Abstract
Workers of the red imported fire ant Solenopsis invicta are repeatedly claimed in the literature not to have ovaries. Here, we demonstrate that we cannot find a source publication that proves the statement, and we show how publications are erroneously citing this statement. To remedy this gap, we dissected 87 S. invicta workers over a range of worker sizes, and demonstrate that S. invicta workers do not have reproductive organs. To the best of our knowledge, this is the first time such a demonstration has been published in the scientific literature. We flag that the same issue of a lack of published evidence for the same statement likely exists for many other species and genera, precluding the ability for appropriate referencing of such details.
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Introduction
Citing publications to substantiate claims or facts, or to show congruency or not with prior results, is a cornerstone of scientific writing. As part of this process, authors are responsible for ensuring that the references they select genuinely support the statement they have written. To do so requires authors to read the references being cited to verify the appropriateness of the paper. Inadequate verification of citations can lead to perpetuation of inaccuracies within the scientific literature, which can become an overwhelming influence given that it has been estimated that 70–90% of scientific citations are copied from reference lists of other papers rather than from the original paper (Simkin and Roychowdhury 2005). Such issues erode the integrity of scientific literature (Santini 2018).
Inaccurate citing is nothing new to scientific writing and has been the lament of numerous publications. Among the numerous issues are incorrect summaries of work (Hernandez and White 1989; Stordal 2009; van de Weert and Stella 2019), and the rise of a persistent incorrect description or understanding of a scenario, such as of the native ant extinctions in Madeira by Pheidole megacephala and Linepithema humile (Wetterer 2006). Here, we present an unusual scenario, whereby we agree that the statement being made is correct, but there appears to be no baseline publication that can be truly cited, either because it never existed, or that demonstrative publication has been lost to knowledge. This statement is that “red imported fire ant Solenopsis invicta workers do not have ovaries”. This statement is cited in many papers, and is a critical underlying basis of highly influential works on eusociality and inclusive fitness (e.g., Keller and Ross 1998). Here, we demonstrate that we cannot find a source publication that proves this statement, we demonstrate how publications are erroneously citing this statement, and finally we provide demonstrative proof of the statement, which to the best of our knowledge is the first time this has been published in the scientific literature.
Materials and methods
We first tried to find a publication that demonstrated S. invicta workers do not have ovaries. We anticipated that demonstration would be in the form of quantified dissections of workers finding a lack of ovarioles and potentially other structures associated with reproduction, such as in Bickford (1895, 1897). To do this, we conducted a literature search using the ISI Web of Science platform and Google Scholar using the following search terms: “ant”, “Solenopsis”, “invicta”, “ovar*”, “steril*”. We also conducted targeted searches of any references cited within publications stating that S. invicta or Solenopsis workers did not have ovaries and/or were sterile. After not finding any suitable references from those searches, we conducted another literature search for the Spanish words “hormiga”, “obrera”, and “ovarios”, on the basis that the native range of S. invicta is within countries that speak Spanish. After again not finding a suitable reference, we then repeated the search in German, Portuguese, and Dutch.
To demonstrate how publications were citing that S. invicta or Solenopsis workers did not have ovaries and/or were sterile, we generated a flow chart. We also compiled a list of papers that provided no citation to support the statement (Fig. 1). Note that these summaries were not intended to be comprehensive of all global literature, just representative to demonstrate the issue. These summaries were also restricted to literature written in English.
Upon not finding any publication that met the criteria of demonstrating that S. invicta workers do not have ovaries, we dissected S. invicta workers to quantify the presence/absence of reproductive structures, specifically ovarioles and spermatheca. Hand collections were made from four nests from throughout Brisbane. Most workers were preserved upon arrival at the Brisbane laboratory, but 25 random workers from each nest were kept alive for 48 h in Brisbane and fed pH-indicating dye to aid photography following dissection. When killed, all workers were preserved in 100% ethanol. A total of 87 workers were dissected, 25 using a Nikon SMZ25 stereoscopic microscope in Brisbane, and 62 using a Zeiss Stemi 2000-C stereoscopic microscope in Darwin.
Because S. invicta is polymorphic (Mirenda and Vinson, 1981), we dissected individuals that represented the full-size range of the individuals collected, in case a subset of workers had reproductive structures such as occurs in yellow crazy ant Anoplolepis gracilipes (Lee et al. 2017; Lenancker et al. 2021). To demonstrate the morphometric diversity we assessed, we measured standard morphometrics of the 62 specimens dissected in Darwin. First, the bodies of the ants (minus the abdomens) were glued to cardboard triangles as per standard ant curation. Then, using the Darwin microscope with an ocular ruler, the individuals were positioned so that their heads were perpendicular to the view, and their head length and width were measured (Fig. 2).
Results
We found many publications were being cited to reference the statement Solenopsis or S. invicta workers do not have ovaries and/or are sterile (Fig. 1), and numerous publications that provided no citation to support the statement (e.g., Aron et al. 1995; Gadagkar 2019; Manfredini et al. 2014; Villalta et al. 2018), but we found no publication that provided any data or evidence that S. invicta workers do not have ovaries. None of the 87 workers dissected contained ovarioles or spermatheca, but all other major abdominal organs were found (Fig. 3).
