Nature's dark artistry: melanic forms discovered in two Neotropical ant species (Hymenoptera, Formicidae)

ABSTRACT

Here we present melanic forms of ants belonging to the light-colored Neotropical species Heteroponera dolo (Ectatomminae) and Prionopelta punctulata (Amblyoponinae). We also discuss the intraspecific variation regarding body color for both species and provide the dominant colors for the light and dark forms based on the amount of red, blue and green tones generated from the HEX code.

Keywords:
Atlantic Forest; Intraspecific variation; Melanism; Ectatomminae; Amblyoponinae

Melanism describes the occurrence of forms mostly or completely dark in comparison to the typical color patterns of a given species (True, 2003). Melanic forms are common among animals, and the occurrence of intraspecific melanic polymorphism has been important to understand aspects of natural selection, ontogeny and molecular genetics of color (Kettlewell, 1973; Brakefield and Lees, 1987; Majerus, 1998). Under suitable conditions, melanic forms can segregate themselves from conspecifics of typical coloration, ultimately leading to the evolution of new taxa. Having a dark body may be advantageous in cooler habitats or with higher UV-B incidence, and may favor camouflage in obscure understories; given that melanic forms are efficient in absorbing heat (Willmer and Unwin, 1981), incident radiation (Ulbing et al., 2019), and are more prone to be mixed up with the background of dark intricate surfaces (Cheng et al., 2018).

In insects, causes and consequences of melanism were mainly studied in flies, moths and beetles (Wright, 1987; Walter et al., 1991; True et al., 1999; Wittkopp et al., 2002; True, 2003). Among ants, a close relation between body color and thermoregulation has been shown in the community level, with lighter and smaller ants dominating communities in environments with warm conditions versus darker and larger ants more abundant in colder habitats (Parr and Bishop, 2022). Complementarily, Law et al. (2020) suggested that ants inhabiting the canopy and understory strata present darker colors in comparison to individuals inhabiting the ground. Klunk et al. (2022) also found that precipitation and size can be factors correlated with melanism evolution. Differently from the studies focused on color gradients in a community or population scale, the incidence of melanism at the individual level seems to be poorly understood or documented.

Here, we report two melanic forms in colonies of the genera Heteroponera and Prionopelta and provide HEX codes of dominant colors composing the light and dark forms, contributing to the knowledge of intraspecific variation in ectatommine and amblyoponine ants.

According Feitosa (2011), the melanic specimens of Heteroponera examined here belong to H. dolo (Roger, 1860). In total, six workers were examined. Three specimens are deposited at the myrmecological collection of the Centro de Pesquisas do Cacau (CPDC), Ilhéus, Bahia and the other three workers were donated to the Coleção Entomológica Padre Jesus Santiago Moure (DZUP), located at the Universidade Federal do Paraná (UFPR). The complete series of melanic Prionopelta ants was identified as P. punctulata Mayr, 1866 based on Ladino and Feitosa (2020) and includes 19 adult workers. All specimens were obtained within the donation of the Formicidae collection formerly owned by Dr. Jorge L. M. Diniz to the DZUP.

The dark forms of H. dolo have been already mentioned in Feitosa (2011). To confirm the identification of the dark specimens of Prionopelta, we compared them with the diagnostic morphological features that delimitate the Neotropical species of the genus (Ladino and Feitosa 2020).

High resolution images of Heteroponera presented here were taken by Dr. Ricardo Kawada with a Leica M205® coupled to a camera Leica DFC 295®, and stacked with the software Leica Application Suite V3.Ink ® at the Museu de Zoologia da Universidade de São Paulo (MZSP). Prionopelta images were taken with a Zeiss Discovery 20 stereomicroscope coupled to a camera Axiocam 305 color and the software Zen 2.3 at the Laboratório de Sistemática e Biologia de Formigas, UFPR. All photos were stacked in the program CombineZP. Attributes of brightness, contrast and sharpness of the final images were adjusted in Adobe Photoshop CC2014, PhotoShop CS3® (Microsoft) and the plates were elaborated using the Adobe Illustrator 2020. Geographic records for each species were plotted in Quantum GIS 2.18 (QGIS Development Team, 2023). When original coordinates were missing, the center of the most specific locality reported in the label was used to record the precedence of the specimens.

First, the background of each photo was removed in Adobe Photoshop CC2014. Posteriorly, the images were rasterized in Adobe Illustrator 2020 and a color palette up to six dominant colors was generated from them. We reported the HEX code - which represents the amount of red, blue and green – in each color of the palette (Figs. 1, 2). Detailed color descriptions are available online at www.colorhexa.com by consulting each HEX code.

