Abstract
The ability to share and store food is paramount in group-living animals, allowing a finely tuned distribution of resources over time and individuals and an enhanced survival over periods of food scarcity. Ants have several ways to store food: one of them is their gastral crop, also known as a “social stomach.” Nutrients in the crop can be regurgitated to nestmates through oral trophallaxis (mouth-to-mouth) or proceed to the midgut by opening the proventriculus, a valve connecting the crop to the midgut. However, some ants are also known to have a so-called “thoracic crop,” an extension of the esophagus that allows for additional storage space. In this study, we provide the first evidence of a thoracic crop in the genus Carebara, in reproductive (queen) and sterile (soldier and worker) castes. We discuss how the ant body plan allowed for the evolution of a novel food storage structure in the mesothorax.
Similar content being viewed by others
References
Abdulmumeen HA, Risikat AN, Sururah AR (2012) Food: its preservatives, additives and applications. Int J Chem Biochem Sci 1:36–47. https://doi.org/10.13140/2.1.1623.5208
Aibekova L, Boudinot BE, Beutel RG et al (2022) The skeletomuscular system of the mesosoma of Formica rufa workers (Hymenoptera: Formicidae). Insect Syst 6:2. https://doi.org/10.1093/isd/ixac002
Anderson PSL, Rivera MD, Suarez AV (2020) “Simple” biomechanical model for ants reveals how correlated evolution among body segments minimizes variation in center of mass as heads get larger. Integr Comp Biol 60:1193–1207. https://doi.org/10.1093/icb/icaa027
Azorsa F, Fisher BL (2018) Taxonomy of the ant genus Carebara Westwood (Formicidae, Myrmicinae) in the Malagasy Region. Zookeys 767:1–149. https://doi.org/10.3897/zookeys.767.21105
Baroni Urbani C, de Andrade ML (1997) Pollen eating, storing, and spitting by ants. Naturwissenschaften 84(6):256–258
Børgesen LW (2000) Nutritional function of replete workers in the pharaoh’s ant, Monomorium pharaonis (L.). Insectes Soc 47:141–146. https://doi.org/10.1007/PL00001692
Burgett DM, Young RG (1974) Lipid storage by honey ant repletes. Ann Entomol Soc Am 67:743–744. https://doi.org/10.1093/aesa/67.5.743
Caetano FH (1988) Anatomia, histologia e histoquímica do sistema digestivo e excretor de operárias de formigas (Hymenoptera, Formicidae). Naturalia 13:129–174
Caetano FH (1993) Ultramorfologia del tracto digestivo de Neoponera villosa (Formicidae). In: Resumenes del XV Congreso Nacional de Entomologia (Vol. 11, p. 43)
Caetano FH, Camargo-Mathias MI, Overal WL (1986) Anatomia e histologia comparada do trato digestivo de Dinoponera gigantea e Paraponera clavata (Formicidae, Panerinae). Naturalia (São José Rio Preto) 11–12:125–134
Caetano FH, Lage Filho AL (1982) Anatomia e histologia do trato digestivo de formigas do gênero Odontomachus (Hymenoptera, Ponerinae). Naturalia (São José do Rio Preto) 7:125–134
Caetano FH, Tomotake MEM, Camargo-Mathias MI (1997) The role of ants esophagus in the trophallaxis. Recent advances in ecobiological research.–APH Publishing Corporation, New Delhi, pp 397–403
Caetano FH, Tomotake MEM, Pimentel MAL, Camargo-Mathias MI (1990) Internal morphology of workers of Dolichoderus attelaboides (Fabricius, 1775) (Formicidae: Dolichoderinae). I. Digestive tract and associated excretory system. Naturalia (São Paulo) 15:57–65
