Skip to main content
SpringerLink
Log in

Optic lobe organization in stomatopod crustacean species possessing different degrees of retinal complexity

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

Stomatopod crustaceans possess tripartite compound eyes; upper and lower hemispheres are separated by an equatorial midband of several ommatidial rows. The organization of stomatopod retinas is well established, but their optic lobes have been studied less. We used histological staining, immunolabeling, and fluorescent tracer injections to compare optic lobes in two 6-row midband species, Neogonodactylus oerstedii and Pseudosquilla ciliata, to those in two 2-row midband species, Squilla empusa and Alima pacifica. Compared to the 6-row species, we found structural differences in all optic neuropils in both 2-row species. Photoreceptor axons from 2-row midband ommatidia supply two sets of lamina cartridges; however, conspicuous spaces lacking lamina cartridges are observed in locations corresponding to where the cartridges of the upper four ommatidial rows of 6-row species would exist. The tripartite arrangement and enlarged projections containing fibers associated with the two rows of midband ommatidia can be traced throughout the entire optic lobe. However, 2-row species lack some features of medullar and lobular neuropils in 6-row species. Our results support the hypothesis that 2-row midband species are derived from a 6-row ancestor, and suggest specializations in the medulla and lobula found solely in 6-row species are important for color and polarization analysis.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

(photograph in b, courtesy of Michael Bok)

Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Ahyong ST (2001) A revision of the Australian stomatopod crustacea. Rec Aust Mus Suppl 26:1–326

    Article  Google Scholar 

  • Ahyong ST, Harling C (2000) The phylogeny of the stomatopod Crustacea. Aust J Zool 48:607–642

    Article  Google Scholar 

  • Ahyong ST, Jarman SN (2009) Stomatopod interrelationships: preliminary results based on analysis of three molecular loci. Arthropod Syst Phylogeny 67:91–98

    Google Scholar 

  • Bodian D (1936) A new method for staining nerve fibers and nerve endings in mounted paraffin sections. Anat Rec 65:89–97

    Article  Google Scholar 

  • Bok MJ, Porter ML, Cronin TW (2015) Ultraviolet filters in stomatopod crustaceans: diversity, ecology and evolution. J Exp Biol 218:2055–2066

    Article  PubMed  Google Scholar 

  • Chiou TH, Kleinlogel S, Cronin T, Caldwell R, Loeffler B, Siddiqi A, Goldizen A, Marshall J (2008) Circular polarization vision in a stomatopod crustacean. Curr Biol 18:429–434

    Article  CAS  PubMed  Google Scholar 

  • Cronin TW (1985) The visual pigment of a stomatopod crustacean, Squilla empusa. J Comp Physiol A 156:679–687

    Article  CAS  Google Scholar 

  • Cronin TW (1986) Optical design and evolutionary adaptation in crustacean compound eyes. J Crust Biol 6:1–23

    Article  Google Scholar 

  • Cronin TW, Marshall NJ (1989a) Multiple spectral classes of photoreceptors in the retinas of gonodactyloid stomatopod crustaceans. J Comp Physiol A 166:261–275

    Article  Google Scholar 

  • Cronin TW, Marshall NJ (1989b) A retina with at least ten spectral types of photoreceptors in a stomatopod crustacean. Nature 339:137–140

    Article  Google Scholar 

  • Cronin TW, Marshall J (2004) The unique visual world of mantis shrimps. In: Prete F (ed) Complex worlds from simpler nervous systems. MIT, Cambridge, pp 239–268

    Google Scholar 

  • Cronin TW, Nair J, Doyle RD, Caldwell RL (1988) Ocular tracking of rapidly moving targets by stomatopod crustaceans. J Exp Biol 138:135–179

    Google Scholar 

  • Cronin TW, Marshall NJ, Caldwell RL (1993) Photoreceptor spectral diversity in the retinas of squilloid and lysiosquilloid stomatopod crustaceans. J Comp Physiol A 172:339–350

    Article  Google Scholar 

  • Cronin TW, Marshall NJ, Quinn CA, King CA (1994) Ultraviolet photoreception in mantis shrimp. Vis Res 34:1443–1449

    Article  CAS  PubMed  Google Scholar 

  • Cronin TW, Marshall NJ, Caldwell RL (1996) Visual pigment diversity in two genera of mantis shrimps implies rapid evolution. J Comp Physiol A 179:371–384

    Article  Google Scholar 

  • Cronin TW, Shashar N, Caldwell RL, Marshall J, Cheroske AG, Chiou TH (2003) Polarization vision and its role in biological signaling. Integr Comp Biol 43:549–558

    Article  PubMed  Google Scholar 

  • Cronin TW, Bok MJ, Marshall NJ, Caldwell RL (2014) Filtering and polychromatic vision in mantis shrimps: themes in visible and ultraviolet vision. Philos Trans R Soc B 369:20130032

