Multiple spectral channels in branchiopods. II. Role in light-dependent behavior and natural light environments

Abstract

Light is a primary environmental factor used by aquatic invertebrates for depth selection behavior. Many branchiopod crustaceans live in ephemeral aquatic habitats. All branchiopod crustaceans studied to date express four or more visual opsins in their compound eyes. We asked whether two branchiopods, and, use multiple spectral channels to regulate their position in the water column. At the lowest intensities that elicited photonegative behavior, both species had broad spectral bandwidths, suggesting they use multiple spectral photoreceptor classes. Male were more likely to maintain a vertical position 8.0-12.0 cm below the surface than females, independently of whether females were present. Male photopositive behavior at low intensity was restricted to a narrow bandwidth centered at 532 nm, suggesting a single photoreceptor class is used to maintain position above females. We compared ephemeral pools from two regions in Arizona and found that diffuse light attenuation coefficients were two orders of magnitude greater than the most heavily attenuating coastal waters. At less than 1 m of depth, pools were often dimmer than terrestrial habitats under starlight. Soil particle size distribution in each region affected spectral light environments, and behavioral responses of field-caught shrimp were adapted to the spectral properties of their region. The results suggest that branchiopods predominantly use luminance vision summed from multiple spectral photoreceptor classes for depth selection in dim, spectrally variable environments. The neuroanatomical basis for summation is described in a companion paper.

Multiple spectral channels in branchiopods. I. Vision in dim light and neural correlates

“…Our evidence suggests that the four spectral photoreceptor classes in the branchiopod compound eyes are predominantly used for luminance detection in environments that are often dim and spectrally variable. As reported in Lessios et al (2018), ephemeral desert pool habitats can have ambient intensities lower than those of terrestrial habitats in dim starlight at depths of less than 1 m. Further, that work shows these desert pools often have high levels of suspended sediment that affect the spectral quality of downwelling irradiance. Branchiopods possess apposition eyes in which each ommatidium is optically isolated with its own dioptric apparatus Odselius, 1981, 1983) and photoreceptor rhabdomeres fused to form a single light guide.…”

“…Our models predict that the minimum intensity to elicit a response above photon shot noise (I min ) in branchiopod compound eyes without spatial summation (7.3±0.23 log photons cm −2 s −1 ) is over one order of magnitude higher than that from compound eyes that incorporate spatial summation from branching short visual fibers and lamina monopolar neurons (6.3±0.29 log photons cm −2 s −1 ). In Lessios et al (2018), we show that T. longicaudatus and S. mackini respond behaviorally within an intensity range of approximately one order of magnitude of the responses we have modeled for their compound eyes. Based on these estimates, we predict that spatial summation from multiple compound eye ommatidia could be responsible for vision in dim light, as the compound eyes would be likely to generate reliable signal above photon shot noise at these intensities.…”

“…We suggest that peak sensitivities of photoreceptor class λmax3 at 528 nm (Table 1, Fig. 1D) may be used for wavelength-specific behavior at 532 nm as reported in Lessios et al (2018). Our absorptance modeling, which is based on the spectral sensitivities reported in Fig.…”

“…(D) S. mackini males. The vertical dashed line indicates the wavelength at which behavioral assays found positive movement towards a light source reported in a companion paper (Lessios et al, 2018). (E) S. mackini females.…”

“…Candidates for spatial summation take into account measurements of lateral processes extending amongst retinal terminals in the lamina that allow predictions as to whether branchiopod compound eyes provide sufficient intensity discrimination for simple visual behaviors in dim environments. To demonstrate how the expressed opsins might contribute to spectral sensitivity and dim light vision, a companion paper (Lessios et al, 2018) reports how multiple spectral channels in S. mackini and T. longicaudatus support behavior at light intensities typical of their natural light environments.…”