Figure 1
Workers of Heteroponera dolo. A-C. Typical form in full-face, lateral and dorsal views (Brazil: RS: Itati). D-F Dark form in full-face, lateral and dorsal views (Brazil: MG: Viçosa), specimen DZUP556102. The palette below each specimen depicts the values for the HEX code as extracted from www.colorhexa.com.

Figure 2
Worker of Prionopelta punctulata. A-C. Typical form in full-face, lateral and dorsal views (Paraguay: Canindeyú). Modified from AntWeb.org (2023) images by April Nobile, specimen: CASENT0102586. D-F Dark form in full-face, lateral and dorsal views (Brazil: SP: Mirassol), specimen: DZUP553776. The palette below each specimen depicts the values for the HEX code as extracted from www.colorhexa.com.

Heteroponera dolo (Roger, 1860)

Species of Heteroponera are found in the Neotropical and Australian regions. However, the highest richness for the genus is found in Brazil, specifically in the Brazilian Atlantic Forest. Members of this genus are predominantly predators, but occasionally feed on plant exudates. Most species nest on the ground, mainly on rotten logs, and the colonies are relatively small, containing a few dozen individuals (Feitosa and Prada-Achiardi, 2019).

Heteroponera dolo is the most common species of the genus, occurring in wet forests from southern Brazil to northern Argentina. Although coloration in Heteroponera species can vary from black (H. carinifrons Mayr, 1887) to pale yellow (H. flava, Kempf, 1962), intraspecific variations in coloration were unknown until now. Females of H. dolo tend to be entirely yellow (Fig. 1A-C) and the males are black. However, during the exam of specimens deposited in the CPDC, one of us (RMF) found a series of six dark workers collected in 2002 on the soil of a fragment of Atlantic Forest in the municipality of Viçosa, Minas Gerais state. These workers are entirely black, with a golden pubescence on the gaster and iridescent reflects throughout the body, resembling some species of the Australian genus Rhytidoponera (Feitosa, 2011).

At first, it was suspected that the series of melanic workers collected in Viçosa could represent a new species, but, except for the coloration, all the other morphological characters analyzed were entirely compatible with the diagnosis of H. dolo (Feitosa, 2011). Diagnostic characters easily separate Heteroponera dolo from most species of the genus. The closest species is certainly H. robusta Kempf, 1972, from which H. dolo can be quickly separated by its slightly smaller size and smooth and shiny mandibles (striated in H. robusta). Except for the dark series recorded here, no other aberrant forms were recorded for H. dolo or any other species of Heteroponerini (Rodrigo Feitosa, pers. obs).

Prionopelta punctulata Mayr, 1866

In March 12^th, 1972 Diniz and Willian collected a series of Prionopelta ants with a combination of dark and desaturated tones of orange/red and a main grayish color (Fig. 2D-F) at the municipality of Mirassol, São Paulo state (Fig. 3). The specimens are currently hosted at DZUP and, after disregarding the option of being preserved in liquid containing artificial colored substances, it was thought to represent a new Neotropical Prionopelta or a dark variety of an already known species.

Figure 3
Geographic records for P. punctulata and H. dolo. The polygons indicate the occurrence of light (yellow) and dark specimens (black).

Prionopelta species are distributed around the world's tropics. These ants nest and forage in soil and litter, and its morphology suggest cryptobiotic habits that may reflect in depigmented (Wong and Guénard, 2017), yellowish, reddish and brownish bodies as in other lineages of ants with similar habits (Franco and Feitosa, 2018; Pierce et al., 2019; Chaul, 2020). Information about variation on body color are available for several developmental stages of workers (Hölldobler and Wilson, 1986; Ito and Billen, 1998), which established that males are commonly more pigmented than females and that workers tend to be lighter than queens (Ladino and Feitosa, 2020). In fact, variation in color patterns were important in the delimitation of some species in the genus (i.e. P. opaca Emery, 1897 and P. talosOverson and Fisher, 2015). The examination of material worldwide suggest that this attribute should be interpreted carefully in the genus, because color might vary throughout body regions and at an intraspecific level, and no melanic forms were known so far. In the Neotropics, most of the species vary from entirely light yellow (P. minutaLadino and Feitosa, 2020) to red-brown (darker specimens of P. amabilis Borgmeier, 1949), or might present dark patches in several sclerites (some individuals of P. dubiaLadino and Feitosa, 2020). However, pronounced differences in body color as those found here for workers of Neotropical species have never been reported (see Brown, 1960; Ladino and Feitosa, 2020).

