Skip to main content
Log in

Semi-arid’s Unsung Heroes: Hymenoptera and the Vital Ecosystem Services Enabled by Encholirium spectabile, a Rupicolous Bromeliad in the Brazilian Semi-arid Region

  • Ecology, Behavior and Bionomics
  • Published:
Neotropical Entomology Aims and scope Submit manuscript

Abstract

The concept of Ecosystem Services (ES) recognizes the importance of natural ecosystems in supporting human well-being. Hymenoptera, a diverse group of insects including ants, bees, and wasps, play crucial roles in providing ESs. Despite their significance, the provision of ESs by Hymenoptera is often undervalued, leading to ecosystem degradation and loss of important services. This study focuses on the association between Hymenoptera and a rupicolous bromeliad species (Encholirium spectabile) and explores the ESs promoted directly and indirectly by these insects. The study area is located in the Caatinga region of Brazil, characterized by irregular rainfall and a dry season. The results show that Hymenoptera, particularly bees, ants, and wasps, provide a range of ESs including pollination, honey production, pest control, cultural symbolism, and educational value. These services are vital for plant reproduction, food production, and ecosystem functioning in both seasons; there are no differences in species richness between seasons, but rather in species composition. Understanding the importance of Hymenoptera for ESs is crucial for informing conservation and management practices to ensure the sustainability of natural ecosystems. The study highlights the need for conservation actions to protect the intricate ecological relationships between Hymenoptera and bromeliads, which indirectly support ESs by providing habitat and resources, especially during droughts when resources are scarce in the region. By recognizing the importance of bromeliads in supporting Hymenopteran communities, conservation efforts can focus on preserving these critical ecological interactions and maintaining ES provision.

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
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data Availability

Data availability can be accessed by requesting the corresponding author.

References

  • Ab’Saber AN (1974) O domínio morfoclimático semi-árido das caatingas brasileiras. Geomorfologia (43):1–39

  • Acuña AM, Caso L, Aliphat MM, Vergara CH (2011) Edible insects as part of the traditional food system of the Popoloca town of Los Reyes Metzontla, Mexico. J Ethnobiol 31:150–169

    Article  Google Scholar 

  • Adana de la Torre JA, Calvache HH, Arias DA (2000) Programa comercial de manejo de Leptopharsa gibbicarina Froeschner (Hemíptera: Tingidae) con la hormiga Crematogaster spp. en una plantación de palma de aceite. Revista Palmas 21:167–173

    Google Scholar 

  • Ajibola A, Chamunorwa JP, Erlwanger KH (2012) Nutraceutical values of natural honey and its contribution to human health and wealth. Nutr Metab (lond) 9:61. https://doi.org/10.1186/1743-7075-9-61

    Article  PubMed  Google Scholar 

  • Akre RD, Myhre EA (1994) The nesting biology and behavior of the California yellowjacket, Vespula sulfurea (Hymenoptera, Vespidae). Entomol News 105:141–148

    Google Scholar 

  • Andersen AN (1997) Using ants as bioindicators: multiscale issues in ant community ecology. Conserv Ecol 1:17

    Google Scholar 

  • Andersen AN, Majer JD (2004) Ants show the way down under: invertebrates as bioindicators in land management. Front Ecol Environ 2:291–298

    Article  Google Scholar 

  • Aryal S, Ghosh S, Jung C (2020) Ecosystem services of honey bees: Regulating, provisioning and cultural functions. J Apiculture [SL] 35(2):119–128. https://doi.org/10.17519/apiculture.2020.06.35.2.119. (The Apicultural Society of Korea)

    Article  Google Scholar 

  • Baccaro FB (2006) Chave para as principais subfamílias e gêneros de formigas (Hymenoptera: Formicidae). Instituto Nacional de Pesquisas da Amazônia, Amazônia

    Google Scholar 

  • Barbiéri C, Francoy TM (2020) Theoretical model for interdisciplinary analysis of human activities: meliponiculture as an activity that promotes sustainability. Ambiente Soc, [SL] 23:1–20. https://doi.org/10.1590/1809-4422asoc20190020r2vu2020l4ao

    Article  Google Scholar 

  • Bento D, Ferreira R, Prous X, Souza-Silva M, Bellini B, Vasconcellos A (2016) Seasonal variations in cave invertebrate communities in the semiarid Caatinga, Brazil. J Cave Karst Stud 78(2):61–71. https://doi.org/10.4311/2015lsc0111

    Article  Google Scholar 

  • Benzing DH, Bennett B, Brown G et al (2000) Bromeliaceae. Bromeliaceae. https://doi.org/10.1017/cbo9780511565175

    Article  Google Scholar 

  • Blondel J (2003) Guilds or functional groups: Does it matter? Oikos 100:223–231. https://doi.org/10.1034/j.1600-0706.2003.12152.x

    Article  Google Scholar 

  • Bommarco R, Miranda F, Bylund H, Bjorkman C (2011) Insecticides suppress natural enemies and increase pest damage in cabbage. J Econ Entomol 104:782–791