    Article  Google Scholar 

  • Cronin TW, Bok MJ, Lin C (2017) Crustacean larvae—vision in the plankton. Integr Comp Biol 57:1139–1150

    Article  CAS  PubMed  Google Scholar 

  • Exner S (1891) Die Physiologie der facettirten Augen von Krebsen und Insekten. Deuticke, Leipzig

    Book  Google Scholar 

  • Harling C (2000) Reexamination of eye design in the classification of stomatopod crustaceans. J Crust Biol 20:172–185

    Article  Google Scholar 

  • Horridge GA (1978) The separation of visual axes in apposition compound eyes. Philos Trans R Soc B 285:1–59

    CAS  Google Scholar 

  • Kleinlogel S, Marshall NJ (2005) Photoreceptor projection and termination pattern in the lamina of gonodactyloid stomatopods (mantis shrimp). Cell Tissue Res 321:273–284

    Article  CAS  PubMed  Google Scholar 

  • Kleinlogel S, Marshall NJ (2006) Electrophysiological evidence for linear polarization sensitivity in the compound eyes of the stomatopod crustacean Gonodactylus chiragra. J Exp Biol 209:4262–4272

    Article  PubMed  Google Scholar 

  • Kleinlogel S, Marshall NJ, Horwood JM, Land MF (2003) Neuroarchitecture of the color and polarization vision system of the stomatopod Haptosquilla. J Comp Neurol 467:326–342

    Article  PubMed  Google Scholar 

  • Lin C, Cronin TW (2018) Two visual systems in one eyestalk: the unusual optic lobe metamorphosis in the stomatopod Alima pacifica. Dev Neurobiol 78:3–14

    Article  CAS  PubMed  Google Scholar 

  • Lin C, Strausfeld NJ (2012) Visual inputs to the mushroom body calyces of the whirligig beetle Dineutus sublineatus: modality switching in an insect. J Comp Neurol 520:2562–2574

    Article  PubMed  Google Scholar 

  • Manning RB (1969) Stomatopod Crustacea of the Western Atlantic. University of Miami Press, Coral Gables

    Google Scholar 

  • Manning RB, Schiff H, Abbott BC (1984) Eye structure and the classification of stomatopod Crustacea. Zool Scripta 13:41–44

    Article  Google Scholar 

  • Marshall NJ (1988) A unique colour and polarization vision system in mantis shrimps. Nature 333:557–560

    Article  CAS  PubMed  Google Scholar 

  • Marshall NJ, Land MF (1993a) Some optical features of the eyes of stomatopods. I. eye shape, optical axes and resolution. J Comp Physiol A 173:565–582

    Article  Google Scholar 

  • Marshall NJ, Land MF (1993b) Some optical features of the eyes of stomatopods. II. Ommatidial design, sensitivity and habitat. J Comp Physiol A 173:583–594

    Article  Google Scholar 

  • Marshall J, Oberwinkler J (1999) The colourful world of the mantis shrimp. Nature 401:873–874

    Article  CAS  PubMed  Google Scholar 

  • Marshall NJ, Land MF, King CA, Cronin TW (1991a) The compound eyes of mantis shrimps (Crustacea, Hoplocarida, Stomatopoda). I. Compound eye structure: the detection of polarized light. Philos Trans R Soc B 334:33–56

    Article  Google Scholar 

  • Marshall NJ, Land MF, King CA, Cronin TW (1991b) The compound eyes of mantis shrimps (Crustacea, Hoplocarida, Stomatopoda). II. Colour pigments in the eyes of stomatopod crustaceans: polychromatic vision by serial and lateral filtering. Philos Trans R Soc B 334:57–84

    Article  Google Scholar 

  • Marshall NJ, Jones JP, Cronin TW (1996) Behavioural evidence for colour vision in stomatopod crustaceans. J Comp Physiol A 179:473–481

    Article  Google Scholar 

  • Marshall J, Cronin TW, Shashar N, Land M (1999) Behavioural evidence for polarisation vision in stomatopods reveals a potential channel for communication. Curr Biol 9:755–758

    Article  CAS  PubMed  Google Scholar 

  • Marshall J, Cronin TW, Kleinlogel S (2007) Stomatopod eye structure and function: a review. Arthropod Struct Dev 36:420–448

    Article  PubMed  Google Scholar 

  • Porter ML, Bok MJ, Robinson PR, Cronin TW (2009) Molecular diversity of visual pigments in Stomatopoda (Crustacea). Vis Neurosci 26:255–266

