM, Tucker, MA, Beard, A, et al. (2020) Diurnal timing of nonmigratory movement by birds: the importance of foraging spatial scales. Journal of Avian Biology, e02612. https://doi.org/10.1111/jav.02612 CrossRefGoogle Scholar
Márquez-Luna, U, Lara, C, Corcuera, P, Valverde, PL (2019) Factors affecting the dominance hierarchy dynamics in a hummingbird assemblage. Current Zoology 65, 261–268. https://doi.org/10.1093/cz/zoy057 CrossRefGoogle Scholar
McNamara, JM, Houston, AI and Lima, SL (1994) Foraging routines of small birds in winter: a theoretical investigation. Journal of Avian Biology 25, 287–302. https://www.jstor.org/stable/3677276 10.2307/3677276CrossRefGoogle Scholar
McWhorter, TJ and López-Calleja, MV (2000) The integration of diet physiology and ecology of nectar-feeding birds. Revista Chilena de Historia Natural 73, 451–460. https://www.scielo.cl/pdf/rchnat/v73n3/art08.pdf 10.4067/S0716-078X2000000300008CrossRefGoogle Scholar
Moir, ML, Brennan, KEC, Koch, JM, Majer, JD and Fletcher, MJ (2005) Restoration of a forest ecosystem: The effects of vegetation and dispersal capabilities on the reassembly of plant-dwelling arthropods. Forest Ecology and Management 217, 294-306. https://doi.org/10.1016/j.foreco.2005.06.012.CrossRefGoogle Scholar
Morellato, LPC, Talora, DC, Takahasi, A, Bencke, CC, Romera, EC and Zipparro, VB (2000) Phenology of Atlantic rain forest trees: a comparative study. Biotropica 32, 811–823. https://www.jstor.org/stable/2663919 Google Scholar
Murphy, DJ and Kelly, D (2003) Seasonal variation in the honeydew invertebrate fruit and nectar resource for bellbirds in a New Zealand mountain beech forest. New Zealand Journal of Ecology 27, 123–137. https://newzealandecology.org/nzje/2174 Google Scholar
Nieto, A, Wüest, RO, Graham, CH, et al. (2023) Diel niche partitioning of a plant–hummingbird network in the Atlantic Forest of Brazil. Oecologia 201, 1025–1037. https://doi.org/10.1007/s00442-023-05347-4 CrossRefGoogle ScholarPubMed
Pacheco, JF, Silveira, LF, Aleixo, A, et al. (2021) Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee—second edition. Ornithology Research 29, 94–105. https://doi.org/10.1007/s43388-021-00058-x CrossRefGoogle Scholar
Paton, DC (1980) The importance of manna honeydew and lerp in the diets of honeyeaters. Emu 80, 213–226. https://doi.org/10.1080/01584197.1980.11799277 CrossRefGoogle Scholar
Pyke, GH (1978) Optimal foraging: movement patterns of bumblebees between inflorescences. Theoretical Population Biology 13, 72–98. https://doi.org/10.1016/0040-5809(78)90036-9 CrossRefGoogle ScholarPubMed
Pyke, GH and Waser, NM (1981) The production of dilute nectars by hummingbird and honeyeater flowers. Biotropica 13, 260–270. https://doi.org/10.2307/2387804 CrossRefGoogle Scholar
R Core Team (2024) R: A language and environment for statistical computing. R Foundation for Statistical Computing Vienna Austria. https://www.r-project.org Google Scholar
Reichholf, H and Reichholf, J (1973) “Honigtau” der Bracatinga-Schildlaus als Winternahrung von Kolibris (Trochilidae) in Süd-Brasilien. Bonner Zoologische Beiträge 24, 7–14. https://archive.org/details/bonner-zoologische-beitraege-24-0007-0014 Google Scholar
Schaefer, HM, Schmidt, V and Bairlein, F (2003) Discrimination abilities for nutrients: which difference matters for choosy birds and why? Animal Behaviour 65, 531–541. https://doi.org/10.1006/anbe.2003.2089 CrossRefGoogle Scholar
Sick, H (1988) Ornitologia brasileira: uma introdução. Brasília: Editora Universidade de Brasília.Google Scholar
Silva, BG and Piratelli, AJ (2014) Foraging behaviour of the Scale-throated Hermit Phaethornis eurynome in Vriesea incurvata (Bromeliaceae). Brazilian Journal of Biology 74, 448–450. https://doi.org/10.1590/1519-6984.15512 Google ScholarPubMed
Stiles, FG (1985) Seasonal patterns and coevolution in the hummingbird-flower community of a Costa Rican subtropical forest. Ornithological Monographs 36, 757–787. https://doi.org/10.2307/40168315 Google Scholar
Teixeira, FD and Azevedo, FCC (2013) Honeydew foraging by birds in an Atlantic Forest fragment of Minas Gerais State Brazil. Biota Neotropica 13, 391–394. https://doi.org/10.1590/S1676-06032013000400035 CrossRefGoogle Scholar
Tobias, JA, Sheard, C, Pigot, AL, et al. (2022) AVONET: morphological ecological and geographical data for all birds. Ecology Letters 25, 581–597. https://doi.org/10.1111/ele.13898 CrossRefGoogle ScholarPubMed
Way, MJ (1963) Mutualism between ants and honeydew-producing Homoptera. Annual Review of Entomology 8, 307–344. https://doi.org/10.1146/annurev.en.08.010163.001515 CrossRefGoogle Scholar
Wickham, H (2016) ggplot2: Elegant Graphics for Data Analysis. New York: Springer-Verlag. https://link.springer.com/book/10.1007/978-3-319-24277-4 Google Scholar
Wolda, H (1988) Insect seasonality: why? Annual Review of Ecology and Systematics 19, 1–18. https://doi.org/10.1146/annurev.es.19.110188.000245 CrossRefGoogle Scholar
Wolff, VRA, Witter, S and Lisboa, BB (2015) Reporte de Stigmacoccus paranaensis Foldi (Hemiptera: Stigmacoccidae) insecto escama asociado con la producción de miel de mielato en Rio Grande do Sul Brasil. Insecta Mundi 434, 1–7. https://digitalcommons.unl.edu/insectamundi/939 Google Scholar
Supplementary material: File

Capelão and Piratelli supplementary material

Capelão and Piratelli supplementary material
Download Capelão and Piratelli supplementary material(File)
File 551.2 KB