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Asynchrony between Host Plant and Insects-Defoliator within a Tritrophic System: The Role of Herbivore Innate Immunity.

Martemyanov VV, Pavlushin SV, Dubovskiy IM, Yushkova YV, Morosov SV, Chernyak EI, Efimov VM, Ruuhola T, Glupov VV - PLoS ONE (2015)

Bottom Line: The effects of asynchrony in the phenology of spring-feeding insect-defoliators and their host plants on insects' fitness, as well as the importance of this effect for the population dynamics of outbreaking species of insects, is a widespread and well-documented phenomenon.We show that a phenological mismatch induced by the delay in the emergence of gypsy moth larvae and following feeding on mature leaves has negative effects on the female pupal weight, on the rate of larval development and on the activity of phenoloxidase in the plasma of haemolymph.This study also reveals some indirect mechanisms of effect related to host plant quality, which operate through the insect innate immune status and affect resistance to both exogenous and endogenous virus.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Insect Pathology, Institute of Systematics and Ecology of Animals SB RAS, Novosibirsk, Russia; Biological Institute, National Research Tomsk State University, Tomsk, Russia.

ABSTRACT
The effects of asynchrony in the phenology of spring-feeding insect-defoliators and their host plants on insects' fitness, as well as the importance of this effect for the population dynamics of outbreaking species of insects, is a widespread and well-documented phenomenon. However, the spreading of this phenomenon through the food chain, and especially those mechanisms operating this spreading, are still unclear. In this paper, we study the effect of seasonally declined leafquality (estimated in terms of phenolics and nitrogen content) on herbivore fitness, immune parameters and resistance against pathogen by using the silver birch Betula pendula--gypsy moth Lymantria dispar--nucleopolyhedrovirus as the tritrophic system. We show that a phenological mismatch induced by the delay in the emergence of gypsy moth larvae and following feeding on mature leaves has negative effects on the female pupal weight, on the rate of larval development and on the activity of phenoloxidase in the plasma of haemolymph. In addition, the larval susceptibility to exogenous nucleopolyhydrovirus infection as well as covert virus activation were both enhanced due to the phenological mismatch. The observed effects of phenological mismatch on insect-baculovirus interaction may partially explain the strong and fast fluctuations in the population dynamics of the gypsy moth that is often observed in the studied part of the defoliator area. This study also reveals some indirect mechanisms of effect related to host plant quality, which operate through the insect innate immune status and affect resistance to both exogenous and endogenous virus.

No MeSH data available.


Related in: MedlinePlus

The effect of mismatch in the egg hatch of L. dispar on (a) the phenoloxidase activity in the plasma of fourth instar larvae, measured as ΔA490 min-1μl-1 plasma (mean±SE), on (b) the phenoloxidase activity in the plasma of fourth instar larvae, measured as ΔA490 min-1 mg-1 protein (mean±SE), on (c) the encapsulation of the nylon implant inserted into the hemocoel of fourth instar larvae (mean±SE), and on (d) the total hemocytes count in the haemolymph of fourth instar larvae (mean±SE).The data were pair-wise compared by the post hoc Fisher LSD procedure. The letters above the bar mean the significant differences (at P<0.05) to be compared with the bars abbreviated by the same letters within the bar. Uppercase letters mark the differences within the female group while lowercase letters mark the differences within the male group. The asterisk means the significant differences at P≤0.05 between males and females within one point of mismatch.
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pone.0130988.g005: The effect of mismatch in the egg hatch of L. dispar on (a) the phenoloxidase activity in the plasma of fourth instar larvae, measured as ΔA490 min-1μl-1 plasma (mean±SE), on (b) the phenoloxidase activity in the plasma of fourth instar larvae, measured as ΔA490 min-1 mg-1 protein (mean±SE), on (c) the encapsulation of the nylon implant inserted into the hemocoel of fourth instar larvae (mean±SE), and on (d) the total hemocytes count in the haemolymph of fourth instar larvae (mean±SE).The data were pair-wise compared by the post hoc Fisher LSD procedure. The letters above the bar mean the significant differences (at P<0.05) to be compared with the bars abbreviated by the same letters within the bar. Uppercase letters mark the differences within the female group while lowercase letters mark the differences within the male group. The asterisk means the significant differences at P≤0.05 between males and females within one point of mismatch.

Mentions: Phenoloxidase (PO) activity in larval plasma was significantly decreased (F4,36 = 9.223, P<0.001 measured as ΔA μl-1 plasma; F4,35 = 6.672, P = 0.001 measured as ΔA mg-1 protein) when the hatching of larvae was mismatched (Fig 5A and 5B). This decrease was linearly mismatch-dependent: n = 5; r2 = 0.88, b = -0.0232±0.0050, P = 0.018 for females, n = 5, r2 = 0.77, b = -0,021±0,0068, P = 0.053, for males, where ΔA μl-1 plasma, n = 5 r2 = 0.73, b = -0.0247±0.0086, P = 0.064 for females, n = 5 r2 = 0.70, b = -0.0184± 0.0070, P = 0.078 where ΔA mg-1 protein. Females possessed significantly higher PO activity compared to that of males when activity was measured as ΔA μl-1 plasma (F1,36 = 7.573, P = 0.009 calculated as ΔA μl-1 plasma, F1,36 = 2.126, P = 0.154 calculated as ΔA mg-1 protein).


