Cone Photoreceptor Diversity in the Retinas of Fruit Bats (Megachiroptera)

Abstract

Older studies have claimed that bats including the Megachiroptera (fruit bats or flying foxes) have pure-rod retinas and possess no cone photoreceptors. We have determined the presence and the population densities of spectral cone types in six megachiropteran species belonging to four genera: Pteropus rufus, P. niger, P. rodricensis, Rousettus madagascariensis, Eidolon dupreanum, and Epomophorus gambianus. Spectral cone types and rods were assessed immunocytochemically with opsin-specific antibodies. All six species have rod-dominated retinas but possess significant cone populations. The high rod densities (range 350,000–800,000/mm², depending on species and retinal location) provide good scotopic sensitivity in these predominantly nocturnal animals. With the cones (density range 1,300–11,000/mm², corresponding to 0.25–0.6% of the photoreceptors, depending on species and retinal location) the retinas also possess the prerequisite for vision at photopic light levels. The three Pteropus species have two spectral cone types, a majority of middle-to-long-wave sensitive (L-) cones, and a minority of short-wave sensitive (S-) cones, indicating the potential for dichromatic color vision. This conforms to the pattern found in most mammals. In contrast, Rousettus, Eidolon and Epomophorus have L-cones but completely lack S-cones, indicating cone monochromacy and color blindness. The discussion relates these findings to the visual behavior of fruit bats.

Behavioral evidence for cone-based ultraviolet vision in divergent bat species and implications for its evolution

“…Among Old World fruit bats (Yinpterochiroptera) roosting in caves with low-ambient light, UV vision should be lost, but not in treeroosting species. Based on the coevolved theory of vision and hearing of bats (SPEAKMAN 2001, ZHAO et al 2009), the possible evolutionary sensory tradeoffs between shortwave vision and echolocation and changes in roosting ecology are consistent with the results of examination of S opsin among 28 species of bats from these four lineages using immunohistochemistry (MULLER & PEICHL 2005, 2006, MULLER et al 2007, KIM et al 2008, FELLER et al 2009), though the exact spectral tuning of S opsin cannot be directly established. Recently, MULLER et al (2009) (NEI et al 1997) and/ or endocrine modulation (BRAINARD et al 1994).…”

“…This indicates that loss of UV vision may be correlated with roosting ecology, i.e., different levels of ambient light. Tree-roosting species at exposed daytime roosts appear to require UV vision to aid their visual discrimination for predator surveillance (MULLER et al 2007) while cave-roosting species may not require color discrimination and experience a relaxation in selective constraint of the S opsin gene, ultimately resulting in loss of UV vision (ZHAO et al 2009).…”

“…Recently, MULLER et al (2009) (NEI et al 1997) and/ or endocrine modulation (BRAINARD et al 1994). Previous studies have only inferred that bats have the prerequisites for cone-based UV vision (MULLER et al 2007(MULLER et al , 2009) and no study has tested this capacity in the order Chiroptera. The search for UV vision in mammals has so far focused mainly on specialized cone types.…”

“…Because their retinas typically contain only a relatively small population of cones (ca 3% in bats with laryngeal echolocation, even less than 0.5% in Old World fruit bats, MULLER & PEICHL 2005, 2006, MULLER et al 2007, KIM et al 2008, it is difficult to study the nature of cone-based vision in nocturnal mammals (JACOBS et al 2001). Following methods used for the demonstration of possible cone-based pathways (JACOBS et al 1991, AMIR & ROBINSON 1996, JACOBS et al 2001, ARRESE et al 2006, PALACIOS et al 2010, only behavioral studies can confirm proposed UV vision (JACOBS 1993, GRIEBEL & PEICHL 2003.…”

“…This method could enlarge the neutral stimulus and has been successfully used in numerous species (from snails to humans, SANGHA et al 2003, KINDT et al 2009). Here we modified fear conditioning procedures to elucidate the bats' capacity for cone-based UV vision, since it is now well established that bats have functional visual systems and the corresponding anatomical evidence shows that both their cornea and lens can transmit UV light (MULLER et al 2007(MULLER et al , 2009). Our experiment was carried out under light conditions to avoid possible rod interference.…”