Besides the dark body color of the specimens reported here, no morphological feature was markedly different from the Neotropical species already known in the genus. All the melanic forms have eleven antennomeres, excluding the options from eight to three species: Prionopelta menininha Ladino and Feitosa, 2020, Prionopelta punctulata Mayr, 1866 and Prionopelta tapatia Ladino and Feitosa, 2020. The anterior margin of clypeus strongly projected medially, a comparatively shallow sculpturing in the head dorsum, the apically convergent margins of the subpetiolar process and its occurrence in São Paulo lead us to identify the ants as P. punctulata. Prionopelta punctulata include individuals with tones mainly ranging from desaturated orange to brown tones (Fig. 2A-C). Most exemplars are known from litter and soil samples frequently collected in southern areas of Brazil. No other melanic series of P. punctulata or for the remaining Neotropical Prionopelta species have been reported in the literature so far (Natalia Ladino, pers. obs.).

Acknowledgements

Thanks to Dr. Jorge L. M. Diniz for donating Prionopelta exemplars to the DZUP, crucial for the elaboration of this manuscript Also, to MSc. Paloma Andrade for the effort organizing material in the DZUP collection and to MSc. Leonardo Tozetto for handing the melanic forms to N. Ladino.

• Funding
  R. M. Feitosa was supported by CNPq (grant 3014495/2019-0).