    Article  CAS  PubMed  Google Scholar 

  • Botelho JB, Weigel VACM (2011) Comunidade sateré-mawé Y’Apyrehyt: ritual e saúde na periferia urbana de Manaus. História, Ciências, Saúde-Manguinhos 18:723–744

    Article  PubMed  Google Scholar 

  • BPBES/REBIPP (2019) Relatório temático sobre Polinização, Polinizadores e Produção de Alimentos no Brasil. Wolowski M, Agostini K, Rech AR, Varassin IG, Maués M, Freitas L, Carneiro LT, Bueno RO, Consolaro H, Carvalheiro L, Saraiva AM, Silva CI. Padgurschi MCG (Org.). 1ª edição, São Carlos, SP: Editora Cubo. 184 páginas. https://doi.org/10.4322/978-85-60064-83-0

  • Brock RE, Cini A, Sumner S (2021) Ecosystem services provided by aculeate wasps. Biol Rev 96:1645–1675. https://doi.org/10.1111/brv.12719

    Article  PubMed  Google Scholar 

  • Brown SGA, Haas MA, Blsck JA, Parameswaran A, Woods GM, Heddle RJ (2004) In vitro testing to diagnose venom allergy and monitor immunotherapy: a placebo-controlled, crossover trial. Clin Exp Allergy 34:792–800

    Article  CAS  PubMed  Google Scholar 

  • Brown SL, Nesse RM, Vinokur AD, Smith DM (2003) Providing social support may be more beneficial than receiving it: results from a prospective study of mortality. Psychol Sci 14(4):320–327. https://doi.org/10.1111/1467-9280.14461

    Article  PubMed  Google Scholar 

  • Cammeraat ELH, Risch AC (2008) The impact of ants on mineral soil properties and processes at different spatial scales. J Appl Entomol 132:285–294

    Article  CAS  Google Scholar 

  • Carreck N, Williams I (1998) The economic value of bees in the UK. Bee World 79:115–123

    Article  Google Scholar 

  • Castaldo S, Capasso F (2002) Propolis, an old remedy used in modern medicine. Fitoterapia 73:S1–S6

    Article  CAS  PubMed  Google Scholar 

  • Celli G, Maccagnani B (2003) Honey bees as bioindicators of environmental pollution. Bulletin of Insectology 56:137–139

    Google Scholar 

  • Cerdà A, Jurgensen M, Bodi M (2009) Effects of ants on water and soil losses from organically-managed citrus orchards in eastern Spain. Biologia 64:527–531

    Article  Google Scholar 

  • Chen Y, Akre RD (1994) Ants used as food and medicine in chine. The Food Insects Newsletter 7(2):1 8–11

    Google Scholar 

  • Chen G, Wang ZW, Qin Y, Sun WB (2017) Seed dispersal by hornets: an unusual insect-plant mutualism. J Integr Plant Biol 59:792–796

    Article  PubMed  Google Scholar 

  • Corlett RT (2001) Pollination in a degraded tropical landscape: a Hong Kong case study. J Trop Ecol 17:155–161

    Article  Google Scholar 

  • Cortopassi-Laurino M, Imperatriz-Fonseca VL, Roubik DW, Dollin A, Heard T, Aguilar I, Venturieri GC, Eardley C, Nogueira-Neto P (2006) Global meliponiculture: challenges and opportunities. Apidologie 37:275–292

    Article  Google Scholar 

  • Das Neves RC, Trentini MM, de Castro e Silva J, Simon KS, Bocca AL, Silva LP, Mortari MR, Kipnis A, Junqueira-Kipnis AP (2016) Antimycobacterial activity of a new peptide polydim-i isolated from neotropical social wasp Polybia dimorpha. PLoS One 11:e0149729

    Article  PubMed  PubMed Central  Google Scholar 

  • Dauber J, Niechoj R, Baltruschat H, Wolters V (2008) Soil engineering ants increase grass root arbuscular mycorrhizal colonization. Biol Fertil Soils 44:791–796

    Article  Google Scholar 

  • De Souza MM, Louzada J, Serro JE, Cola Zanuncio J (2010) Social wasps (Hymenoptera: Vespidae) as indicators of conservation degree of riparian forests in Southeast Brazil. Sociobiology 56:387–396

    Google Scholar 

  • DeFoliart GR (1997) An overview of the role of edible insects in preserving biodiversity. Ecol Food Nutr 36:109–132

    Article  Google Scholar 

  • DeFoliart GR (1999) Insects as food: why the Western attitude is important. Annu Rev Entomol 44:21–50

    Article  CAS  PubMed  Google Scholar 

  • Del Toro I, Floyd K, Gardea-Torresdey J, Borrok D (2010) Heavy metal distribution and bioaccumulation in Chihuahuan Desert rough harvester ant (Pogonomyrmex rugosus) populations. Environ Pollut 158:1281–1287

    Article  PubMed  Google Scholar 

  • Del Toro I, Ribbons R, Pelini SL (2012) The little things that run the world revisited: a review of ant-mediated ecosystem services and disservices (Hymenoptera: Formicidae). Myrmecological News 17:133–146