Casadei-Ferreira A, Fischer G, Economo EP (2020) Evidence for a thoracic crop in the workers of some Neotropical Pheidole species (Formicidae: Myrmicinae). Arthropod Struct Dev 59:100977. https://doi.org/10.1016/j.asd.2020.100977
Fischer G, Azorsa F, Hita Garcia F et al (2015) Two new phragmotic ant species from Africa: morphology and next-generation sequencing solve a caste association problem in the genus Carebara Westwood. ZooKeys 525:77–105. https://doi.org/10.3897/zookeys.525.6057
Gignac PM, Kley NJ, Clarke JA et al (2016) Diffusible iodine-based contrast-enhanced computed tomography (diceCT): an emerging tool for rapid, high-resolution, 3-D imaging of metazoan soft tissues. J Anat 228:889–909. https://doi.org/10.1111/joa.12449
Glancey BM, Glover A, Lofgren CS (1981) Thoracic crop formation following dealation by virgin females of two species of Solenopsis. Fla Entomol 64:454
Glancey BM, Stringer CE Jr, Craig CH et al (1973) Evidence of a replete caste in the fire ant Solenopsis invicta. Ann Entomol Soc Am 66:233–234. https://doi.org/10.1093/aesa/66.1.233
Gobin B, Peeters C, Billen J (1998) Production of trophic eggs by virgin workers in the ponerine ant Gnamptogenys menadensis. Physiol Entomol 23(4):329–336
Gobin B, Ito F (2000) Queens and major workers of Acanthomyrmex ferox redistribute nutrients with trophic eggs. Naturwissenschaften 87:323–326
Hasegawa E (1993) Caste specialization in food storage in the dimorphic ant Colobopsis nipponicus (Wheeler). Insectes Soc 40:261–271. https://doi.org/10.1007/BF01242362
Hashimoto Y, Yamauchi K, Hasegawa E (1995) Unique habits of stomodeal trophallaxis in the ponerine ant Hypoponera sp. Insect Soc 42:137–144
Hölldobler B (1966) Futterverteilung durch Männchen im Ameisenstaat. Zeitschrift für vergleichende Physiologie 52:430–455
Janet C (1907) Anatomie du corselet et histolyse des muscles vibrateurs, après le vol nuptial chez la reine de la fourmi: Lasius niger, vol 1. Ducourtieux et Gout
Johnson RA (2000) Seed-harvester ants (Hymenoptera: Formicidae) of North America: an overview of ecology and biogeography. Sociobiology 36:89–122
Keller RA, Peeters C, Beldade P (2014) Evolution of thorax architecture in ant castes highlights trade-off between flight and ground behaviors. Elife 3:e01539. https://doi.org/10.7554/eLife.01539
Keller RA, Peeters C (2021) Poneroid ants. In: Encyclopedia of social insects. Springer International Publishing, Cham, pp 749–754
Khalife A, Peeters C (2020) Food storage and morphological divergence between worker and soldier castes in a subterranean myrmicine ant, Carebara perpusilla. J Nat Hist 54:3131–3148. https://doi.org/10.1080/00222933.2021.1890851
Khalife A, Peeters C, Economo EP (2022) Minute workers and large soldiers in the subterranean ant Carebara perpusilla: musculoskeletal consequences of Haller’s rule in the thorax. Arthropod Struct Dev 69:101188. https://doi.org/10.1016/j.asd.2022.101188
Kuijt I, Finlayson B (2009) Evidence for food storage and predomestication granaries 11,000 years ago in the Jordan Valley. Proc Natl Acad Sci 106:10966–10970. https://doi.org/10.1073/pnas.0812764106
Kurihara Y, Ogawa K, Chiba Y et al (2022) Thoracic crop formation is spatiotemporally coordinated with flight muscle histolysis during claustral colony foundation in Lasius japonicus queens. Arthropod Struct Dev 69:101169. https://doi.org/10.1016/j.asd.2022.101169
Lachaud JP, Passera L, Grimal A et al (1992) Lipid storage by major workers and starvation resistance in the ant Pheidole pallidula (Hymenoptera, Formicidae). In: First European Congress of Social Insects, Leuven (Belgium), 19-22 Aug 1991. Leuven University Press
