Seminar of Applied Entomology and Zoology by LUO Zhixin
December 6, 2012
Effect of changed environmental CO2 on oviposition behavior
in nocturnal Lepidoptera insect
Carbon dioxide (CO2) is a ubiquitous sensory cue that plays multiple roles in insect behavior. The most
famous and well-known example is CO2 releasing from vertebrates (eg. human) helps blood-sucking insects (eg.
mosquito) detect and orientate toward a host and thus plays a role in foraging. After years of research, the roles
of CO2 cues in oviposition and foraging behaviors of phytophagous insects and the mechanistic bases of
behavioral modulation by CO2 (sensory organ, receptor-cells and antennal lobes in brain) are currently being
revealed and understood.
Considering the yellow peach moth in my study is a nocturnal species, which may also utilize changed
environmental CO2 levels and/or other signals (such as volatiles, humidity, temperature) from host-plant or its
fruits for oviposition or suitable habitat orientation, I focus on two particularly well suited nocturnal species in
Lepidoptera in this review.
The pyralid moth Cactoblastis cactorum (CC) females oviposit on cladodes of their host plant cactus Opuntia
stricta (OS), a crassulacean acid metabolism (CAM) plant, as egg sticks. Adopt to dry weather condition, OS plants
open stomata and assimilate CO2 (CO2 fixation) after sunset and thus are nocturnal CO2 sinks on the cladode
surfaces (Stange 1997), generating a negative CO2 gradient (>80ppm) within a boundary layer of about 5mm over
the surface of the plant (Stange et al.1995).
In contrast, Datura and Nicotiana plants (C3 plant) which the sphingid moth Manduca sexta (MS) feeding
and ovipositing on are important sources of respiratory CO2 in the evening. Night-blooming flowers of Datura
wrightii (DW) show transient emissions of up to 200 ppm above-ambient CO2, when nectar rewards are richest
(Goyret et al. 2008).
The labial palp (a paired mouthpart) of adult Lepidoptera occurs throughout this order and contains a large
number of sensory neurons. The labial-palp pit organ (LPO), looks like a pore, normally on the distalmost
segment of labial palp has been identified as being specialized to sensing CO2. It contains a number of sensilla
that vary from a few to more than 1000 depending on the species. All those sensilla contain receptor cells (RCs)
specialized to encode rapid changes in CO2 level (Kent et al. 1986, Stange et al. 1995, Guerenstein & Hildebrand
2008).
In CC, male has vestigial LPO, whereas female uses its well developed LPO to detect gradients of CO2
concentration for oviposition on host cactus (Stange et al.1995, Stange 1997). By contrast, the LPOs of adult MS
are well developed in both sexes (Kent et al. 1986), suggesting that they contribute to adult nectar foraging rather
than, or in addition to, oviposition (Abrell et al. 2005, Goyret et al. 2008).
The LPO of CC contains
approximately 200 sensilla (Stange et al. 1995). In comparison, the LPO of MS contains 1750 sensilla, Antheraea
polyphemus 40 sensilla (Kent et al. 1986).
The CO2 receptor cells in CC are sensitive to short stimulation of higher CO2 concentration (1s) or rapid
changes in 5-mm-boundary-layer of plant surface. However, they decrease or stop firing under increased
background levels CO2 (Stange et al. 1995, Abrell et al. 2005). In comparison, CO2 RCs in MS do not show signs
of sensory fatigue during continued stimulation (increased background). These cells can function under a wide
range of environmental CO2 levels while still responding to rapid changes in CO2 levels (Abrell et al. 2005).
In free-air CO2 enrichment (FACE) ring oviposition experiments of CC, host plants surrounded with both a
doubled-fluctuated and a doubled non-fluctuated CO2 level are less attractive for oviposition of CC. It was
suggested that reduced input from CO2 receptor cells strongly interfere with brain processing of signals involved
in oviposition behavior of moths (Stange 1997). The preference of MS for oviposition on control plants was also
greater than higher-fluctuating CO2 level (Abrell et al. 2005). These suggests that CO2 fluctuations are relevant
to moth behavior and large CO2 fluctuations confuse the animal’s system for sensing plant-derived CO2.
In the habitat of host plant of CC, two types of CO2 gradients occur that are detectable by female for
oviposition. The first gradient, related to soil respiration, is vertical and extends from the soil surface to 1 m. It
provides female a cue for keeping flight in floor boundary layer until landing. The second gradient, caused by
CO2 fixation, is from the plant surface to about 5 mm. It helps females detect the healthiest plants with higher
metabolic activity by probing the cladode boundary layer with LPO rapidly before ovipositing. Both gradients
are well above the detection threshold (40ppm, 1s) of the CO2-detection system (Stange et al. 1995).
While the habit that adult MS feeding and oviposition on host plant makes researchers difficult to conduct a
absolute oviposition experiment (Abrell et al. 2005). In nectar foraging experiment, both female and male
significantly preferred to scented paper flowers emitted above-ambient CO2 levels (Visual + Olfactory cues +CO2)
under host-plant volatiles context, suggesting CO2 contributes to feeding behavior of this species. Unexpectedly,
host plant volatiles context had a dramatic influence on female responses, which strongly suggests a combined
oviposition-feeding behavior in host recognization (Goyret et al. 2008).
In conclusion, changed environmental CO2 levels is associated with oviposition behavior of CC and
oviposition-feeding behavior of the MS, that broadens our knowledge of the behavioral roles of CO2 in the
interaction between nocturnal Lepidoptera insects and their host plants. Large fluctuations of CO2
concentration can confuse nocturnal moth’s system for sensing plant-derived CO2, which may be utilized for
disturbing and controlling selective CO2-sensing pest insects in the future.
The intra- and interspecific difference of CO2 sensory organ in CC and MS (vestigial or not, number of sensilla,
sensitivity of RCs) is relevant to sexual dimorphism in life habits of themselves (host for feeding and/or oviposition)
and also to life habits of their host (C3 and CAM plant), which indicates their adaptation in evolution process.
The evidence obtained so far for these two species is indirect. To obtain direct evidence, plants emitting
different natural levels of CO2 should be offered in a choice test. Therefore, a developed artificial model of host
plant or special part (eg. fruit) will be helpful to research different stimuli for multi-propose host recognization.
Keywords CO2・ oviposition・ nocturnal Lepidoptera・ host plant・ LPO・ RCs
References
Stange, G (1997) Effects of changes in atmospheric carbon dioxide on the location of hosts by the moth, Cactoblastis cactorum.
Oecologia 110: 539-545
Abrell L, Guerenstein PG, Mechaber WL, Stange G, Christensen TA, Nakanishi K, Hildebrand JG (2005)
Effect of elevated
atmospheric CO2 on oviposition behavior in Manduca sexta moths. Global Change Biology 11: 1272-1282
Stange G, Monro J, Stowe S, Osmond CB (1995) CO2 sense of the moth Cactoblastis cactorum and its probable role in the biological
control of the CAM plant Opuntia stricta. Oecologia 102: 341-352
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Goyret J, Markwell PM, Raguso RA (2008) Context- and scale-dependent effects of floral CO2 on nectar foraging by Manduca sexta.
PNAS 105: 4565-4570
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