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Baculovirus-Induced Climbing Behavior Favors Intraspecific Necrophagy and Efficient Disease Transmission in Spodoptera exigua.

Rebolledo D, Lasa R, Guevara R, Murillo R, Williams T - PLoS ONE (2015)

Bottom Line: We examined whether this risky behavior was induced by olfactory or phagostimulant compounds associated with infected cadavers.Laboratory choice tests and olfactometer studies, involving infected and non-infected cadavers placed on spinach leaf discs, revealed no evidence for greater attraction of healthy larvae to virus-killed over non-infected cadavers.Healthy larvae also encountered and fed on infected cadavers significantly more frequently and more rapidly than larvae that fed on non-infected cadavers.

View Article: PubMed Central - PubMed

Affiliation: Instituto de Ecología AC, Xalapa, Veracruz, 91070, Mexico.

ABSTRACT
Shortly prior to death, many species of Lepidoptera infected with nucleopolyhedrovirus climb upwards on the host plant. This results in improved dissemination of viral occlusion bodies over plant foliage and an increased probability of transmission to healthy conspecific larvae. Following applications of Spodoptera exigua multiple nucleopolyhedrovirus for control of Spodoptera exigua on greenhouse-grown sweet pepper crops, necrophagy was observed by healthy S. exigua larvae that fed on virus-killed conspecifics. We examined whether this risky behavior was induced by olfactory or phagostimulant compounds associated with infected cadavers. Laboratory choice tests and olfactometer studies, involving infected and non-infected cadavers placed on spinach leaf discs, revealed no evidence for greater attraction of healthy larvae to virus-killed over non-infected cadavers. Physical contact or feeding on infected cadavers resulted in a very high incidence of transmission (82-93% lethal disease). Observations on the behavior of S. exigua larvae on pepper plants revealed that infected insects died on the uppermost 10% of foliage and closer to the plant stem than healthy conspecifics of the same stage, which we considered clear evidence of baculovirus-induced climbing behavior. Healthy larvae that subsequently foraged on the plant were more frequently observed closer to the infected than the non-infected cadaver. Healthy larvae also encountered and fed on infected cadavers significantly more frequently and more rapidly than larvae that fed on non-infected cadavers. Intraspecific necrophagy on infected cadavers invariably resulted in virus transmission and death of the necrophagous insect. We conclude that, in addition to improving the dissemination of virus particles over plant foliage, baculovirus-induced climbing behavior increases the incidence of intraspecific necrophagy in S. exigua, which is the most efficient mechanism of transmission of this lethal pathogen.

No MeSH data available.


Related in: MedlinePlus

Mean distance between healthy larvae and infected or non-infected cadavers.a) Hourly means of observations performed over a 48 h period on each larva (n = 22 larvae). Points labeled with numerical values indicate number of acts of necrophagy observed at each time point (values shown in blue refer to necrophagy on non-infected cadavers, values in red refer to necrophagy on infected cadavers); b) Mean percentage of observations in which the experimental insect was closer to the infected (red column) or non-infected (blue column) cadaver. Vertical bars indicate SE.
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pone.0136742.g004: Mean distance between healthy larvae and infected or non-infected cadavers.a) Hourly means of observations performed over a 48 h period on each larva (n = 22 larvae). Points labeled with numerical values indicate number of acts of necrophagy observed at each time point (values shown in blue refer to necrophagy on non-infected cadavers, values in red refer to necrophagy on infected cadavers); b) Mean percentage of observations in which the experimental insect was closer to the infected (red column) or non-infected (blue column) cadaver. Vertical bars indicate SE.

Mentions: The straight-line distance was measured between healthy larvae and infected and non-infected cadavers at each hourly observation (Fig 4A). The frequencies with which each larva was closer to the infected or non-infected cadaver were compared by fitting a generalized linear model with a binomial error structure specified. On average, larvae were observed to be closer to the infected cadaver on two-thirds (66.5%) of occasions and closer to the non-infected cadaver on one third (33.5%) of occasions, indicating a significant tendency to be closer to the infected cadaver than expected given a random distribution on the plant (χ2 = 175.1, df = 1, P < 0.001) (Fig 4B).