    Google Scholar 

  • Del Toro I, Ribbons RR, Ellison AM (2015) Ant-mediated ecosystem functions on a warmer planet: effects on soil movement, decomposition and nutrient cycling. J Anim Ecol 84:1233–1241

    Article  PubMed  Google Scholar 

  • Duplantier JE, Freeman TM, Bahna SL, Good RA, Sher MR (1998) Successful rush immunotherapy for anaphylaxis to imported fire ants. J Allergy Clin Immunol 101:855–856

    Article  CAS  PubMed  Google Scholar 

  • Drummond F, Choat B (2011) Ants as biological control agents in agricultural cropping systems. Terr Arthropod Rev 4:157–180

    Article  Google Scholar 

  • Eldridge DJ, Bowker MA, Maestre FT, Roger E, Reynolds JF, Whitford WG (2011) Impacts of shrub encroachment on ecosystem structure and functioning: towards a global synthesis. Ecol Lett 14:709–722. https://doi.org/10.1111/j.1461-0248.2011.01630.x

    Article  PubMed  PubMed Central  Google Scholar 

  • Elisei T (2017) Vespas sociais (Hymenoptera, Vespidae, Polistinae) do estado da Paraíba: diversidade e estudo comportamental. Universidade Federal da Paraíba, Tese

    Google Scholar 

  • Elizalde L, Arbetman M, Arnan X, Eggleton P, Leal IR, Lescano MN, Saez A, Werenkraut V, Pirk GI (2020) The ecosystem services provided by social insects: traits, management tools and knowledge gaps. Biol Rev 95:1418–1441. https://doi.org/10.1111/brv.12616

    Article  PubMed  Google Scholar 

  • Farji-Brener AG, Werenkraut V (2017) The effects of ant nests on soil fertility and plant performance: a meta-analysis. J Animal Ecol 86:866–877

    Article  Google Scholar 

  • Fateryga A (2010) Trophic relations between vespid wasps (Hymenoptera, Vespidae) and flowering plants in the Crimea. Entomol Rev 90:698–705

    Article  Google Scholar 

  • Frouz J, Jilková V (2008) The effect of ants on soil properties and processes (Hymenoptera: Formicidae). Myrmecological News 11:191–199

    Google Scholar 

  • Gaston KJ, Lawton JH (1988) Patterns in the distribution and abundance of insect populations. Nature 331:709–712

    Article  Google Scholar 

  • Ginzburg O, Whitford WG, Steinberger Y (2008) Effects of harvester ant (Messor spp.) activity on soil properties and microbial communities in a Negev Desert ecosystem. Biol Fertil Soils 45:165–173

    Article  Google Scholar 

  • Ghosh S, Jeon H, Jung C (2020) Foraging behavior and preference of pollen sources by honey bee (Apis mellifera) relative to protein contents. J Ecol Environ 44:4. https://doi.org/10.1186/1743-7075-9-61

    Article  Google Scholar 

  • Gonthier DJ, Kuesel R, Perfecto I (2015) Pest suppression by ant biodiversity is modified by pest biodiversity. PeerJ Preprints:1–23

  • Gould WP, Jeanne RL (1984) Polistes wasps (Hymenoptera:Vespidae) as control agents for lepidopterous cabbage pests. Environ Entomol 13:150–156

    Article  Google Scholar 

  • Greeney HF, Dyer LA, Smilanich AM (2012) Feeding by lepidopteran larvae is dangerous: a review of caterpillars’ chemical, physiological, morphological, and behavioral defenses against natural enemies. Invertebr Surviv J 9:7–34

    Google Scholar 

  • Griffiths HM, Ashton LA, Walker AE, Hasan F, Evans TA, Eggleton P, Parr CL (2018) Ants are the major agents of resource removal from tropical rainforests. J Anim Ecol 87:293–300

    Article  PubMed  Google Scholar 

  • Grissell E (2010) Bees, wasps, and ants: The indispensable role of Hymenoptera in gardens. Timber Press, Portland, Oregon and London, p 336

    Google Scholar 

  • Hallett AC, Mitchell RJ, Chamberlain ER, Karron JD (2017) Pollination success following loss of a frequent pollinator: the role of compensatory visitation by other effective pollinators. AoB Plants 9:plx020

    Article  PubMed  PubMed Central  Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4(1):9pp. Harper DAT. (ed.). 1999. Numerical Palaeobiology. John Wiley & Sons.

  • Harris RJ (1991) Diet of the wasps Vespula vulgaris and V. Germanica in honeydew beech forest of the South Island, New Zealand. NZ J Zool 18:159–169

    Article  Google Scholar 

  • Hölldobler B, Wilson EO (1990) The ants, 1st edn. Harvard University Press, Cambridge, MA, p 732

    Book  Google Scholar 

  • Hunt JH, Rossi AM, Holmberg NJ, Smith SR, Sherman WR (1998) Nutrients in social wasp (Hymenoptera: Vespidae, Polistinae) honey. Ann Entomol Soc Am 91:466–472

    Article  CAS  Google Scholar 

  • IBGE (2023) Produção agrícola municipal: culturas temporárias e permanentes. IBGE, Rio de Janeiro

