Nocturnal forays, part 3: light, dark, and hunger

Romero, Alvaro, Michael F Potter, and Kenneth F Haynes. 2010. Circadian rhythm of spontaneous locomotor activity in the bed bug, Cimex lectularius L. Journal of Insect Physiology 56: 1516-1522. doi:10.1016/j.jinsphys.2010.04.025.  

If you don’t have access to this article, then I recommend, highly recommend, that you access Dr. Romero’s dissertation. It’s publicly available and an awesome read.

Some time ago, very briefly, we mentioned the phases of host-seeking in blood-sucking insects described by Lehane. Another author has proposed some reorderings and extensions as follows (Lazzari 2009):

  1. activation
  2. appetitive search
  3. host detection
  4. host finding
  5. host contact
  6. host biting
  7. food recognition and feeding
  8. leaving the host

Quite the long list of things to investigate in the bed bug? (And of tasks for the bed bug itself.) But we can try to understand what is being discovered and place what came before in some context, if possible — though Mellanby’s bed bugs, rooming as they were with rats, very efficient predators of bed bugs those rats!, may give us some trouble. And, by the way, aren’t rats themselves nocturnal? How would that fit in?

Regarding the first step, Lazzari says simply: “When hosts are less active or the environmental conditions become adequate for food search, the insects start moving spontaneously.” Before coming into contact with or indeed searching for host cues. This spontaneous activity may be, and I think usually is, controlled by an internal clock. Many other processes, like mating, laying and emerging from eggs, emerging from nymphal stages, indeed the time of day when an insect is more or less sensitive to odors, may be controlled by internal clocks (Lazzari and Insausti 2008). And these clocks can synchronize with external cues, such as the daily cycles of light and temperature. Adjustable internal clocks seem convenient for the enterprise of living, making it possible to anticipate changes, learn and adapt.

For circadian terms, I have been relying on this Dictionary of Circadian Physiology which you may also find very useful:

The zeitgeber [synchronizing stimulus] “gives” the local time, not the ability to keep time (which the organism already possesses).

Back then to Romero et al. 2010:

Evidence of endogenous rhythms of activity is revealed when the animal is experimentally exposed to contstant dark (DD), or constant light (LL), where temperature and any possible external factor (Zeitgeber) are kept constant (Aschoff, 1960).

The insects used in this study were female and male adults and 5th instar nymphs. Three nutritional states were examined: unfed for one week (adults and 5th instars), unfed for five weeks (adults and 5th instars), and recently fed (2 days before) adults.

The method of this study is very interesting, digital photographs. Thousands of photographs taken at 10-minute intervals were examined and the positional changes of the bed bug recorded. A minimum of 864 photos per bed bug, 12 bed bugs per experimental group.

Findings

Bed bugs are nocturnal! (But this wouldn’t be about bed bugs if there weren’t some rather tricky and enigmatic aspects.)

Most movement (more than 80% of recorded positional changes for adults and more than 60% for nymphs regardless of nutritional state) occurs in the dark segment of a 24-hr light-dark cycle of 14 hours of light followed by 10 hours of dark, 14:10 L:D. This dark segment is called the scotophase, but we will call it night where possible here. Movement begins soon after lights-off, continues and remains high for several hours, and then declines in the last third of the night. Onset of activity is about 2 hours into the night. There are gender and nutritional state differences in the offset of activity, with females stopping movements later in the night (8.3 ± 0.14 h) than males (7.9 ± 0.14 h), and 1-week-unfed adults stopping later (8.7 ± 0.14 h) than 5-week-unfed adults (7.5 ± 0.18 h) or 2-days-recently-fed adults (8.1 ± 0.17).

The study further shows that bed bugs have an internally controlled rhythm of activity that persists under conditions of constant dark (DD) or constant light (LL) for 4 days. Thereafter “the rhythms were disrupted in DD and became less distinct in LL.”

If the dark segment of the light-dark cycle is extended 12 hours, bed bugs gradually shift their activity to the new “night” and require four days to recover to previous peaks of activity.

