Internal clocks, or circadian rhythms, are nearly ubiquitous across taxa (e.g., animals, plants, fungi, and cyanobacteria), and it is widely believed that a biological clock benefits organisms by enabling them to schedule behavioral and physiological changes in anticipation of predictable changes in environmental conditions. Theory and evidence suggest it is important that the internal clock resonate closely with the 24-h daily cycle. Recently, however, Cyclosa turbinata (Walckenaer, 1841) (Araneidae) was revealed to have a circadian clock with a period of about 19 h, which was presumed to be anomalous. Here, we report on the behavioral rhythms of a nocturnal orbweaver, Metazygia wittfeldae (McCook, 1894), from the same family. Under laboratory conditions of a 12:12 h light:dark cycle, we found that locomotor activity initiates shortly after dark, reaching a peak early in the dark phase, continuing at a lower level throughout the remaining dark phase, and then diminishing shortly after lights-on. Locomotor activity continued to cycle under constant dark conditions with a mean free-running period of 22.7 h. We also found a second component in the free-running activity (mean 11.5 h) which correlated very tightly with the free-running period. Thus, M. wittfeldae has what can be considered a typical circadian clock resonating with the 24-h day. Notably, however, there were two outliers close to the 19-h period observed in C.Turbinata, suggesting that there may be sufficient variation in clock period among araneid spiders upon which selection could act leading to the short-period clocks in C.Turbinata.

Most eukaryotic organisms have an internal circadian clock which allows them to maintain their physiological and behavioral cycles in phase with the 24-hour day. The ability to synchronize with (entrain to) the 24-hour day prevents mismatch between the internal circadian clock and the daily cycle which could lead to serious health risks. Some spider species, including Parasteatoda tepidariorum, appear to be exempt from the negative consequences of being out of phase with the 24-hour day. Parasteatoda tepidariorum, the common house spider, is a nocturnal species that consistently demonstrates a short-period circadian clock averaging 21.6 hours when left in constant darkness, yet they are able to entrain to the 24-hour light cycle. Here we test if these spiders are able to use cues (Zeitgebers) other than light to entrain to the 24-hour day. These non-photic Zeitgebers included food, disturbance, and temperature changes. The spiders were assigned into groups which received the given external cues at 24-hour intervals for 7 days followed by 7 days without any external cues. Food, disturbance, and temperature were not found to be effective Zeitgebers for the spiders’ entrainment. There were significant results between random feedings with consistent scheduled feedings which suggests that these spiders were able to manipulate the duration of activity based on the consistency and regularity of a food source. Adjusting the span of activity based on availability of food sources would be advantageous for spiders considering that prey availability in natural environments may not be rhythmic. Given that these spiders tend to build webs in dark secluded spaces, it would be a particular advantage for them to be able to use an environmental cue in addition to light to entrain their internal clocks. However, our data to date suggest otherwise.

A major advantage of having behavior controlled by a circadian clock is that the organism may be able to anticipate, rather than respond to, important daily events in its environment. Here, we describe the behavioral rhythms of locomotor activity and web building in the orb-weaving spider Cyclosa turbinata (Walckenaer, 1841). Web building occurs late in the scotophase, in absolute darkness, and is initiated and completed before lights-on under light:dark cycles in the laboratory. This scheduling presumably enables web-building to occur under the cover of darkness, thereby avoiding visual predators. Locomotor activity occurs predominantly in the dark with a sharp peak within one hour after lights-off and a broader peak occurring before lights-on. The locomotor activity rhythm free runs under constant dark and constant temperature conditions, thus indicating endogenous circadian control. Evidence from the free running rhythm suggests that the first peak under light:dark cycles is a result of masking but that the second peak is attributable to the endogenous circadian oscillator. The period of the free run is exceptionally short, about 19 hours. In comparison with locomotor activity, web building is quite sporadic under constant dark conditions, making detection of periodicities difficult and, therefore, whether web-building is under endogenous circadian control or is driven by exogenous factors remains unresolved.

Circadian rhythms are ubiquitous among eukaryotic organisms and have evolved several times independently which strongly suggests that the presence of a biological clock is adaptive. A prevailing, though relatively untested, hypothesis is that having an internal clock allows organisms to anticipate daily changes in the environment and physiologically and/or behaviorally prepare for them. Locomotor activity is commonly interpreted as an indicator of neurological arousal, and, thus, is a useful indicator in studies of circadian rhythm. We have observed that some species of spiders exhibit a tight and predictable band of activity at a particular time of day, while in other species activity is more spread out through the day. Such patterns tend to continue, or are exaggerated, under conditions of constant darkness. We hypothesize that these predators with tight activity bands are ‘circadian specialists’ using their internal clocks to focus their attention in the narrow temporal window when prey are available to them. On the other hand, the species with broader activity bands are employing a ‘circadian generalist’ strategy, and are able to be more opportunistic with temporally unpredictable prey. Some support of this hypothesis comes from the observation that species that forage only at night tend to have tighter bands of locomotor activity than those species which forage continuously day and night. In this study we present a simulation model that supports this idea that a tight distribution of neurological alertness is advantageous when prey is predictable, but an evenly clumped distribution of alertness is favored when prey are unpredictable. We also tested the abilities of four nocturnal spider species to opportunistically respond to an unexpected period of darkness. Consistent with our hypothesis, we found that in the predicted circadian specialist species activity could not be elicited with unexpected darkness at any time of day, while the predicted circadian generalist showed activity in mid and late day. In two species intermediate on the specialist-generalist scale we only elicited activity in late day. This work represents a test of a novel hypothesis regarding the adaptiveness of circadian rhythms.

