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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

Distribution of live larvae on plant when they were eating, walking and resting, as well as the position of the cadavers (infected and uninfected), (n = 23).a) Height on plant, the scale is presented in terms of relative height with respect to the total height of each plant. b) Distance from stem (cm). Different letters indicate significant differences (ANOVA, p <0.05).
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pone.0136742.g003: Distribution of live larvae on plant when they were eating, walking and resting, as well as the position of the cadavers (infected and uninfected), (n = 23).a) Height on plant, the scale is presented in terms of relative height with respect to the total height of each plant. b) Distance from stem (cm). Different letters indicate significant differences (ANOVA, p <0.05).

Mentions: Of the 30 insects (replicates), 8 fell off the plant and did not climb back on during the 48 h observation period; these insects were eliminated from the study, leaving 22 active larvae and a total of 1056 hours of observation. As plants varied in height, the vertical position of each insect was expressed as percentage of total plant height (Fig 3A), with 100% being the topmost point on the plant. The vertical distribution of larvae on the plants varied significantly according to infection status (non-infected vs. infected cadavers) and the activity of the healthy insects (F = 3.33, df = 4, 95, P = 0.01). On average, infected larvae died on the upper 10% of the plant, whereas at the moment of death of the infected insect, non-infected larvae were observed at a significantly lower height, in the upper middle part of the plant (at ∼75% of the total height of the plant), (t = 3.2, df = 95, P = 0.001). At this moment, non-infected larvae were sacrificed in situ.


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)

Distribution of live larvae on plant when they were eating, walking and resting, as well as the position of the cadavers (infected and uninfected), (n = 23).a) Height on plant, the scale is presented in terms of relative height with respect to the total height of each plant. b) Distance from stem (cm). Different letters indicate significant differences (ANOVA, p <0.05).
© Copyright Policy
Related In: Results  -  Collection

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

pone.0136742.g003: Distribution of live larvae on plant when they were eating, walking and resting, as well as the position of the cadavers (infected and uninfected), (n = 23).a) Height on plant, the scale is presented in terms of relative height with respect to the total height of each plant. b) Distance from stem (cm). Different letters indicate significant differences (ANOVA, p <0.05).
Mentions: Of the 30 insects (replicates), 8 fell off the plant and did not climb back on during the 48 h observation period; these insects were eliminated from the study, leaving 22 active larvae and a total of 1056 hours of observation. As plants varied in height, the vertical position of each insect was expressed as percentage of total plant height (Fig 3A), with 100% being the topmost point on the plant. The vertical distribution of larvae on the plants varied significantly according to infection status (non-infected vs. infected cadavers) and the activity of the healthy insects (F = 3.33, df = 4, 95, P = 0.01). On average, infected larvae died on the upper 10% of the plant, whereas at the moment of death of the infected insect, non-infected larvae were observed at a significantly lower height, in the upper middle part of the plant (at ∼75% of the total height of the plant), (t = 3.2, df = 95, P = 0.001). At this moment, non-infected larvae were sacrificed in situ.

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