Based on the discussion of peak activity recovery after a phase shift, if I understand correctly, the night-time peaks of activity (in the dark segment of a 12:12 L:D cycle) were 6.2h [5.1–7.3] for females and 6.3 h [5.3–7.4] for males.

And this is very interesting, a burst of activity occurs shortly after lights-on:

In the transition from dark to light, most of the insects showed a sudden increase in activity, but the frequency of movements rapidly decreased, persisting at low levels throughout the photophase [...] Half of the photophase movements in all groups occurred 1 h after lights-on.

The authors suggest two possible explanations: “an excitatory reaction of bed bugs caused by the lights-on transitional signal (Aboul-Nasr and Erakey, 1968)” or else the lights-on signal may be “an indication to wandering bed bugs that it is time to return to the less exposed harborages.”

Note that each bed bug in the experimental chamber rested on filter paper inside a petri dish, thus exposed and not in a refugium.

As for the relative movement of female vs male and fed vs unfed bed bugs:

Adults held unfed for one week (averaging females and males) moved 18% more often than those unfed for five weeks (36.0 and 25.1 positional changes per day, respectively) (t = 3.5; df = 78; P < 0.05) and 22% more than adults that had fed (36.0 and 23.0, respectively) (t = 4.3; df = 77; P < 0.05) (Fig. 6). There was no significant difference in the number of positional changes between adults held unfed for five weeks and those that had fed (t = 0.77; df = 78; P = 0.72). Overall, females changed position significantly more than males (30.4 and 25.5 movements per day, respectively) (F = 3.9; df = 1, 78; P < 0.05).

Finally, the pattern of activity over time (6 days) [you can see these fluctuation charts on page 45 (Romero 2009), and indeed all the other charts] is described thus:

Adults that had fed showed a different daily fluctuation in the pattern of movements (Fig. 7A). By day three, males had increased movements with respect to day one by 61%, but female movement only increased 10% (Fig. 7A). However, after day three, males moved gradually less until the end of the experiment at day six, reaching levels similar to those recorded on day one. In contrast, females increased their activity only after day three until day six, having an increase of 46% at this time compared to movements recorded on day one. Adults held unfed for one week showed a marked fluctuation in daily activity over the six days of recording (Fig. 7B). By the third day, bed bugs from this group had increased their spontaneous activity by 21 and 30% (females and males, respectively), in relation to the first day. After day three the number of movements of both groups gradually decreased. By the end of the recording period, females and males from this group reduced daily movements by 18 and 13%, respectively, in relation to day one, and 32 and 33% from their respective activity peak (Fig. 7B). A less pronounced fluctuation of activity was displayed by bed bugs held unfed for five weeks (Fig. 7C). During the first days, the activity of females and males remained relatively stable; then after day three, the daily rate of movements began to decrease until the end of the experiment. Females and males from this group reduced the overall number of daily movements by 33 and 29%, respectively, in relation to day one (Fig. 7C).

Questions!

First the obligatory question about what this could mean for dispersal, as we have been wondering forever. Not sure why I even expect new information to shed light on this question, seems the most difficult one, just being hopeful and wondering. So: if 5 weeks of starvation are enough to make bed bugs a bit conservative in their spontaneous activity, then who are the dispersers, if there is such a word, the bed bugs that will move long distances in search of a host (instead of giving up? or remaining where they are?), and what possible combination of nutritional, environmental or conspecific cues make them go? Obviously, more research is needed.

More related to what we have reviewed in the previous two posts, you may well be thinking that none of this described so far (actually, that’s not quite right, none of it except for the nocturnal part and the suggested relationship between nutritional state and activity) is very congruent with what Mellanby observed, or rather concluded from his trap catches.

What to make of this?

Regarding the differences between their findings and Mellanby’s, the authors cite the difference in methodology, as their experiments were conducted under controlled conditions without a host, and Mellanby’s was based on passive trap catches, and further, the recurring appearance of someone checking the traps every 3 hours which could have disturbed the normal pattern of activity.