Asynchrony between Host Plant and Insects-Defoliator within a Tritrophic System: The Role of Herbivore Innate Immunity.

Martemyanov VV, Pavlushin SV, Dubovskiy IM, Yushkova YV, Morosov SV, Chernyak EI, Efimov VM, Ruuhola T, Glupov VV - PLoS ONE (2015)

The effect of mismatch in the egg hatch of L. dispar on (a) the phenoloxidase activity in the plasma of fourth instar larvae, measured as ΔA490 min-1μl-1 plasma (mean±SE), on (b) the phenoloxidase activity in the plasma of fourth instar larvae, measured as ΔA490 min-1 mg-1 protein (mean±SE), on (c) the encapsulation of the nylon implant inserted into the hemocoel of fourth instar larvae (mean±SE), and on (d) the total hemocytes count in the haemolymph of fourth instar larvae (mean±SE).The data were pair-wise compared by the post hoc Fisher LSD procedure. The letters above the bar mean the significant differences (at P<0.05) to be compared with the bars abbreviated by the same letters within the bar. Uppercase letters mark the differences within the female group while lowercase letters mark the differences within the male group. The asterisk means the significant differences at P≤0.05 between males and females within one point of mismatch.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4482610&req=5

pone.0130988.g005: The effect of mismatch in the egg hatch of L. dispar on (a) the phenoloxidase activity in the plasma of fourth instar larvae, measured as ΔA490 min-1μl-1 plasma (mean±SE), on (b) the phenoloxidase activity in the plasma of fourth instar larvae, measured as ΔA490 min-1 mg-1 protein (mean±SE), on (c) the encapsulation of the nylon implant inserted into the hemocoel of fourth instar larvae (mean±SE), and on (d) the total hemocytes count in the haemolymph of fourth instar larvae (mean±SE).The data were pair-wise compared by the post hoc Fisher LSD procedure. The letters above the bar mean the significant differences (at P<0.05) to be compared with the bars abbreviated by the same letters within the bar. Uppercase letters mark the differences within the female group while lowercase letters mark the differences within the male group. The asterisk means the significant differences at P≤0.05 between males and females within one point of mismatch.
Mentions: Phenoloxidase (PO) activity in larval plasma was significantly decreased (F4,36 = 9.223, P<0.001 measured as ΔA μl-1 plasma; F4,35 = 6.672, P = 0.001 measured as ΔA mg-1 protein) when the hatching of larvae was mismatched (Fig 5A and 5B). This decrease was linearly mismatch-dependent: n = 5; r2 = 0.88, b = -0.0232±0.0050, P = 0.018 for females, n = 5, r2 = 0.77, b = -0,021±0,0068, P = 0.053, for males, where ΔA μl-1 plasma, n = 5 r2 = 0.73, b = -0.0247±0.0086, P = 0.064 for females, n = 5 r2 = 0.70, b = -0.0184± 0.0070, P = 0.078 where ΔA mg-1 protein. Females possessed significantly higher PO activity compared to that of males when activity was measured as ΔA μl-1 plasma (F1,36 = 7.573, P = 0.009 calculated as ΔA μl-1 plasma, F1,36 = 2.126, P = 0.154 calculated as ΔA mg-1 protein).

Bottom Line: The effects of asynchrony in the phenology of spring-feeding insect-defoliators and their host plants on insects' fitness, as well as the importance of this effect for the population dynamics of outbreaking species of insects, is a widespread and well-documented phenomenon.We show that a phenological mismatch induced by the delay in the emergence of gypsy moth larvae and following feeding on mature leaves has negative effects on the female pupal weight, on the rate of larval development and on the activity of phenoloxidase in the plasma of haemolymph.This study also reveals some indirect mechanisms of effect related to host plant quality, which operate through the insect innate immune status and affect resistance to both exogenous and endogenous virus.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Insect Pathology, Institute of Systematics and Ecology of Animals SB RAS, Novosibirsk, Russia; Biological Institute, National Research Tomsk State University, Tomsk, Russia.

ABSTRACT
The effects of asynchrony in the phenology of spring-feeding insect-defoliators and their host plants on insects' fitness, as well as the importance of this effect for the population dynamics of outbreaking species of insects, is a widespread and well-documented phenomenon. However, the spreading of this phenomenon through the food chain, and especially those mechanisms operating this spreading, are still unclear. In this paper, we study the effect of seasonally declined leafquality (estimated in terms of phenolics and nitrogen content) on herbivore fitness, immune parameters and resistance against pathogen by using the silver birch Betula pendula--gypsy moth Lymantria dispar--nucleopolyhedrovirus as the tritrophic system. We show that a phenological mismatch induced by the delay in the emergence of gypsy moth larvae and following feeding on mature leaves has negative effects on the female pupal weight, on the rate of larval development and on the activity of phenoloxidase in the plasma of haemolymph. In addition, the larval susceptibility to exogenous nucleopolyhydrovirus infection as well as covert virus activation were both enhanced due to the phenological mismatch. The observed effects of phenological mismatch on insect-baculovirus interaction may partially explain the strong and fast fluctuations in the population dynamics of the gypsy moth that is often observed in the studied part of the defoliator area. This study also reveals some indirect mechanisms of effect related to host plant quality, which operate through the insect innate immune status and affect resistance to both exogenous and endogenous virus.

No MeSH data available.


Related in: MedlinePlus