References

• AntWeb.org, 2023. AntWeb.org Version 8.86.1. California Academy of Sciences. Available in: https://www.antweb.org (accessed 15 May 2023).
  » https://www.antweb.org
• Brakefield, P., Lees, D., 1987. Melanism in Adalia ladybirds and declining air pollution in Birmingham. Heredity 59 (2), 273-277. http://doi.org/10.1038/hdy.1987.123
  » http://doi.org/10.1038/hdy.1987.123
• Brown, W., 1960. Contributions toward a reclassification of the Formicidae. III. Tribe Amblyoponini (Hymenoptera). Bull. Mus. Comp. Zool. 122, 143-230.
• Chaul, J., 2020. A new species of Discothyrea Roger (Hymenoptera: Formicidae) from the Brazilian Atlantic Rainforest. Bol. Mus. Para. Emílio Goeldi Ciênc. Nat. 15 (1), 199-217. http://doi.org/10.46357/bcnaturais.v15i1.266
  » http://doi.org/10.46357/bcnaturais.v15i1.266
• Cheng, W., Xing, S., Chen, Y., Lin, R., Bonebrake, T. C., Nakamura, A., 2018. Dark butterflies camouflaged from predation in dark tropical forest understories: predation and butterfly wing coloration. Ecol. Entomol. 43 (3), 304-309. http://doi.org/10.1111/een.12499
  » http://doi.org/10.1111/een.12499
• Feitosa, R. M., 2011. Revisão taxonômica e análise filogenética de Heteroponerinae (Hymenoptera, Formicidae). Doctoral Dissertation, Universidade de São Paulo.
• Feitosa, R.M., Prada-Achiardi, F.C., 2019. Subfamilia Ectatomminae. In: Fernández, F., Guerrero, R.J., Delsinne, T. (Eds.). Hormigas de Colombia. Universidad Nacional de Colombia, Bogotá, pp. 659-679.
• Franco, W., Feitosa, R. M., 2018. Discovery of the termite specialist ant genus Centromyrmex, Mayr 1866 (Hymenoptera: Formicidae: Ponerinae) for the Guiana Shield. Sociobiology 65 (2), 345-347. http://doi.org/10.13102/sociobiology.v65i2.2069
  » http://doi.org/10.13102/sociobiology.v65i2.2069
• Hölldobler, B., Wilson, W., 1986. Ecology and behavior of the primitive cryptiobiotic ant Prionopelta amabilis (Hymenoptera: formicidae). Insectes Soc. 33 (1), 45-58. http://doi.org/10.1007/BF02224034
  » http://doi.org/10.1007/BF02224034
• Ito, F., Billen, J., 1998. Larval hemolymph feeding and oophagy: behavior of queen and workers in the primitive ponerine ant Prionopelta kraepelini (Hymenoptera, Formicidae). Belg. J. Zool. 128, 201-210.
• Kettlewell, H. B. D., 1973. The Evolution of Melanism: the Study of a Recurring Necessity. Clarendon Press, Oxford, 423 pp.
• Klunk, C. L., Fratoni, R. O., Rivadeneira, C. D., Schaedler, L. M., Perez, D. M., 2022. Climate and body size have differential roles on melanism evolution across workers in a worldwide ant genus. Oecologia 199 (3), 579-587. http://doi.org/10.1007/s00442-022-05211-x
  » http://doi.org/10.1007/s00442-022-05211-x
• Ladino, N., Feitosa, R. M., 2020. Taxonomic revision of the genus Prionopelta Mayr, 1866 (Formicidae: Amblyoponinae) for the Neotropical region. Zootaxa 4821 (2), 201-249. http://doi.org/10.11646/zootaxa.4821.2.1
  » http://doi.org/10.11646/zootaxa.4821.2.1
• Law, S. J., Bishop, T. R., Eggleton, P., Griffiths, H., Ashton, L., Parr, C., 2020. Darker ants dominate the canopy: testing macroecological hypotheses for patterns in colour along a microclimatic gradient. J. Anim. Ecol. 89 (2), 347-359. http://doi.org/10.1111/1365-2656.13110
  » http://doi.org/10.1111/1365-2656.13110
• Majerus, M. E. N., 1998. Melanism: evolution in action. Oxford University Press, Oxford. http://doi.org/10.1093/oso/9780198549833.001.0001
  » http://doi.org/10.1093/oso/9780198549833.001.0001
• Overson, R., Fisher, B., 2015. Taxonomic revision of the genus Prionopelta (Hymenoptera, Formicidae) in the Malagasy region. ZooKeys 507, 115-150. http://doi.org/10.3897/zookeys.507.9303
  » http://doi.org/10.3897/zookeys.507.9303
• Parr, C. L., Bishop, T. R., 2022. The response of ants to climate change. Glob. Change Biol. 28 (10), 3188-3205. http://doi.org/10.1111/gcb.16140
  » http://doi.org/10.1111/gcb.16140
• Pierce, M. P., Leong, C. M., Guénard, B., 2019. A new species and new record of the cryptobiotic ant genus Ponera Latreille, 1804 (Hymenoptera, Formicidae) from Hong Kong. ZooKeys 867, 9-21. http://doi.org/10.3897/zookeys.867.36139
  » http://doi.org/10.3897/zookeys.867.36139
• QGIS Development Team, 2023. QGIS Geographic Information System. QGIS Association. Available in: http://www.qgis.org (accessed 15 May 2023).
  » http://www.qgis.org
• True, J. R., Edwards, K. A., Yamamoto, D., Carroll, S. B., 1999. Drosophila wing melanin patterns form by vein-dependent elaboration of enzymatic prepatterns. Curr. Biol. 9 (23), 1382-1391. http://doi.org/10.1016/S0960-9822(00)80083-4
  » http://doi.org/10.1016/S0960-9822(00)80083-4
• True, J. R., 2003. Insect melanism: the molecules matter. Trends Ecol. Evol. 18 (12), 640-647. http://doi.org/10.1016/j.tree.2003.09.006
  » http://doi.org/10.1016/j.tree.2003.09.006
• Ulbing, C. K., Muuse, J. M., Miner, B. E., 2019. Melanism protects alpine zooplankton from DNA damage caused by ultraviolet radiation. Proc. Biol. Sci. 286 (1914), 20192075. http://doi.org/10.1098/rspb.2019.2075
  » http://doi.org/10.1098/rspb.2019.2075
• Walter, M. F., Black, B. C., Afshar, G., Kermabon, A. Y., Wright, T. R., Biessmann, H., 1991. Temporal and spatial expression of the yellow gene in correlation with cuticle formation and dopa decarboxylase activity in Drosophila development. Dev. Biol. 147 (1), 32-45. http://doi.org/10.1016/S0012-1606(05)80005-3
  » http://doi.org/10.1016/S0012-1606(05)80005-3
• Willmer, P. G., Unwin, D. M., 1981. Field analysis of insect heat budgets: reflectance, size and heating rates. Oecologia 50 (2), 250-255. http://doi.org/10.1007/BF00348047
  » http://doi.org/10.1007/BF00348047
• Wittkopp, P. J., Vaccaro, K., Carroll, S. B., 2002. Evolution of yellow gene regulation and pigmentation in Drosophila. Curr. Biol. 12 (18), 1547-1556. http://doi.org/10.1016/S0960-9822(02)01113-2
  » http://doi.org/10.1016/S0960-9822(02)01113-2
• Wong, M. K. L., Guénard, B., 2017. Subterranean ants: summary and perspectives on field sampling methods, with notes on diversity and ecology (Hymenoptera: Formicidae). Myrmecol. News 25, 1-16. http://doi.org/10.25849/myrmecol.news_025:001
  » http://doi.org/10.25849/myrmecol.news_025:001
• Wright, T. R., 1987. The genetics of biogenic amine metabolism, sclerotization, and melanization in Drosophila melanogaster. Adv. Genet. 24, 127-222. http://doi.org/10.1016/S0065-2660(08)60008-5
  » http://doi.org/10.1016/S0065-2660(08)60008-5

Edited by

• Associate Editor:
  Tathiana Sobrinho

Publication Dates

• Publication in this collection
  11 Nov 2024
• Date of issue
  2024

History

• Received
  03 June 2024
• Accepted
  01 Oct 2024