    Google Scholar 

  • IPBES (2016). The assessment report of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services on pollinators, pollination and food production. Potts SG, Imperatriz-Fonseca VL, Ngo HT (eds). Secretariat of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services, Bonn, Germany. 552 pages. https://doi.org/10.5281/zenodo.3402856

  • Islair P, Carvalho KS, Ferreira FC, Zina J (2014) Bromeliads in Caatinga: an oasis for invertebrates. Biotemas 28(1):67

    Article  Google Scholar 

  • Iverson AL, Marín LE, Ennis KK, Gonthier DJ, Connor-Barrie BT, Remfert JL, Cardinale BJ, Perfecto I (2014) Review: Do polycultures promote win-wins or trade-offs in agricultural ecosystem services? A meta-analysis. J Appl Ecol 51:1593–1602. https://doi.org/10.1111/1365-2664.12334

    Article  Google Scholar 

  • Jones R (2019) Wasp. Reaktion Books Ltd, London

    Google Scholar 

  • Jorge JS, Rocha LHS, Silva Jorge JP et al (2018) Floral visitors and potential pollinators of a rupicolous bromeliad (Pitcairnioideae) in the Brazilian semiarid. Neotrop Biol Conserv 13:101–110. https://doi.org/10.4013/nbc.2018.132.02

    Article  Google Scholar 

  • Jorge JS, Sales RFD, Santos RL, Freire EMX (2020) Living among thorns: herpetofaunal community (Anura and Squamata) associated to the rupicolous bromeliad Encholirium spectabile (Pitcairnioideae) in the Brazilian semi-arid Caatinga. Zoologia 37:1–12. https://doi.org/10.3897/zoologia.37.e46661

    Article  Google Scholar 

  • Jorge JS, Silva-Jorge JP, Santos RL et al (2021b) Association of Strymon serapio (Lycaenidae: Theclinae) and Castnia invaria (Castniidae: Castniini) with the habitat-forming bromeliad Encholirium spectabile (Bromeliaceae: Pitcairnioideae) in the Brazilian Semiarid Caatinga. J Lepid Soc 75:37–43. https://doi.org/10.18473/lepi.75i1.a5

    Article  Google Scholar 

  • Jorge JS, Sousa PHP, de Albuquerque França BR et al (2023) Among flowers and thorns: birds associated with Encholirium spectabile, a keystone bromeliad in a Brazilian semi-arid region. Ornithol Res 31:93–102. https://doi.org/10.1007/s43388-023-00129-1

    Article  Google Scholar 

  • Jorge JS, Freire EMX, Caliman A (2021a) The rupicolous bromeliad (Encholirium spectabile) as a keystone species for Brazilian semiarid biodiversity. Ecology 102:. https://doi.org/10.1002/ecy.3357

  • Kaspari M, Chang C, Weaver J (2010) Salted roads and sodium limitation in a northern forest ant community. Ecol Entomol 35:543–548

    Article  Google Scholar 

  • Kaspari M, Yanoviak SP (2009) Biogeochemistry and the structure of tropical brown food webs. Ecology 90:3342–3351

    Article  PubMed  Google Scholar 

  • Kevan P, Nunes-Silva P (2021) Pollination and agriculture. In: Encyclopedia of social insects, Starr, CK

  • King JR, Warren RJ, Maynard DS, Bradford MA (2018) Ants: ecology and impacts in dead wood. In: Ulyshen MD (ed) Saproxylic insects, zoological monographs, 1st edn, pp 237–262

  • Kitching RL (2000) Food Webs and Container Habitats: The Natural History and Ecology of Phytotelmata. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Klatt B, Holzschuh A, Westphal C, Clough Y, Smit I, Pawelzik E, Tscharntke T (2014) Bee pollination improves crop quality, shelf life and commercial value. Proc Biol Sci/ Royal Soc 281:20132440. https://doi.org/10.1098/rspb.2013.2440

    Article  Google Scholar 

  • Klein A-M, Vaissière B, Cane JH, Steffan-Dewenter I, Cunningham S, Kremen C, Tscharntke T (2006) Importance of pollinators in changing landscapes for world crops. Proc Royal Soc B: Biol Sci [SL] 274(1608):303–313. https://doi.org/10.1098/rspb.2006.3721

    Article  Google Scholar 

  • Krell R (1996) Value-added products from beekeeping. In: FAO agricultural services bulletin, 124. Food and Agriculture Organization of the United Nations, Rome

    Google Scholar 

  • Kroiss J, Kaltenpoth M, Schneider B, Schwinger MG, Hertweck C, Maddula RK, Strohm E, Svatos A (2010) Symbiotic Streptomycetes provide antibiotic combination prophylaxis for wasp offspring. Nat Chem Biol 6(4):261–263. https://doi.org/10.1038/nchembio.331

    Article  CAS  PubMed  Google Scholar 

  • Lavelle P, Decaens T, Aubert M, Barot S, Blouin M, Bureau F, Margerie P, Mora P, Rossi J (2006) Soil invertebrates and ecosystem services. Eur J Soil Biol 42:S3–S15