LeBoeuf AC, Waridel P, Brent CS, Gonçalves AN, Menin L, Ortiz D et al (2016) Oral transfer of chemical cues, growth proteins and hormones in social insects. elife 5:e20375. https://doi.org/10.7554/eLife.20375.001
Lee CC, Lin YT, Chiu MC, Yang CCS, Lin CC (2022) Preferential food allocation to an essential worker subcaste in the invasive yellow crazy ant, Anoplolepis gracilipes (Hymenoptera: Formicidae). Myrmecol News 32:139–147. https://doi.org/10.25849/myrmecol.news_032:139
Leistner L (2000) Basic aspects of food preservation by hurdle technology. Int J Food Microbiol 55:181–186. https://doi.org/10.1016/S0168-1605(00)00161-6
Limaye A (2012) Drishti: a volume exploration and presentation tool. In: Developments in x-ray tomography VIII. SPIE, pp 191–199
Liu S-P, Richter A, Stoessel A, Beutel RG (2019) The mesosomal anatomy of Myrmecia nigrocincta workers and evolutionary transformations in Formicidae (Hymenoptera). Arthropod Syst Phylogeny 77:1–19. https://doi.org/10.26049/ASP77-1-2019-01
Maschwitz U, Hahn M, Schönegge P (1979) Paralysis of prey in ponerine ants. Naturwissenschaften 66:213–214. https://doi.org/10.1007/BF00366035
Matte A, Billen J (2021) Flight muscle histolysis in Lasius niger queens. Asian Myrmecol 13. https://doi.org/10.20362/AM.013003
Meurville M-P, LeBoeuf AC (2021) Trophallaxis: the functions and evolution of social fluid exchange in ant colonies (Hymenoptera: Formicidae). Myrmecol News 31. https://doi.org/10.25849/MYRMECOL.NEWS_031:001
Moffett MW (1986) Notes on the behavior of the dimorphic ant Oligomyrmex overbecki (Hymenoptera: Formicidae). Psyche 93:107–116. https://doi.org/10.1155/1986/62438
Moffett MW (2019) Marauder ants (Carebara in part). In: Starr C (ed) Encyclopedia of social insects. Springer International Publishing, Cham, pp 1–8. https://doi.org/10.1007/978-3-319-90306-4_75-1
Morgan C (2012) Modeling modes of hunter-gatherer food storage. Am Antiq 77:714–736. https://doi.org/10.7183/0002-7316.77.4.714
Peeters C (1997) Morphologically ‘primitive’ ants: comparative review of social characters, and the importance of queen–worker dimorphism. In: Crespi BJ, Choe JC (eds) The evolution of social behaviour in insects and arachnids. Cambridge University Press, Cambridge, pp 372–391
Peeters C, Ito F (2015) Wingless and dwarf workers underlie the ecological success of ants (Hymenoptera: Formicidae). Myrmecol News 21:117–130
Peeters C, Keller RA, Khalife A et al (2020) The loss of flight in ant workers enabled an evolutionary redesign of the thorax for ground labour. Front Zool 17:33. https://doi.org/10.1186/s12983-020-00375-9
Peeters C, Lin C-C, Quinet Y et al (2013) Evolution of a soldier caste specialized to lay unfertilized eggs in the ant genus Crematogaster (subgenus Orthocrema). Arthropod Syst Phylogeny 42:257–264. https://doi.org/10.1016/j.asd.2013.02.003
Petersen-Braun M, Buschinger A (1975) Entstehung und Funktion eines thorakalen Kropfes bei Formiciden-Königinnen. Insect Soc 22:51–66. https://doi.org/10.1007/BF02223123
Reyes-López JL, Fernández-Haeger J (2002) Food storage in the nest and seed selectivity in the harvester ant Messor barbarus. Sociobiology 39:1–6
Rissing SW (1984) Replete caste production and allometry of workers in the honey ant, Myrmecocystus mexicanus Wesmael (Hymenoptera: Formicidae). J Kans Entomol Soc 57:347–350