Discussion
This paper is the first known publication of quantified work that demonstrates S. invicta workers do not have ovaries. Our findings align with the often made statement that workers of this species are completely sterile, not even able to contribute trophic eggs to colony nutrition, as can occur in other ant species (Bourke 1988). We were certainly not the first people to dissect this species to conduct the same investigation though, as we had informal discussions with numerous researchers who had historically done so, but they had not published quantified findings. Potentially such a quantitative study has been conducted and published previously, but if so the knowledge of its existence appears to have been lost. That others have also been unable to find a baseline publication is clear from the large number of different and inappropriate papers being cited to support the statement. Indeed, even one of us (BDH) was found to have previously made this citation error within Lenancker et al. (2019). We acknowledge that the samples were obtained from the invasive range only, but we are unaware of any instance of a species having different organ composition between its native ant exotic range as has been shown for other aspects such as morphology, diet and colony structure (Wills et al. 2014).
Although our work focused solely on S. invicta, while reading literature associated with our searches, we noted that many other species and genera were stated as not having ovaries, but we did not come across the base research that proved those statements. Likely most of these statements are correct, but we foresee that the same referencing issue we have identified here may extend to many other ant species and genera. Moreover, while most are likely correct, some may well not be. We suggest to the scientific community that if their own literature searches fail to find a base publication that supports a statement, especially a broad statement used often in publications, there may be a general need for somebody to conduct a simple demonstrative investigation to provide an adequate reference. Such work could indeed be highly beneficial should the broad statement prove to be erroneous (Letrud and Hernes 2019).
References
Aron S, Vargot EL, Passera L (1995) Primary and secondary sex ratios in monogyne colonies of the fire ant. Anim Behav 49(3):749–757. https://doi.org/10.1016/0003-3472(95)80207-X
Bickford EE (1897) Ueber die morphologie und physiologie der ovarien der ameisen arbeiterinnen. Zool Jahrb 9:1–26
Bickford EE (1895) Ueber die morphologie und physiologie der ovarien der ameisen-arbeiterinnen. PhD dissertation. University of Freiburg. Gustav Fischer Jena, pp 1–31 pls 1 and 2
Bourke AFG (1988) Worker reproduction in the higher eusocial Hymenoptera. Quart Rev Biol 63(3):291–311
Bourke AFG, Franks NR (1995) Social evolution in ants. Princeton University Press, New Jersey, p 529
Cole BJ (1986) The social behavior of Leptothorax allardycei (Hymenoptera, Formicidae): time budgets and the evolution of worker reproduction. Behav Ecol Sociobiol 18:165–173. https://doi.org/10.1007/BF00290820
Deheer C, Tschinkel W (1998) The success of alternative reproductive tactics in monogyne populations of the ant Solenopsis invicta: significance for transitions in social organization. Behav Ecol 9(2):130–135
Dietemann V, Hölldobler B, Peeters C (2002) Caste specialization and differentiation in reproductive potential in the phylogenetically primitive ant Myrmecia gulosa. Insectes Soc 49:289–298. https://doi.org/10.1007/s00040-002-8316-9
Endler A, Liebig J, Schmitt T, Parker JE, Jones GR, Schreier P, Hölldobler B (2004) Surface hydrocarbons of queen eggs regulate worker reproduction in a social insect. Proc Natl Acad Sci 101(9):2945–2950. https://doi.org/10.1073/pnas.0308447101
Fletcher DJC, Ross KG (1985) Regulation of reproduction in eusocial Hymenoptera. Ann Rev Entomol 30:319–343. https://doi.org/10.1146/annurev.en.30.010185.001535
Gadagkar R (2019) Ant, bee and wasp social evolution. In: Choe JC (ed) Encyclopedia of animal behavior, 2nd edn. Elsevier, pp 599–608
Goetsch W (1953) Vergleichende biologie der insektenstaaten. Geest and Portig, Leipzig Germany, p 482
Hawkings C, Tamborindeguy C (2018) Expression analysis of vitellogenins in the workers of the red imported fire ant (Solenopsis invicta). Peer J 6:e4875. https://doi.org/10.7717/peerj.4875
Hawkings C, Calkins TL, Pietrantonio PV, Tamborindeguy C (2019) Caste-based differential transcriptional expression of hexamerins in response to a juvenile hormone analog in the red imported fire ant (Solenopsis invicta). PLoS ONE 14(5):e0216800. https://doi.org/10.1371/journal.pone.0216800
Heinze J (2008) The demise of the standard ant (Hymenoptera: formicidae). Myrmecological News 11:9–20