    Article  Google Scholar 

  • Lengyel S, Gove AD, Latimer AM, Majer JD, Dunn RR (2010) Convergent evolution of seed dispersal by ants, and phylogeny and biogeography in flowering plants: a global survey. Perspect Plant Ecol Evol Syst 12:43–55

    Article  Google Scholar 

  • Levin E, Yom-Tov Y, Barnea A (2009) Frequent summer nuptial flights of ants provide a primary food source for bats. Naturwissenschaften 96:477–483

    Article  CAS  PubMed  Google Scholar 

  • Liu C, Han C, Jiang S, Zhao X, Tian Y, Yan K, Wang X, Xiang W (2018) Streptomyces lasii sp. nov., a novel actinomycete with antifungal activity isolated from the head of an ant (Lasius flavus). Curr Microbiol 75:353–358

    Article  CAS  PubMed  Google Scholar 

  • Lobry de Bruyn LA (1999) Ants as bioindicators of soil function in rural environments. Agric Ecosyst Environ 74:425–441

    Article  Google Scholar 

  • Majer JD (1976) The influence of ants and ant manipulation on the cocoa farm fauna. J Appl Ecol 13:157–175

    Article  Google Scholar 

  • Majer JD (1983) Ants: bio-indicators of minesite rehabilitation, land-use, and land conservation. Environ Manag 7:375–383

    Article  Google Scholar 

  • Mant J, Brown GR, Weston PH (2005) Opportunistic pollinator shifts among sexually deceptive orchids indicated by a phylogeny of pollinating and non-pollinating thynnine wasps (Tiphiidae). Biol J Linn Soc 86:381–395

    Article  Google Scholar 

  • Mant JG, Schiestl FP, Peakall R, Weston PH (2002) A phylogenetic study of pollinator conservatism among sexually deceptive orchids. Evolution 56:888–898

    CAS  PubMed  Google Scholar 

  • Mariño-Pérez RM-AC (2006) Los insectos en el Cine: un es-tudio preliminar. Boletín Sociedad Entomológica Aragonesa 36:413–421

    Google Scholar 

  • Matias DMS, Leventon J, Rau A-L, Borgemeister C, von Wehrden H (2017) A review of ecosystem service benefits from wild bees across social contexts. Ambio 46:456–467. https://doi.org/10.1007/s13280-016-0844-z

    Article  PubMed  Google Scholar 

  • Mello MAR, de Santos GMM, Mechi MR, Hermes MG (2011) High generalization in flower-visiting networks of social wasps. Acta Oecol 37:37–42

    Article  Google Scholar 

  • Mendes TD, Borges WS, Rodrigues A, Solomon SE, Vieira PC, Duarte MCT, Pagnocca FC (2013) Anti-Candida properties of urauchimycins from actinobacteria associated with Trachymyrmex ants. Biomed Res Int 2013:835081

    Article  PubMed  PubMed Central  Google Scholar 

  • Millenium Ecosystem Assessment. Ecosystems and Human Well-being: Synthesis. Washington DC: Island Press; 2005. www.millenniumassessment.org. Accessed 20 Jun 2022

  • Moreno M, Zurita E, Giralt E (2014) Delivering wasp venom for cancer therapy. J Control Release 182:13–21

    Article  CAS  PubMed  Google Scholar 

  • Mortimer R, Saj S, David C (2018) Supporting and regulating ecosystem services in cacao agroforestry systems. Agrofor Syst 92:1639–1657

    Article  Google Scholar 

  • Ness JH, Bronstein JL, Andersen AN, Holland JN (2004) Ant body size predicts dispersal distance of ant-adapted seeds: implications of small-ant invasions. Ecology 85:1244–1250

    Article  Google Scholar 

  • Ness JH, Morin DF, Giladi I (2009) Uncommon specialization in a mutualism between a temperate herbaceous plant guild and an ant: are Aphaenogaster ants keystone mutualists? Oikos 118:1793–1804

    Article  Google Scholar 

  • Nonaka K (2010) Cultural and commercial roles of edible wasps in Japan. In: Durst PB, Johnson DV, Leslie RN, Shono K (eds) Forest insects as food: humans bite back. Food and Agriculture Organisation of the United Nations, Bangkok, pp 123–130

    Google Scholar 

  • Noriega JA, Hortal J, Azcarate FM, Berg MP, Bonada N, Briones MJI, del Toro I, Goulson D, Ibanez S, Landis DA, Moretti M, Potts SG, Slade EM, Stout JC, Ulyshen MD et al (2018) Research trends in ecosystem services provided by insects. Basic Appl Ecol 26:8–23

    Article  Google Scholar 

  • Paris CI, Polo MG, Garbagnoli C, Martinez P, de Ferre GS, Folgarait PJ (2008) Litter decomposition and soil organisms within and outside of Camponotus punctulatus nests in sown pasture in northeastern Argentina. Appl Soil Ecol 40:271–282

    Article  Google Scholar 

  • Parr CL, Robertson HG, Biggs HC, Chown SL (2004) Response of African savanna ants to long-term fire re-gimes. J Appl Ecol 41:630–642

