Ak Clarke

Synchronized Circadian Bioluminescence in Cave-Dwelling Arachnocampa tasmaniensis (Glowworms)

Larvae of the genus Arachnocampa, known as glowworms, are bioluminescent predatory insects that use light to attract prey. One species, Arachnocampa flava, is known to possess true circadian regulation of bioluminescence: light:dark cycles entrain the rhythm of nocturnal glowing. Given the absence of natural light as a cue in caves, we addressed the question of whether cave populations of Arachnocampa tasmaniensis, a species known to inhabit caves as well as epigean environments, are rhythmic. We found that the major dark-zone cave populations of A. tasmaniensis maintain a high-amplitude 24-hour rhythm of bioluminescence, with the acrophase during external daylight hours. Populations of A. tasmaniensis in caves many kilometers apart show similar, but not exactly the same, timing of the acrophase. Systematic investigation of colonies in the dark zone of a single cave showed that some smaller colonies distant to the main ceiling colony, also in the dark zone, glow in antiphase. Periodic monitoring of a single colony over several years showed that the acrophase shifted from nocturnal to diurnal some time between October 2008 and January 2009. Prey availability was investigated as a possible zeitgeber. The acrophase of prey availability, as measured by light trapping, and the acrophase of bioluminescence do not precisely match, occurring 3 hours apart. Using in-cave artificial light exposure, we show that after LD cycles, cave larvae become entrained to bioluminesce during the foregoing photophase. In contrast, epigean larvae exposed to artificial LD cycles after a period of DD become entrained to bioluminesce during the foregoing scotophase. One explanation is that individuals within colonies in the dark zone synchronize their bioluminescence rhythms through detection and matching of each other ’s bioluminescence.

Same temporal niche, opposite rhythmicity: two closely related bioluminescent insects with opposite bioluminesce propensity rhythms

Arachnocampa species, commonly called glowworms, are flies whose larvae use light to attract prey. Here we compare rhythmicity in two of the nine described species: the Tasmanian species, Arachnocampa tasmaniensis, which inhabits caves and wet forest, and the eastern Australian mainland species, A. flava, primarily found in subtropical rainforest. Both species show the same nocturnal glowing pattern in external (epigean) environments and the same inhibition of bioluminescence by light and both species show circadian regulation of bioluminescence. We find that the underlying circadian bioluminescence propensity rhythm (BPR) of the two species peaks at opposite phases of the day:night cycle. Larvae of A. flava, placed in constant darkness in the laboratory, bioluminesce during the subjective scotophase, typical of nocturnal animals, whereas A. tasmaniensis shows the opposite tendency, bioluminescing most intensely during the subjective photophase. In A. tasmaniensis, which are exposed to natural day:night cycles, light exposure during the day overrides the high bioluminescence propensity through negative masking and leads to a release of bioluminescence after dusk when the BPR is on the wane. A consequence is that A. tasmaniensis is able to start glowing at any phase of the light:dark cycle as soon as masking by light is released, whereas A. flava is locked into nocturnal bioluminescence. We suggest that the paradoxical BPR of A. tasmaniensis is an adaptation for living in the cave environment. Observations of bioluminescence in colonies of A. tasmaniensis located in the transition from a cave mouth to the dark zone show that glowing is inhibited by light exposure but a peak bioluminescence follows immediately after “dusk” at their location. The substantial difference in the circadian regulation of bioluminescence between the two species probably reflects adaptation to the cave (hypogean) habitat in A. tasmaniensis and the forest (epigean) habitat in A. flava. (Author correspondence: d.merritt@uq.edu.au)