Baculovirus-Induced Climbing Behavior Favors Intraspecific Necrophagy and Efficient Disease Transmission in Spodoptera exigua.

Rebolledo D, Lasa R, Guevara R, Murillo R, Williams T - PLoS ONE (2015)

Mean distance between healthy larvae and infected or non-infected cadavers.a) Hourly means of observations performed over a 48 h period on each larva (n = 22 larvae). Points labeled with numerical values indicate number of acts of necrophagy observed at each time point (values shown in blue refer to necrophagy on non-infected cadavers, values in red refer to necrophagy on infected cadavers); b) Mean percentage of observations in which the experimental insect was closer to the infected (red column) or non-infected (blue column) cadaver. Vertical bars indicate SE.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4581871&req=5

pone.0136742.g004: Mean distance between healthy larvae and infected or non-infected cadavers.a) Hourly means of observations performed over a 48 h period on each larva (n = 22 larvae). Points labeled with numerical values indicate number of acts of necrophagy observed at each time point (values shown in blue refer to necrophagy on non-infected cadavers, values in red refer to necrophagy on infected cadavers); b) Mean percentage of observations in which the experimental insect was closer to the infected (red column) or non-infected (blue column) cadaver. Vertical bars indicate SE.
Mentions: The straight-line distance was measured between healthy larvae and infected and non-infected cadavers at each hourly observation (Fig 4A). The frequencies with which each larva was closer to the infected or non-infected cadaver were compared by fitting a generalized linear model with a binomial error structure specified. On average, larvae were observed to be closer to the infected cadaver on two-thirds (66.5%) of occasions and closer to the non-infected cadaver on one third (33.5%) of occasions, indicating a significant tendency to be closer to the infected cadaver than expected given a random distribution on the plant (χ2 = 175.1, df = 1, P < 0.001) (Fig 4B).

Bottom Line: We examined whether this risky behavior was induced by olfactory or phagostimulant compounds associated with infected cadavers.Laboratory choice tests and olfactometer studies, involving infected and non-infected cadavers placed on spinach leaf discs, revealed no evidence for greater attraction of healthy larvae to virus-killed over non-infected cadavers.Healthy larvae also encountered and fed on infected cadavers significantly more frequently and more rapidly than larvae that fed on non-infected cadavers.

View Article: PubMed Central - PubMed

Affiliation: Instituto de Ecología AC, Xalapa, Veracruz, 91070, Mexico.

ABSTRACT
Shortly prior to death, many species of Lepidoptera infected with nucleopolyhedrovirus climb upwards on the host plant. This results in improved dissemination of viral occlusion bodies over plant foliage and an increased probability of transmission to healthy conspecific larvae. Following applications of Spodoptera exigua multiple nucleopolyhedrovirus for control of Spodoptera exigua on greenhouse-grown sweet pepper crops, necrophagy was observed by healthy S. exigua larvae that fed on virus-killed conspecifics. We examined whether this risky behavior was induced by olfactory or phagostimulant compounds associated with infected cadavers. Laboratory choice tests and olfactometer studies, involving infected and non-infected cadavers placed on spinach leaf discs, revealed no evidence for greater attraction of healthy larvae to virus-killed over non-infected cadavers. Physical contact or feeding on infected cadavers resulted in a very high incidence of transmission (82-93% lethal disease). Observations on the behavior of S. exigua larvae on pepper plants revealed that infected insects died on the uppermost 10% of foliage and closer to the plant stem than healthy conspecifics of the same stage, which we considered clear evidence of baculovirus-induced climbing behavior. Healthy larvae that subsequently foraged on the plant were more frequently observed closer to the infected than the non-infected cadaver. Healthy larvae also encountered and fed on infected cadavers significantly more frequently and more rapidly than larvae that fed on non-infected cadavers. Intraspecific necrophagy on infected cadavers invariably resulted in virus transmission and death of the necrophagous insect. We conclude that, in addition to improving the dissemination of virus particles over plant foliage, baculovirus-induced climbing behavior increases the incidence of intraspecific necrophagy in S. exigua, which is the most efficient mechanism of transmission of this lethal pathogen.

No MeSH data available.


Related in: MedlinePlus