    Article  Google Scholar 

  • Peakall R (1989) The unique pollination of Leporella fimbriata (Orchidaceae) – pollination by pseudocopulating male ants (Myrmecia urens, Formicidae). Plant Syst Evol 167:137–148

    Article  Google Scholar 

  • Penn HJ, Crist TO (2018) From dispersal to predation: a global synthesis of ant–seed interactions. Ecol Evol 8:9122–9138. https://doi.org/10.1002/ece3.4377

    Article  PubMed  PubMed Central  Google Scholar 

  • Perez-Balam J, Quezada-Euan JJ, Alafaro-Bates R, Medina S, McKendrick L, Soro A, Paxton RJ (2012) The contribution of honey bees, flies and wasps to avocado (Persea americana) pollination in southern Mexico. J Pollinat Ecol 8:42–47

    Article  Google Scholar 

  • Perfecto I, Philpott, SM (2023) Ants (Hymenoptera: formicidae) and ecosystem functions and services in urban areas. Austrian Soc Entomofaunistics, [S.L.], p. 103–122. The Austrian Society of Entomofaunistics. https://doi.org/10.25849/MYRMECOL.NEWS_033:103

  • Philpott SM, Armbrecht I (2006) Biodiversity in tropical agroforests and the ecological role of ants and ant diversity in predatory function. Ecol Entomol 31:369–377

    Article  Google Scholar 

  • Polidori C, Gobbi M, Chatenoud L, Santoro D, Montani O, Andrietti F (2010) Taxon-biased diet preference in the ‘generalist’ beetlehunting wasp Cerceris rubida provides insights on the evolution of prey specialization in apoid wasps. Biol J Lin Soc 99:544–558

    Article  Google Scholar 

  • Porrini C, Ghini S, Sabatini AG GS, Gattavecchia E, Celli G (2002) Use of honey bees as bioindicators of environmental pollution in Italy. In: Devillers J, Pham-Delegue M-H (eds) Honey bees: estimating the environmental impact of chemicals. CRC Press, pp 200–261

    Google Scholar 

  • Preston C (2006) Bee - animal. Reaktion books

    Google Scholar 

  • Prezoto F, Maciel TT, Detoni M, Mayorquin AZ, Barbosa BC (2019) Pest control potential of social wasps in small farms and urban gardens. Insects 10:192

    Article  PubMed  PubMed Central  Google Scholar 

  • Puwastien P, Attig GA (1997) Edible insects in Thailand: an unconventional protein source? Ecol Food Nutr 36:133–149

    Article  Google Scholar 

  • Queiroz JA, Quirino ZGM, Lopes AV, Machado IC (2016) Vertebrate mixed pollination system in Encholirium spectabile: A bromeliad pollinated by bats, opossum and hummingbirds in a tropical dry forest. J Arid Environ 125:21–30. https://doi.org/10.1016/j.jaridenv.2015.09.015

    Article  Google Scholar 

  • Raksakantong P, Meeso N, Kubola J, Siriamornpun S (2010) Fatty acids and proximate composition of eight Thai edible terricolous insects. Food Res Int 43:350–355

    Article  CAS  Google Scholar 

  • Ramos Elorduy J, Rodríguez HB (1977) Valor nutritivo de ciertos insectos comestibles de México y lista de algunos insectos comestibles del mundo, vol 48. Instituto Biologico del la Uni-versidad Nacional Autonoma de Mexico Serie Zoologica, pp 165–186

    Google Scholar 

  • Rastogi N (2011) Provisioning services from ants: food and pharmaceuticals. Asian Myrmecol 4:103–120

    Google Scholar 

  • Reddy N, Xu HL, Yang YQ (2011) Unique natural-protein hollow-nanofiber membranes produced by weaver ants for medical applications. Biotechnol Bioeng 108:1726–1733

    Article  CAS  PubMed  Google Scholar 

  • Redford KH, Dorea JG (2009) The nutritional value of invertebrates with emphasis on ants and termites as food for mammals. J Zool 203:385–395

    Article  Google Scholar 

  • Ribeiro LB, Freire EMX (2011) Trophic ecology and foraging behavior of Tropidurus hispidus and Tropidurus semitaeniatus (Squamata, Tropiduridae) in a Caatinga area of northeastern Brazil. Iheringia Série Zoologia 101:225–232

    Article  Google Scholar 

  • Rizzini CT (1997) Tratado de fitogeografia do Brasil: aspectos ecológicos, sociológicos e florísticos, 2nd edn. Ambito Cultural, Rio de Janeiro

    Google Scholar 

  • Rostás M, Tautz J (2011) Ants as pollinators of plants and the role of floral scents. In: Dubinsky Z, Seckbach J (eds) All flesh is grass: plant-animal interrelationships. Springer, Netherlands, Dordrecht, pp 149–161

    Google Scholar 

  • Sales RFD, Ribeiro LB, Freire EMX (2011) Feeding ecology of Ameiva ameiva in a Caatinga area of northeastern Brazil. Herpetol J 21:199–207

