Skip to main content
Log in

The composition of the bacterial community in the foam produced by Mahanarva fimbriolata is distinct from those at gut and soil

  • Environmental Microbiology - Research Paper
  • Published:
Brazilian Journal of Microbiology Aims and scope Submit manuscript


The development of insects is strongly influenced by their resident microorganisms. Symbionts play key roles in insect nutrition, reproduction, and defense. Bacteria are important partners due to the wide diversity of their biochemical pathways that aid in the host development. We present evidence that the foam produced by nymphs of the spittlebug Mahanarva fimbriolata harbors a diversity of bacteria, including some that were previously reported as defensive symbionts of insects. Analysis of the microbiomes in the nymph gut and the soil close to the foam showed that the microorganisms in the foam were more closely related to those in the gut than in the soil, suggesting that the bacteria are actively introduced into the foam by the insect. Proteobacteria, Actinobacteria, and Acidobacteria were the predominant groups found in the foam. Since members of Actinobacteria have been found to protect different species of insects by producing secondary metabolites with antibiotic properties, we speculate that the froth produced by M. fimbriolata may aid in defending the nymphs against entomopathogenic microorganisms.

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


  1. Guilbeau BH (1908) The origin and formation of the froth in spittle-insects. Am Nat 42:783–798

    Article  Google Scholar 

  2. Kato K (1958) The origin and composition of the cuckoo spit. Rept Saitama Univ, B 3:33–53

    CAS  Google Scholar 

  3. Weaver C, King D (1954) Meadow spittlebug. Ohio Agric Exp Station Res Bull 741:1–99.,+Philaenus+leucophthalmus+(L.)&author=Weaver,+C.R.&author=King,+D.R.&publication_year=1954&journal=Ohio+Agric.+Exp.+Stat.+Bull.&volume=741&pages=1%E2%80%9399

  4. Marshall AT (1973) Protein synthesis and secretion by the Malpighian tubules of cercopoid larvae (Homoptera). J Insect Physiol 19:2317–2326

    Article  CAS  Google Scholar 

  5. Mello MLS, Pimentel ER, Yamada AT, Storopoli-Neto A (1987) Composition and structure of the froth of the spittlebug, Deois sp. Insect Biochem 17:493–502

    Article  CAS  Google Scholar 

  6. Tonelli M, Gomes G, Silva WD, Magri NTC, Vieira DM, Aguiar CL et al (2018) Spittlebugs produce foam as a thermoregulatory adaptation. Sci Rep 8:4729.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Whittaker JB (1970) Cercopid spittle as a microhabitat. Oikos. 21:59–64.

    Article  Google Scholar 

  8. del Campo ML, King JT, Gronquist MR (2011) Defensive and chemical characterization of the froth produced by the cercopid Aphrophora cribrata. Chemoecology. 21:1–8.

    Article  CAS  Google Scholar 

  9. Leite LG, Machado LA, Goulart RM, Tavares FM, Batista FA (2005) Screening of entomopathogenic nematodes (Nemata: Rhabditida) and the efficiency of Heterorhabditis sp. against the sugarcane root spittlebug Mahanarva fimbriolata (Fabr.) (Hemiptera: Cercopidae). Neotrop Entomol 34:785–790.

    Article  Google Scholar 

  10. Dinardo-Miranda LL, Vasconcelos ACM, Vieira SR, Fracasso JV, Grego CR (2007) Uso da geoestatística na avaliação da distribuição espacial de Mahanarva fimbriolata em cana-de-açúcar. Bragantia. 66:449–455

    Article  Google Scholar 

  11. Rezende JM, Zanardo ABR, da Silva LM, Delalibera I, Rehner SA (2015) Phylogenetic diversity of Brazilian Metarhizium associated with sugarcane agriculture. BioControl. 60:495–505.

    Article  Google Scholar 

  12. Ferrari J, Darby AC, Daniell TJ, Godfray HCJ, Douglas AE (2004) Linking the bacterial community in pea aphids with host-plant use and natural enemy resistance. Ecol Entomol 29:60–65.