Diel rhythms of physiology and behaviour are present in virtually all taxa examined to date. However, few studies have rigorously assessed the adaptive value of physiological and behavioural rhythms in animals. We laid the groundwork for an assessment of the adaptive rhythm hypothesis by assaying diel rhythms of foraging and antipredator behaviour in the trashline orb-weaver Cyclosa turbinata (Araneae: Araneidae). When confronted with a predator stimulus in experimental arenas, C.turbinata showed thanatosis behaviour more frequently and for longer durations during the day. However, assays of antipredator response within webs revealed more complex diel patterns of avoidance behaviours and no pattern of avoidance behaviour duration. A preliminary assay of prey capture behaviour suggested that C.turbinata also shows nocturnal patterns of foraging aggression. A refined foraging experiment, in which we randomized prey stimulus frequency, found that time of day and spider ID strongly predicted the likelihood of showing prey capture behaviour. Only spider ID predicted latency to attack the prey stimulus despite low individual repeatability (r= 0.10). These results support our prediction that C.turbinata modulate foraging aggression over the diel cycle, but we found no evidence of a trade-off between foraging behaviour and predator vigilance. However, overall patterns of vigilance may be masked by diel changes in antipredator strategies that correspond to fluctuations in the relative abundances of predator types.

Despite recent interest, there still is relatively little known about the ecology and physiology of diel and circadian rhythms in spiders. However, previous work on spiders suggests that there is a striking amount of variation in circadian period both among, and within, species, when compared to model organisms. Whereas previous studies of behavioral rhythms in spiders focused on females, here we describe the diel and circadian patterns of locomotor activity in male Parasteatoda tepidariorum (C. L. Koch, 1841) (Theridiidae). We found that the males showed mostly nocturnal activity under a light:dark cycle, with activity peaking very early after lights off and steadily declining to near zero just prior to lights on. Under constant darkness most individuals showed significant circadian rhythmicity with a mean free-running period of about 21.2 h. Though not the shortest average free-running period described for spiders, being so out of resonance with the 24 h solar day strains conventional circadian rhythm theory. Our data also suggest that the phase angle of entrainment for locomotor activity is in the mid-to-late photophase, but that activity may be masked by light. Of particular note is that both the diel and circadian activity patterns reported here for male P. tepidariorum are similar to those reported elsewhere for females of the species. This study deepens our understanding of the nature and variation in circadian rhythm in spiders and builds a case for further developing spiders as a model system for research integrating the fields of chronobiology and ecology.

Circadian rhythms are endogenous cycles that control physiological and behavioral changes that can be affected by environmental factors which allow most eukaryotic organisms to synchronize their daily activities with the 24-hour day. Parasteatoda tepidariorum,the common house spider, demonstrates a short-period circadian clock averaging 21.6 hours when left in constant darkness, yet they are able to entrain to a 24-hour light cycle. We tested whether these spiders were able to use non-photic Zeitgebers to entrain to the 24-hour day. Periodic presentation of food and disturbance were not found to be effective cues for the spiders’ entrainment. A few individuals were clearly able to entrain to an 8 oC amplitude temperature cycle, while most did not.

Few studies have rigorously assessed the adaptive value of diel rhythms in animals. We laid the groundwork for assessing the adaptive rhythm hypothesis by assaying diel rhythms of foraging and antipredator behavior in the orb-weaving spider Cyclosa turbinata. When confronted with a predator stimulus in experimental arenas, C. turbinata exhibited thanatosis behavior more frequently and for longer durations during the day. However, assays of antipredator response within webs revealed more complex diel patterns of avoidance behaviors and no pattern of avoidance behavior duration. Assays of prey capture behavior found that the likelihood of exhibiting prey capture behavior varied significantly across times of day and test subjects, but only test subject predicted attack latencies. Although C. turbinata foraging aggression changed over the diel cycle, we found no evidence of a trade-off between foraging behavior and predator vigilance. However, overall patterns of vigilance may be masked by diel changes in antipredator strategies.