    Google Scholar 

  • Santos WE, Carneiro LT, Alves ACF, Creão-Duarte AJ, Martins CF (2014) Stingless bees (Hymenoptera: Apidae: Meliponini) attracted to animal carcasses in the Brazilian Dry Forest and implications for forensic entomology. Sociobiology 61(4):490–493. https://doi.org/10.13102/sociobiology.v61i4.490-493

    Article  Google Scholar 

  • Santos L, Pieroni M, Menegasso A, Pinto J, Palma M (2011) A new scenario of bioprospecting of Hymenoptera venoms through proteomic approach. Journal of Venomous Animals and Toxins including Tropical Diseases (JVATiTD) 17:364–377

    CAS  Google Scholar 

  • Sears ALW, Smiley JT, Hilker M, Muller F, Rank NE (2001) Nesting behavior and prey use in two geographically separated populations of the specialist wasp Symmorphus cristatus (Vespidae: Eumeninae). Am Midl Nat 145:233–246

    Article  Google Scholar 

  • Shuttleworth A, Johnson SD (2012) The Hemipepsis wasp-pollination system in South Africa: a comparative analysis of trait convergence in a highly specialized plant guild. Bot J Linn Soc 168:278–299

    Article  Google Scholar 

  • Silva J, Monge-Fuentes V, Gomes F, Lopes K, Anjos L, Campos G, Arenas C, Biolchi A, Gonçalves J, Galantes P, Campos L, Mortari M (2015) Pharmacological alternatives for the treatment of neurodegenerative disorders: wasp and bee venoms and their components as new neuroactive tools. Toxins 7:3179–3209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Siri S, Maensiri S (2010) Alternative biomaterials: natural, non-woven, fibro in based silk nanofibers of weaver ants (Oecophylla smaragdina). Int J Biol Macromol 46:529–534

    Article  CAS  PubMed  Google Scholar 

  • Silveira FA, Melo GAR, Almeida EAB (2002) Abelhas Brasileiras: Sistemática e Identificação. Fundação Araucária, Belo Horizonte

    Google Scholar 

  • Skaldina O, Peraniemi S, Sorvari J (2018) Ants and their nests as indicators for industrial heavy metal contamination. Environ Pollut 240:574–581

    Article  CAS  PubMed  Google Scholar 

  • Slaa EJ, Sánchez Chaves LA, Malagodi-Braga KS, Hofstede FE (2006) Stingless bees in applied pollination: practice and perspectives. Apidologie 37:293–315

    Article  Google Scholar 

  • Sleigh C (2003) Ant - animal. Reaktion books

    Google Scholar 

  • Sleigh C (2004) Ant, 1st edn. University of Chicago Press, Chicago, p 216

    Google Scholar 

  • Somavilla A, Barbosa BC, Souza MM, Prezoto F (2021) List of species of social wasps from Brazil. In: Prezoto F, Nascimento FS, Barbosa BC, Somavilla A (2021) Neotropical social wasps: Basic and applied aspects. Springer Cham. https://doi.org/10.1007/978-3-030-53510-0

  • Southon RJ, Fernandes OA, Nascimento FS, Sumner S (2019) Social wasps are effective biocontrol agents of key lepidopteran crop pests. Proc Royal Soc: Biol Sci 286:20191676

    Google Scholar 

  • Southwick EE, Southwick L (1992) Estimating the economic value of honey bees (Hymenoptera: Apidae) as agricultural pollinators in the United States. J Econ Entomol 85:621–633

    Article  Google Scholar 

  • Sribandit W, Wiwatwitaya D, Suksard S, Offenberg J (2008) The importance of weaver ant (Oecophylla smaragdina Fabricus) harvest to a local community in northeastern Thailand. Asian Myrmecol 2:129–138

    Google Scholar 

  • StatSoft Inc (2001) STATISTICA (Data Analysis Software System), Version 10. http://www.statsoft.com. Accessed 20 Jun 2022

  • Sumner S, Law G, Cini A (2018) Why we love bees and hate wasps. Ecol Entomol 43:836–845

    Article  Google Scholar 

  • Urbini A, Sparvoli E, Turillazzi S (2006) Social paper wasps as bioindicators: a preliminary research with Polistes dominulus (Hymenoptera Vespidae) as a trace metal accumulator. Chemosphere 64:697–703

    Article  CAS  PubMed  Google Scholar 

  • van Klink R, Bowler DE, Gongalsky KB, Swengel AB, Gentile A, Chase JM (2020) Meta-analysis reveals declines in terrestrial but increases in freshwater insect abundances. Science 368(6489):417–420. https://doi.org/10.1126/science.aax9931. (Erratum in: Science. 2020 Oct 23;370(6515))

    Article  CAS  PubMed  Google Scholar 

  • Van Mele P (2008) A historical review of research on the weaver ant Oecophylla in biological control. Agric Forest Entomol 10:13–22

    Article  Google Scholar 

  • Van Mele P, Cuc NTT (2001) Farmers' perceptions and practices in use of Dolichoderus thoracicus (SMITH) (Hyme-noptera: Formicidae) for biological control of pests of sapo-dilla. Biol Control 20:23–29