    Article  Google Scholar 

  13. Oh D-C, Poulsen M, Currie CR, Clardy J (2009) Dentigerumycin: a bacterial mediator of an ant-fungus symbiosis. Nat Chem Biol 5:391–393.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Douglas AE (2015) Multiorganismal insects: diversity and function of resident microorganisms. Annu Rev Entomol 60:17–34.

    Article  CAS  PubMed  Google Scholar 

  15. Flórez LV, Biedermann PHW, Engl T, Kaltenpoth M (2015) Defensive symbioses of animals with prokaryotic and eukaryotic microorganisms. Nat Prod Rep 32:904–936.

    Article  CAS  PubMed  Google Scholar 

  16. Kaltenpoth M, Göttler W, Herzner G, Strohm E (2005) Symbiotic bacteria protect wasp larvae from fungal infestation. Curr Biol 15:475–479.

    Article  CAS  PubMed  Google Scholar 

  17. Kaltenpoth M (2009) Actinobacteria as mutualists: general healthcare for insects? Trends Microbiol 17:529–535.

    Article  CAS  PubMed  Google Scholar 

  18. Scarborough CL, Ferrari J, Godfray HCJ. Aphid protected from pathogen by endosymbiont. Science (80- ). 2005;310:1781

  19. Mahadav A, Gerling D, Gottlieb Y, Czosnek H, Ghanim M (2008) Parasitization by the wasp Eretmocerus mundus induces transcription of genes related to immune response and symbiotic bacteria proliferation in the whitefly Bemisia tabaci. BMC Genomics 9:342.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Dillon RJ, Dillon VM (2004) The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 49:71–92.

    Article  CAS  PubMed  Google Scholar 

  21. Krishnan M, Bharathiraja C, Pandiarajan J, Prasanna VA, Rajendhran J, Gunasekaran P (2014) Insect gut microbiome - an unexploited reserve for biotechnological application. Asian Pac J Trop Biomed 4(Suppl 1):S16–S21.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Lewis Z, Lizé A (2015) Insect behaviour and the microbiome. Curr Opin Insect Sci 9:86–90.

    Article  PubMed  Google Scholar 

  23. Douglas AE (2011) Lessons from studying insect symbioses. Cell Host Microbe 10:359–367.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Zucchi TD, Prado SS, Cônsoli FL (2012) The gastric caeca of pentatomids as a house for actinomycetes. BMC Microbiol 12:101.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Salem H, Kreutzer E, Sudakaran S, Kaltenpoth M (2013) Actinobacteria as essential symbionts in firebugs and cotton stainers (Hemiptera, Pyrrhocoridae). Environ Microbiol 15:1956–1968.

    Article  PubMed  Google Scholar 

  26. Moran NA, Tran P, Gerardo NM (2005) Symbiosis and insect diversification: an ancient symbiont of sap-feeding insects from the bacterial phylum Bacteroidetes. Appl Environ Microbiol 71:8802–8810.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Koga R, Bennett GM, Cryan JR, Moran NA (2013) Evolutionary replacement of obligate symbionts in an ancient and diverse insect lineage. Environ Microbiol 15:2073–2081.

    Article  PubMed  Google Scholar 

  28. Koga R, Moran NA (2014) Swapping symbionts in spittlebugs: evolutionary replacement of a reduced genome symbiont. ISME J 8:1237–1246.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Scopel W, Cônsoli FL. Culturable symbionts associated with the reproductive and digestive tissues of the neotropical brown stinkbug Euschistus heros. Antonie Van Leeuwenhoek. 2018;:1–12.

  30. Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M et al (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41:e1–e1.

    Article  CAS  PubMed  Google Scholar 

  32. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Pylro VS, Roesch LFW, Morais DK, Clark IM, Hirsch PR, Tótola MR (2014) Data analysis for 16S microbial profiling from different benchtop sequencing platforms. J Microbiol Methods 107:30–37.