Hernandez NR, White A (1989) Pass it on: errors in direct quotes in a sample of scholarly journal articles. J Couns Dev 67:509–512. https://doi.org/10.1002/j.1556-6676.1989.tb02132.x
Hölldobler B, Wilson EO (1990) The ants. Harvard University Press Springer-Verlag, Berlin, p 732
Keller L, Ross KG (1998) Selfish genes: a green beard in the red fire ant. Nature 394:573–575
Khila A, Abouheif E (2008) Reproductive constraint is a developmental mechanism that maintains social harmony in advanced ant societies. Proc Natl Acad Sci USA 105(46):17884–17889. https://doi.org/10.1073/pnas.0807351105
Lee C-C, Nakao H, Tseng S-P, Hsu H-W, Lin G-L, Tay J-W, Billen J, Ito F, Lee C-Y, Lin C-C, Yang C-C (2017) Worker reproduction of the invasive yellow crazy ant Anoplolepis gracilipes. Zoology 14:24. https://doi.org/10.1186/s12983-017-0210-4
Lenancker P, Hoffmann BD, Tay WT, Lach L (2019) Strategies of the invasive tropical fire ant (Solenopsis geminata) to minimize inbreeding costs. Sci Rep 9:4566. https://doi.org/10.1038/s41598-019-41031-5
Lenancker P, Feldhaar H, Holzinger A, Greenfield M, Strain A, Yeeles P, Hoffmann BD, Tay WT, Lach L (2021) Origin, behaviour and genetics of reproductive workers in an invasive ant. Front Zool 18(13):1–16. https://doi.org/10.1186/s12983-021-00392-2
Letrud K, Hernes S (2019) Affirmative citation bias in scientific myth debunking: a three-in-one case study. PLoS One 14(9):e0222213
Manfredini F, Lucas C, Nicolas M, Keller L, Shoemaker D, Grozinger CM (2014) Molecular and social regulation of worker division of labour in fire ants. Mol Ecol 23(3):660–672. https://doi.org/10.1111/mec.12626
Mirenda JT, Vinson SB (1981) Division of labour and specification of castes in the red imported fire ant Solenopsis invicta Buren. Anim Behav 29:410–420. https://doi.org/10.1016/S0003-3472(81)80100-5
Oster GF, Wilson EO (1978) Caste and ecology in the social insects. Princeton University Press, New Jersey, p 352
Ross KG, Fletcher DJ (1985) Comparative study of genetic and social structure in two forms of the fire ant Solenopsis invicta (Hymenoptera: formicidae). Behav Ecol Sociobiol 17:349–356. https://doi.org/10.1007/BF00293212
Ross KG, Vargo EL, Fletcher DJ (1988) Colony genetic structure and queen mating frequency in fire ants of the subgenus Solenopsis (Hymenoptera: formicidae). Biol J Lin Soc 34(2):105–117. https://doi.org/10.1111/j.1095-8312.1988.tb01952.x
Santini A (2018) The Importance of Referencing. J Crit Care Med 4(1):3–4. https://doi.org/10.1515/jccm-2018-0002.PMID:29967893;PMCID:PMC5953266
Simkin MV, Roychowdhury VP (2005) Stochastic modeling of citation slips. Scientometrics 62:367–384. https://doi.org/10.1007/s11192-005-0028-2
Stordal B (2009) Citations, citations everywhere but did anyone read the paper? Colloids Surfaces Biointerfaces 72(2):312–313. https://doi.org/10.1016/j.colsurfb.2009.04.001
Tschinkel W (1988) Distribution of the fire ants Solenopsis invicta and S. geminata (Hymenoptera: Formicidae) in northern Florida in relation to habitat and disturbance. Ann Entomol Soc Am 81(1):76–81. https://doi.org/10.1093/aesa/81.1.76
Van de Weert M, Stella L (2019) The dangers of citing papers you did not read or understand. J Mol Struct 1186:102–103. https://doi.org/10.1016/j.molstruc.2019.03.024
Villalta I, Abril S, Cerdá X, Boulay R (2018) Queen control or queen signal in ants: what remains of the controversy 25 years after Keller and Nonacs’ seminal paper? J Chem Ecol 44:805–817. https://doi.org/10.1007/s10886-018-0974-9
Villet MH, Crewe RM, Duncan FD (1991) Evolutionary trends in the reproductive biology of ponerine ants (Hymenoptera: formicidae). J Nat Hist 25(6):1603–1610. https://doi.org/10.1080/00222939100770991
Wetterer JK (2006) Quotation error, citation copying, and ant extinctions in Madeira. Scientometrics 67:351–372. https://doi.org/10.1556/Scient.67.2006.3.2
Wills BD, Moreau CS, Wray BD, Hoffmann BD, Suarez AV (2014) Body size variation and caste ratios in geographically distinct populations of the invasive big-headed ant, Pheidole megacephala. Biol J Lin Soc 113:423–438
Wilson EO (1971) The insect societies. Harvard University Press, Cambridge, Massachusetts, p 548
Acknowledgements
Comments by Tomer Czaczkes, Timothy Linksvayer, and two anonymous reviewers improved the draft manuscript.
Funding
Open access funding provided by CSIRO Library Services.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors state that they have no competing interests.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Hoffmann, B.D., Pettit, M. & Ghodke, A.B. Red imported fire ant Solenopsis invicta buren workers do not have ovaries. Insect. Soc. 71, 43–48 (2024). https://doi.org/10.1007/s00040-024-00951-w
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00040-024-00951-w