Scent of doom improves larvae's vision

Abstract

Crab mums will never win the ‘Best Zoological Parent’ award: as soon as a female releases her young, she's off, leaving the offspring to head for the depths and fend for themselves. Corie Charpentier from the University of Delaware, USA, explains that the minute creatures only ascend to feed under cover of dark, descending again when the sun rises: ‘The daytime depth is set by the lowest light intensity that they can detect’, Charpentier says. These zooplankton are also sensitive to sudden changes in light intensity – dodging deeper to evade detection when a predator's shadow passes over – and the tiny crustaceans seem to become even more sensitive to light changes after sniffing a predator's odour; ‘Crab larvae descend following smaller increases in downwelling light after exposure to predator chemical cues’, explains Charpentier. However, it wasn't clear how the threatening odours, known as kairomones, affected the larvae's vision. ‘Little work has been done to understand how zooplankton integrate these visual and chemical cues to control swimming behaviour’, Charpentier says, so she and her thesis advisor, Jonathan Cohen, set about finding out how the aroma of fear affects crab larval vision.Fortunately, collecting the larvae was as easy as taking egg-laden crab mums-to-be from nearby estuaries and waiting for them to release their offspring. Charpentier and Cohen also decided to investigate two local species with dramatically different larval lifestyles: dwarf crab (Rhithropanopeus harrisii) larvae live in predator-infested estuaries while invasive Asian shore crab (Hemigrapsus sanguineus) larvae are transported offshore to safer waters. Then, the duo gently wiped mucus from the bodies of a local fish, the mummichog, and diluted the goo to produce ‘eau de predator’ before testing its effects on larval vision.Filming the larvae's responses as she simulated 3 s flashes of light filtering down to depths of 9–12 m, Charpentier saw that the lowest light levels that triggered the larvae's defensive descent were 1.1×1013 photons m–2 s–1 for the dwarf crab larvae and 4.77×1012 photons m–2 s–1 for the Asian shore crab larvae. However, when the youngsters had been bathed for up to 3 h in the menacing fish odour, both species became much more sensitive, plunging to safety at intensities that were only a third as bright as the light that had triggered an escape response before they sniffed the odour.But how had the alarming smell affected the larvae's eyes? Charpentier painstakingly measured electrical activity in the retina of larvae as she exposed the animals to increasingly dimmer flashes of light, and found that the retina's light sensitivity increased after bathing in the kairomone stench. And when she tested the effect of the odour on the speed of the retina's response to light, she was surprised that the sensitised larvae responded as fast, and sometimes even faster, than the larvae that had not experienced the kairomone threat. Charpentier explains that this was unexpected as an increase in light sensitivity is usually accompanied by slower visual responses in most animals.Having confirmed that kairomones affect the visual sensitivity of the larvae's retina, Charpentier took a closer look at the structures that comprised the crustacean's compound eye to see whether they had altered, and she was impressed to discover that each eyelet (rhabdom) became wider, increasing the structure's light sensitivity, while the dwarf crab's eye structures also became shorter. Exposure to kairomone odours released by predatory fish was altering the sensitivity of the larvae's eyes to light by directly affecting the eye structure and retina activity to give them a head start when danger looms.