    Article  CAS  PubMed  Google Scholar 

  34. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 26:2460–2461.

    Article  CAS  PubMed  Google Scholar 

  35. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K et al (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. R Core Team. R: Language And Environment For Statistical Computing R Foundation for Statistical Computing. 2017

  37. Ferreira EB, Cavalcanti PP, Nogueira DA (2014) ExpDes: an R package for ANOVA and experimental designs. Appl Math 05:2952–2958.

    Article  Google Scholar 

  38. McMurdie PJ, Holmes S (2014) Waste not, want not: why rarefying microbiome data is inadmissible. PLoS Comput Biol 10:e1003531.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Dhariwal A, Chong J, Habib S, King IL, Agellon LB, Xia J (2017) MicrobiomeAnalyst: a web-based tool for comprehensive statistical, visual and meta-analysis of microbiome data. Nucleic Acids Res 45:W180–W188.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Kroiss J, Kaltenpoth M, Schneider B, Schwinger M-G, Hertweck C, Maddula RK et al (2010) Symbiotic streptomycetes provide antibiotic combination prophylaxis for wasp offspring. Nat Chem Biol 6:261–263.

    Article  CAS  PubMed  Google Scholar 

  41. Marshall AT (1965) Batelli glands of cercopoid nymphs (Homoptera). Nature. 205:925

    Article  Google Scholar 

  42. Cecil R (1930) The alimentary canal of Philaenus leucophthalmus L. Ohio J Sci 30:120–130

    Google Scholar 

  43. Wilson HA, Dorsey CK (1957) Studies on the composition and microbiology of insect spittle. Ann Entomol Soc Am 50:399–406.

    Article  CAS  Google Scholar 

  44. Ben BC, Cordon-Rosales C, Durvasula RV (2002) Bacterial symbionts of the triatominae and their potential use in control of Chagas disease transmission. Annu Rev Entomol 47:123–141.

    Article  Google Scholar 

  45. Hosokawa T, Kikuchi Y, Nikoh N, Shimada M, Fukatsu T (2006) Strict host-symbiont cospeciation and reductive genome evolution in insect gut bacteria. PLoS Biol 4:e337.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Prado SS, Rubinoff D, Almeida RPP (2006) Vertical transmission of a pentatomid caeca-associated symbiont. Ann Entomol Soc Am 99:577–585.[577:vtoapc];2

    Article  Google Scholar 

  47. Park D-S, Oh H-W, Jeong W-J, Kim H, Park H-Y, Bae KS (2007) A culture-based study of the bacterial communities within the guts of nine longicorn beetle species and their exo-enzyme producing properties for degrading xylan and pectin. J Microbiol 45:394–401

    CAS  PubMed  Google Scholar 

  48. Lefebvre T, Miambi E, Pando A, Diouf M, Rouland-Lefèvre C (2009) Gut-specific actinobacterial community structure and diversity associated with the wood-feeding termite species, Nasutitermes corniger (Motschulsky) described by nested PCR-DGGE analysis. Insect Soc 56:269–276.

    Article  Google Scholar 

  49. Hedges LM, Brownlie JC, O’Neill SL, Johnson KN (2008) Wolbachia and virus protection in insects. Science. 322:702.

    Article  CAS  PubMed  Google Scholar 

Download references


This work was supported in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brazil (CAPES), Finance Code 001, and the National Institute of Science and Technology – Semiochemicals in Agriculture (Fundação de Amparo à Pesquisa do Estado de São Paulo and Conselho Nacional de Desenvolvimento Científico e Tecnológico [grants #2014/50871-0 and #465511/2014-7, respectively]).

Author information

Authors and Affiliations


Corresponding author

Correspondence to José Maurício S. Bento.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Additional information

Responsible Editor: Lucy Seldin.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material


(DOCX 19 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tonelli, M., Cotta, S.R., Rigotto, A. et al. The composition of the bacterial community in the foam produced by Mahanarva fimbriolata is distinct from those at gut and soil. Braz J Microbiol 51, 1151–1157 (2020).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: