Skip to main content
Springer Nature Link
Log in

The visual system of male scale insects

  • Original Paper
  • Published:
Naturwissenschaften Aims and scope Submit manuscript

Abstract

Animal eyes generally fall into two categories: (1) their photoreceptive array is convex, as is typical for camera eyes, including the human eye, or (2) their photoreceptive array is concave, as is typical for the compound eye of insects. There are a few rare examples of the latter eye type having secondarily evolved into the former one. When viewed in a phylogenetic framework, the head morphology of a variety of male scale insects suggests that this group could be one such example. In the Margarodidae (Hemiptera, Coccoidea), males have been described as having compound eyes, while males of some more derived groups only have two single-chamber eyes on each side of the head. Those eyes are situated in the place occupied by the compound eye of other insects. Since male scale insects tend to be rare, little is known about how their visual systems are organized, and what anatomical traits are associated with this evolutionary transition. In adult male Margarodidae, one single-chamber eye (stemmateran ocellus) is present in addition to a compound eye-like region. Our histological investigation reveals that the stemmateran ocellus has an extended retina which is formed by concrete clusters of receptor cells that connect to its own first-order neuropil. In addition, we find that the ommatidia of the compound eyes also share several anatomical characteristics with simple camera eyes. These include shallow units with extended retinas, each of which is connected by its own small nerve to the lamina. These anatomical changes suggest that the margarodid compound eye represents a transitional form to the giant unicornal eyes that have been described in more derived species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Explore related subjects

Discover the latest articles, books and news in related subjects, suggested using machine learning.

References

  • Berry RP, Stange G, Warrant EJ (2007a) Form vision in the insect dorsal ocelli: an anatomical and optical analysis of the dragonfly median ocellus. Vision Res 47(10):1394–1409 doi:10.1016/j.visres.2007.01.019

    Article  PubMed  Google Scholar 

  • Berry RP, Warrant EJ, Stange G (2007b) Form vision in the insect dorsal ocelli: an anatomical and optical analysis of the Locust Ocelli. Vision Res 47(10):1382–1393 doi:10.1016/j.visres.2007.01.020

    Article  PubMed  Google Scholar 

  • Buschbeck EK, Friedrich M (2008) Evolution of insect eyes: tales of ancient heritage, deconstruction, reconstruction, remodeling, and recycling. Evol Edu Outreach. doi:10.1007/s12052-008-0086-z

  • Buschbeck E, Ehmer B, Hoy R (1999) Chunk versus point sampling: visual imaging in a small insect. Science 286(5442):1178–1180

    Article  PubMed  CAS  Google Scholar 

  • Buschbeck EK, Ehmer B, Hoy RR (2003) The unusual visual system of the Strepsiptera: external eye and neuropils. J Comp Phys A 189(8):617–630

    Article  CAS  Google Scholar 

  • Cook LG, Gullan PJ, Trueman HE (2002) A preliminary phylogeny of the scale insects (Hemiptera: Sternorrhyncha: Coccoidea) based on nuclear small-subunit ribosomal DNA. Mol Phylogenet Evol 25(1):43–52

    Article  PubMed  CAS  Google Scholar 

  • Davenport HA, Windle WF, Buch RH (1934) Block staining of nervous tissue. IV. Embryos. Stain Technol 29:165–173

    Google Scholar 

  • Duelli P (1978) An insect retina without microvilli in the male scale insect, Eriococcus sp. (Eriococcidae, Homoptera). Cell Tissue Res 187:417–427

    Article  PubMed  CAS  Google Scholar 

  • Duelli P (1985) A new functional interpretation of the visual system of male scale insects (Coccida, Homoptera). Experientia 41(8):1036–1036

    Article  Google Scholar 

  • Egelhaaf A, Altenfeld H, Hoffmann HU (1988) Evidence for the priming role of the central retinula cell in ommatidium differentiation of Ephestia kuehniella. Roux Arch Dev Biol 197(3):184–189

    Article  Google Scholar 

  • Friedrich M (2003) Evolution of insect eye development: first insights from fruit fly, grasshopper and flour beetle. Integr Comp Biol 43(4):508–521

    Article  Google Scholar 

  • Friedrich M (2006) Ancient mechanisms of visual sense organ development based on comparison of the gene networks controlling larval eye, ocellus, and compound eye specification in Drosophila. Arthropod Struct Dev 35(4):357–378

    Article  PubMed  Google Scholar 

  • Friedrich M, Dong Y, Jackowska M (2006) Insect interordinal relationships: evidence from the visual system. Arthropod Syst Phylogeny 62(2):133–148

    Google Scholar 

  • Goodman LJ (1981) Organization and physiology of the insect dorsal ocellar system. In: Autrum H (ed) Handbook of sensory physiology. Springer, Berlin, pp 201–286

    Google Scholar 

  • Gullan PJ, Cook LG (2007) Phylogeny and higher classification of the scale insects (Hemiptera: Sternorrhyncha: Coccoidea). Zootaxa (1668):413–425

  • Gullan PJ, Kosztarab M (1997) Adaptations in scale insects. Annu Review Entomol 42:23–50

    Article  CAS  Google Scholar 

  • Hodgson CJ, Foldi I (2006) A review of the Margarodidae sensu Morrison (Hemiptera : Coccoidea) and some related taxa based on the morphology of adult males. Zootaxa (1263):1–250

  • Hodgson CJ, Henderson RC (2004) Coccidae (Insecta: Hemiptera: Coccoidea): adult males, pupae and prepupae of indigenous species. Fauna of New Zealand 51:1–228

    Google Scholar 

  • Kring JB (1977) Structure of the eyes of the pea aphid, Acyrthosiphon pisum. Ann Entomol Soc Am 70:855–860

    Google Scholar 

  • Labhart T, Meyer EP (1999) Detectors for polarized skylight in insects: a survey of ommatidial specializations in the dorsal rim area of the compound eye. Microsc Res Tech 47(6):368–379

    Article  PubMed  CAS  Google Scholar 

  • Land MF, Nilsson DE (2002) Animal eyes. Oxford University Press, Oxford

    Google Scholar 

  • Land MF, Gibson G, Horwood J, Zeil J (1999) Fundamental differences in the optical structure of the eyes of nocturnal and diurnal mosquitoes. J Comp Physiol A 185(1):91–103

    Article  Google Scholar 

  • Liu ZY, Friedrich M (2004) The Tribolium homologue of glass and the evolution of insect larval eyes. Dev Biol 269(1):36–54

    Article  PubMed  CAS  Google Scholar 

  • Liu ZY, Yang XY, Dong Y, Friedrich M (2006) Tracking down the “head blob”: comparative analysis of wingless expression in the developing insect procephalon reveals progressive reduction of embryonic visual system patterning in higher insects. Arthropod Struct Dev 35(4):341–356

    Article  PubMed  Google Scholar 

  • Maksimovic S, Layne JE, Buschbeck EK (2007) Behavioral evidence for within-eyelet resolution in twisted-winged insects (Strepsiptera). J Exp Biol 210(16):2819–2828

    Article  PubMed  Google Scholar 

  • Nilsson DE, Modlin RF (1994) A mysid shrimp carrying a pair of binoculars. J Exp Biol 189:213–236

    PubMed  Google Scholar 

  • Normark BB (2004) The strange case of the armored scale insect and its bacteriome. Plos Biology 2(3):298–301

    Article  CAS  Google Scholar 

  • Paulus HF (1979) Eye structure and the monophyly of the Arthropoda. In: Gupta AP (ed) Arthropod phylogeny. Van Nostrad Reinhold, New York, pp 299–384

    Google Scholar 

  • Paulus HF (2000) Phylogeny of the Myriapoda–Crustacea–Insecta: a new attempt using photoreceptor structure. J Zool Syst Evol Res 38(3):189–208

    Article  Google Scholar 

  • Pflugfelder O (1936) Bau und morphologische Bedeutung der sogenannten Ozellen der Schildlausmännchen. Zool Anz 114:49–55

    Google Scholar 

  • Presburg M, Kumps C, De Vos L (2002) Submicroscopic anatomy of photoreceptors in the female scale insect Eupulvinaria hydrangeae (Homopteres, Coccidae). J Submicrosc Cytol Pathol 34(1):9–16

    PubMed  CAS  Google Scholar 

  • Sbita SJ, Morgan RC, Buschbeck EK (2007) Eye and optic lobe metamorphosis in the sunburst diving beetle, Thermonectus marmoratus (Coleoptera: Dytiscidae). Arthropod Struct Dev 36(4):449–462

    Article  PubMed  Google Scholar 

  • Srivastava WS, Sinha PK (1966) The eyes of Centrococcus insolitus (Coccoidea). The Entomologist 99:261–268

    Google Scholar 

  • Stange G (1981) The ocellar component of flight equilibrium control in dragonflies. J Comp Physiol A 141(3):335–347

    Article  Google Scholar 

  • Stange G, Stowe S, Chahl JS, Massaro A (2002) Anisotropic imaging in the dragonfly median ocellus: a matched filter for horizon detection. J Comp Physiol A 188(6):455–467

    Article  CAS  Google Scholar 

  • Strausfeld NJ (1976) Atlas of an insect brain. Springer, New York

    Google Scholar 

  • Strausfeld NJ, Lee JK (1991) Neuronal basis for parallel visual processing in the fly. Visual Neurosci 7(1–2):13–33

    Article  CAS  Google Scholar 

  • Strausfeld NJ, Seyan HS (1985) Convergence of visual, haltere, and prosternal inputs at neck motor neurons of Calliphora erythrocephala. Cell Tissue Res 247:5–10

    Article  Google Scholar 

  • Theron JG (1958) Comparative studies on the morphology of male scale insects (Hemiptera: Coccoidea). Annals of the University of Stellenbosch 34(Sect. A, No.1):1–71

    Google Scholar 

  • Warrant E (2006) Invertebrate vision in dim light. In: Warrant E, Nilsson DE (eds) Invertebrate vision. Cambridge University Press, Cambridge, pp 83–126

    Google Scholar 

Download references

Acknowledgments

We thank Dr. P.J. Gullan (University of California, Davis, CA, USA), and Dr. G. Watson (California Department of Food and Agriculture, Sacramento, CA, USA) for their help and expertise in identifying and providing material. We also thank P. Tripotin (Rouen, France) for making material available from his intensive collecting effort in South Korea, I. Vilinsky for helpful discussions, and Suzanne Murray for editing this manuscript. The comments of three anonymous reviewers greatly improved this document. This work has been supported by the NSF (IOB-0545978).

Author information

Authors and Affiliations

  1. Department of Biological Sciences, University of Cincinnati, Cincinnati, OH, 45221-0006, USA

    Elke K. Buschbeck

  2. Plant Pest Diagnostics Branch, California Department of Food & Agriculture, 3294 Meadowview Road, Sacramento, CA, 95832-1448, USA

    Martin Hauser

Authors
  1. Elke K. Buschbeck
    View author publications

    Search author on:PubMed Google Scholar

  2. Martin Hauser
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Elke K. Buschbeck.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Buschbeck, E.K., Hauser, M. The visual system of male scale insects. Naturwissenschaften 96, 365–374 (2009). https://doi.org/10.1007/s00114-008-0484-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00114-008-0484-7

Keywords