But this isn’t very satisfying, isn’t it? Because if Mellanby’s peak trap catch was not a measurement of peak activity of bed bugs, what was it a measurement of?

So much work has to be done. But indeed who will look at 864 photographs of each bed bug or perform similar feats!

Just to look at some complexities and interactions that may (or may not!) be studied later in the bed bug, consider that in another blood-sucking insect, Triatoma infestans (the kissing bug), there are two peaks of locomotor activity in what is called a bimodal circadian rhythm. One occurs early in the night and is associated with host-seeking and the second peak occurs before dawn and is associated with refuge-seeking (Lorenzo and Lazzari 1998). T. infestans actually remains outside its harborage in the intervening hours between the two peaks, “performing a copious diuresis” (Lorenzo 1997, cited in Lorenzo Figueiras and Lazzari 2000). T. infestans is not attracted by the fresh fecal traces of conspecifics and does not assemble on fecal “footprints” until 8-10 hours hours have passed from its blood meal (Lorenzo Figueiras and Lazzari 2000). An investigation into the temporal change of the aggregation response yielded the insight that peak aggregation (insects clustered together with other insects) occurs just before sunrise (Minoli et al. 2007).

Reading about triatomines is enormously interesting even if there are seemingly many important differences between them and old Cimex l.

What do you think? Were Mellanby’s bed bugs exhibiting a marked aggregation response at a certain time, confusing a trap for refuge? Something to think about when considering Mellanby’s traps or useless spitballing? I confess I’m slightly confused, and therefore reaching.

References:

Lazzari, Claudio R. 2009. Orientation Towards Hosts in Haematophagous Insects: An Integrative Perspective. Advances in Insect Physiology 37: 1-58. doi:10.1016/S0065-2806(09)37001-0

Lazzari, C.R. and Insausti, T.C. 2008. Circadian rhythms in insects, In: M.L. Fajul-Moles & R. Aguilar-Roblero (eds.) Comparative aspects of circadian rhythms. Research Signpost (ISBN 978-81-7895-329-8). [PDF available here]

Lorenzo, Marcelo G., and Claudio R. Lazzari. 1998. Activity pattern in relation to refuge exploitation and feeding in Triatoma infestans (Hemiptera: Reduviidae). Acta Tropica 70: 163-170. doi:10.1016/S0001-706X(98)00025-4.

Lorenzo Figueiras, A N, and C R Lazzari. 2000. Temporal change of the aggregation response in Triatoma infestans. Memórias Do Instituto Oswaldo Cruz 95: 889-892. doi:10.1590/S0074-02762000000600026

Mellanby, Kenneth. 1939. The Physiology and Activity of the Bed-Bug (Cimex Lectularius L.) in a Natural Infestation. Parasitology 31: 200-211. doi:10.1017/S0031182000012762.  

Mellanby, Kenneth. 1940. Rhythmic Activity in Domestic Insects. Acta Medica Scandinavica 103: 89-98. doi:10.1111/j.0954-6820.1940.tb11083.x

Minoli, S A, S Baraballe, and A N Lorenzo Figueiras. 2007. Daily rhythm of aggregation in the haematophagous bug Triatoma infestans (Heteroptera: Reduviidae). Memórias Do Instituto Oswaldo Cruz 102: 449-454. doi:10.1590/S0074-02762007005000033

Romero, Alvaro. 2009. Biology and Management of the Bed Bug, Cimex lectularius L. (Heteroptera: Cimicidae). Ph.D. dissertation, University of Kentucky. http://archive.uky.edu/handle/10225/1119

Romero, Alvaro, Michael F Potter, and Kenneth F Haynes. 2010. Circadian rhythm of spontaneous locomotor activity in the bed bug, Cimex lectularius L. Journal of Insect Physiology 56: 1516-1522. doi:10.1016/j.jinsphys.2010.04.025.  

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