    Article  Google Scholar 

  • Vandermeer J, Perfecto I, Philpott S (2010) Ecological complexity and pest control in organic coffee production:uncovering an autonomous ecosystem service. Bioscience 60:527–537

    Article  Google Scholar 

  • Vasconcellos A, Andreazze R, Almeida AM, Araujo HF, Oliveira ES, Oliveira U (2010) Seasonality of insects in the semi-arid Caatinga of northeastern Brazil. Revista Brasileira de Entomologia 54:471–476

    Article  Google Scholar 

  • Vega C, Gómez JM (2014) Polinización por hormigas: conceptos, evidencias y futuras direcciones. Revista Ecosistemas 23:48–57

    Google Scholar 

  • Vele A, Frouz J, Holusa J, Kalcik J (2010) Chemical properties of forest soils as affected by nests of Myrmica ruginodis (Formicidae). Biologia 65:122–127

    Article  CAS  Google Scholar 

  • Velloso AL, Sampaio EVSB, Pareyn FGC (2002) Ecorregiões Propostas para o Bioma Caatinga, 1st edn. The Nature Conservancy do Brasil, Recife

    Google Scholar 

  • Vieira LC, Oliveira NG, Gayubo SF (2011) On the use of Apiformes and Spheciformes (Insecta: Hymenoptera) populations as a management tool. Biodivers Conserv 20:519–530

    Article  Google Scholar 

  • Villas-Bôas JK (2018) Manual Tecnológico de Aproveitamento Integral dos Produtos das Abelhas Nativas Sem Ferrão. In: Brasília - DF. Instituto Sociedade, População e Natureza (ISPN). 2a edição, Brasil

  • Vlasakova B, Raabova J, Kyncl T, Dostal P, Kovar-Ova M, Kovar P, Herben T (2009) Ants accelerate suc-cession from mountain grassland towards spruce forest. J Veg Sci 20:577–587

    Article  Google Scholar 

  • Wagner DL, Grames EM, Forister ML, Berenbaum MR, Stopak D (2021) Insect decline in the Anthropocene: death by a thousand cuts. Proc Natl Acad Sci [SL] 118(2):1–10. https://doi.org/10.1073/pnas.2023989118

    Article  CAS  Google Scholar 

  • Wagner D, Jones JB (2006) The impact of harvester ants on decomposition, N mineralization, litter quality, and the avail-ability of N to plants in the Mojave Desert. Soil Biol Biochem 38:2593–2601

    Article  CAS  Google Scholar 

  • Wallace HM, Howell MG, Ldd DJ (2008) Standard yet unusual mechanisms of long-distance dispersal: seed dispersal of Corymbia torelliana by bees. Divers Distrib 14:87–94

    Article  Google Scholar 

  • Wielgoss A, Tscharntke T, Rumede A, Fiala B, Seidel H, Shahabuddin S, Clough Y (2014) Interaction complexity matters: disentangling services and disservices of ant communities driving yield in tropical agroecosystems. Proc R Soc B Biol Sci 281:20132144

    Article  Google Scholar 

  • Wilson EE, Mullen LM, Holway DA (2009) Life history plasticity magnifies the ecological effects of a social wasp invasion. Proc Natl Acad Sci USA 106:12809–12813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Winfree R, Williams NM, Dushoff J, Kremen C (2007) Native bees provide insurance against ongoing honeybee losses. Ecol Lett 10:1105–1113

    Article  PubMed  Google Scholar 

  • Wolff A, Debussche M (1999) Ants as seed dispersers in a Mediterranean oldfield succession. Oikos 84:443–452

    Article  Google Scholar 

  • Yamada Y, Shinohara Y, Kakudo T, Chaki S, Futaki S, Kamiya H, Harashima H (2005) Mitochondrial delivery of mastoparan with transferrin liposomes equipped with a pH-sensitive fusogenic peptide for selective cancer therapy. Int J Pharm 303:1–7

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We also thank the employees of Fazenda Tanques for their support in the field and all others who helped by giving feedback to improve the manuscript. We also thank too the handling editor and the three anonymous reviewers for helpful comments on the manuscript.

Funding

This study was supported by research grants from the National Council for Scientific and Technological Development (CNPq) to JSJ (process130363/2014–6, 150053/2023–1) AC (process 304636/2022–3) and EMXF (process 313661/2017–0) and from the Coordination for the Improvement of Higher Education Personnel (CAPES).

Author information

Authors and Affiliations

Authors

Contributions

The first draft of the manuscript was written by JJ and AC. Data collection and analysis were performed by JJ, RLS, and AC. AFVD, RLS, and EMXF revised the text and adapted it to the journal’s norms. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Jaqueiuto S. Jorge.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Edited by Márcia M Maués

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 43 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jorge, J.S., Duarte, A.F.V., Santos, R.L. et al. Semi-arid’s Unsung Heroes: Hymenoptera and the Vital Ecosystem Services Enabled by Encholirium spectabile, a Rupicolous Bromeliad in the Brazilian Semi-arid Region. Neotrop Entomol 53, 514–530 (2024). https://doi.org/10.1007/s13744-024-01152-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13744-024-01152-7

Keywords

Navigation