Solis DR, Caetano FH, Yabuki AT, Moretti TC, Bueno OC (2009) Ultramorphology of the digestive tract of Paratrechina longicornis (Hymenoptera, Formicidae). Sociobiology 53(1):51–59
Solis DR, Rossi ML, Fox EGP, de Lima Nogueira N, Tanaka FAO, Bueno OC (2013) On the morphology of the digestive system of two Monomorium ant species. J Insect Sci 13(1):70
Steiner AL (1986) Stinging behaviour of solitary wasps. In: Piek T (ed) Venoms of the Hymenoptera. Biochemical, pharmacological and behavioural aspects. Academic Press, London, pp 63–148
Tschinkel WR (1999) Sociometry and sociogenesis of colony-level attributes of the Florida harvester ant (Hymenoptera: Formicidae). Ann Entomol Soc Am 92:80–89. https://doi.org/10.1093/aesa/92.1.80
Tsuji K (1990) Nutrient storage in the major workers of Pheidole ryukyuensis (Hymenoptera : Formicidae). Appl Entomol Zool 25:283–287. https://doi.org/10.1303/aez.25.283
Vander Meer RK, Glancey BM, Lofgren CS (1982) Biochemical changes in the crop, oesophagus and postpharyngeal gland of colony-founding red imported fire ant queens (Solenopsis invicta). Insect Biochem 12:123–127. https://doi.org/10.1016/0020-1790(82)90079-8
Wilson EO (1986) Caste and division of labor in Erebomyrma, a genus of dimorphic ants (Hymenoptera: Formicidae: Myrmicinae). Insectes Soc 33:59–69. https://doi.org/10.1007/BF02224035
Wilson EO (1984) The relation between caste ratios and division of labor in the ant genus Pheidole (Hymenoptera: Formicidae). Behav Ecol Sociobiol 16:89–98. https://doi.org/10.1007/BF00293108
Yang AS (2006) Seasonality, division of labor, and dynamics of colony-level nutrient storage in the ant Pheidole morrisi. Insectes Soc 53:456–462. https://doi.org/10.1007/s00040-005-0896-3
Yushkevich PA, Piven J, Hazlett HC, Smith RG, Ho S, Gee JC, Gerig G (2006) User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage 31(3):1116–1128
Zhuang Y, Xu W, Zhang G et al (2022) Unparalleled details of soft tissues in a Cretaceous ant. BMC Evol Biol 22:146. https://doi.org/10.1186/s12862-022-02099-2
Acknowledgements
We are grateful to the late Christian Peeters for stimulating conversations on food storage in ants and suggesting the potential interest of Carebara perpusilla’s esophagus. We thank the Okinawa Institute of Science and Technology Graduate University (OIST) Imaging Section for providing access to the micro-CT scanner. We also acknowledge the assistance of An Vandoren in producing the histological sections.
Funding
This work was supported by subsidy funding to OIST and Japanese Society for the Promotion of Science (JSPS) grants (KAKENHI grant-in-aid 22F22761 for AK and 17K15180 for EPE).
Author information
Authors and Affiliations
Contributions
Adam Khalife: methodology, investigation (microCT and behavior), visualization, and writing—original draft; Johan Billen: investigation (histology), visualization, and writing—review and editing; Evan P. Economo: supervision, conceptualization, resources, and writing—review and editing.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Communicated by: Matthias Waltert
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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.
About this article
Cite this article
Khalife, A., Billen, J. & Economo, E.P. Evidence of a thoracic crop in workers, soldiers, and queens of Carebara perpusilla ants (Formicidae: Myrmicinae). Sci Nat 110, 36 (2023). https://doi.org/10.1007/s00114-023-01866-5
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00114-023-01866-5