    Article  PubMed  Google Scholar 

  • Porter ML, Zhang Y, Desai S, Caldwell RL, Cronin TW (2010) Evolution of anatomical and physiological specialization in the compound eyes of stomatopod crustaceans. J Exp Biol 213:3473–3486

    Article  CAS  PubMed  Google Scholar 

  • Porter ML, Speiser DI, Zaharoff AK, Caldwell RL, Cronin TW, Oakley TH (2013) The evolution of complexity in the visual systems of stomatopods: insights from transcriptomics. Integr Comp Biol 53:39–49

    Article  CAS  PubMed  Google Scholar 

  • Porter ML, Awata H, Bok MJ, Cronin TW (2019) Exceptional diversity of opsin expression patterns in Neogonodactylus oerstedii (Stomatopoda) retinas. Proc Natl Acad Sci (in press)

  • Roberts NW, Chiou T-S, Marshall NJ, Cronin TW (2009) A biological quarter-wave retarder with excellent achromaticity in the visible wavelength region. Nat Photon 11:641–644

    Article  CAS  Google Scholar 

  • Schiff H (1963) Dim light vision of Squilla mantis. Am J Physiol 205:927–940

    Article  CAS  PubMed  Google Scholar 

  • Schönenberger N (1977) The fine structure of the compound eye of Squilla mantis (Crustacea, Stomatopoda). Cell Tissue Res 176:205–233

    Article  PubMed  Google Scholar 

  • Strausfeld NJ (2005) The evolution of crustacean and insect optic lobes and the origins of chiasmata. Arthropod Struct Dev 34:235–256

    Article  Google Scholar 

  • Strausfeld NJ, Nässel DR (1981) Neuroarchitectures serving compound eyes of Crustacea and insects. In: Autrum H (ed) Comparative physiology and evolution of vision in invertebrates. Handbook of sensory physiology, vol VII/6B. Springer, Berlin, pp 1–132

    Google Scholar 

  • Strausfeld NJ, Ma X, Edgecombe GD, Fortey RA, Land MF, Liu Y, Cong P, Hou X (2016) Arthropod eyes: the early Cambrian fossil record and divergent evolution of visual systems. Arthropod Struct Dev 45:152–172

    Article  PubMed  Google Scholar 

  • Sztarker J, Strausfeld NJ, Tomsic D (2005) Organization of optic lobes that support motion detection in a semiterrestrial crab. J Comp Neurol 493:396–411

    Article  PubMed  PubMed Central  Google Scholar 

  • Thoen HH, How MJ, Chiou TH, Marshall J (2014) A different form of color vision in mantis shrimp. Science 343:411–413

    Article  CAS  PubMed  Google Scholar 

  • Thoen HH, Strausfeld NJ, Marshall J (2017) Neural organization of afferent pathways from the stomatopod compound eye. J Comp Neurol 525:3010–3030

    Article  CAS  PubMed  Google Scholar 

  • Thoen HH, Sayre ME, Marshall J, Strausfeld NJ (2018) Representation of the stomatopod’s retinal midband in the optic lobes: putative neural substrates for integrating chromatic, achromatic and polarization information. J Comp Neurol 526:1148–1165

    Article  CAS  PubMed  Google Scholar 

  • Valdez-Lopez JC, Donohue MW, Bok MJ, Wolf J, Cronin TW, Porter ML (2018) Sequence, structure, and expression of opsins in the monochromatic stomatopod Squilla empusa. Integr Comp Biol 58:386–397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wortham JL (2009) Abundance and distribution of two species of Squilla (Crustacea: Stomatopoda: Squillidae) in the northern Gulf of Mexico. Gulf Caribbean Res 21:1–12

    Article  Google Scholar 

Download references

Acknowledgements

We thank Tagide deCarvalho and the UMBC Keith Porter Imaging Facility for much assistance with the confocal imaging. We are grateful to Michael Bok for the image used in Fig. 1b. This work was supported by the Air Force Office of Scientific Research under Grant number FA9550-18-1-0278. All applicable institutional guidelines for the care and use of animals were followed.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, University of Maryland Baltimore County, Baltimore, MD, 21250, USA

    Chan Lin, Alice Chou & Thomas W. Cronin

  2. Department of Invertebrate Zoology, Smithsonian National Museum of Natural History, Washington, DC, 20560, USA

    Chan Lin

Authors
  1. Chan Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alice Chou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thomas W. Cronin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Thomas W. Cronin.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to declare.

Additional information

Publisher's Note

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

Supporting Grant: Air Force Office of Scientific Research (FA9550-18-1-0278).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lin, C., Chou, A. & Cronin, T.W. Optic lobe organization in stomatopod crustacean species possessing different degrees of retinal complexity. J Comp Physiol A 206, 247–258 (2020). https://doi.org/10.1007/s00359-019-01387-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-019-01387-5

Keywords

Search

Navigation