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Caterpillars and fungal pathogens: two co-occurring parasites of an ant-plant mutualism.

Roux O, Céréghino R, Solano PJ, Dejean A - PLoS ONE (2011)

Bottom Line: This probable temporal priority effect also allows female moths to lay new eggs on trees that already shelter caterpillars, and so to occupy the niche longer and exploit Cecropia resources before colonization by ants.Although no higher herbivory rates were noted, these caterpillars are ineffective in protecting their host trees from a pathogenic fungus, Fusarium moniliforme (Deuteromycetes), that develops on the trichilium in the absence of mutualistic ants.The cost of greater FB production plus the presence of the pathogenic fungus likely affect tree growth.

View Article: PubMed Central - PubMed

Affiliation: CNRS, Écologie des Forêts de Guyane (UMR-CNRS 8172), Campus Agronomique, Kourou, France. olivier.roux@ird.fr

ABSTRACT
In mutualisms, each interacting species obtains resources from its partner that it would obtain less efficiently if alone, and so derives a net fitness benefit. In exchange for shelter (domatia) and food, mutualistic plant-ants protect their host myrmecophytes from herbivores, encroaching vines and fungal pathogens. Although selective filters enable myrmecophytes to host those ant species most favorable to their fitness, some insects can by-pass these filters, exploiting the rewards supplied whilst providing nothing in return. This is the case in French Guiana for Cecropia obtusa (Cecropiaceae) as Pseudocabima guianalis caterpillars (Lepidoptera, Pyralidae) can colonize saplings before the installation of their mutualistic Azteca ants. The caterpillars shelter in the domatia and feed on food bodies (FBs) whose production increases as a result. They delay colonization by ants by weaving a silk shield above the youngest trichilium, where the FBs are produced, blocking access to them. This probable temporal priority effect also allows female moths to lay new eggs on trees that already shelter caterpillars, and so to occupy the niche longer and exploit Cecropia resources before colonization by ants. However, once incipient ant colonies are able to develop, they prevent further colonization by the caterpillars. Although no higher herbivory rates were noted, these caterpillars are ineffective in protecting their host trees from a pathogenic fungus, Fusarium moniliforme (Deuteromycetes), that develops on the trichilium in the absence of mutualistic ants. Therefore, the Cecropia treelets can be parasitized by two often overlooked species: the caterpillars that shelter in the domatia and feed on FBs, delaying colonization by mutualistic ants, and the fungal pathogen that develops on old trichilia. The cost of greater FB production plus the presence of the pathogenic fungus likely affect tree growth.

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Trichilium of Cecropia.A- Azteca alfari workers removing food bodies (arrow) from a Cecropia obtusa trichilium. B- Pseudocabima guianalis caterpillars occupying the upper part of a C. obtusa. They gnawed an entrance hole into the prostomata (p) in order to enter into the hollow internodes. Secreted strands of silk cover the trichilium and keep the withered stipules (DS) from falling. C- Trichilium of C. obtusa infested by Fusarium moniliforme. D- Penetration by a filament of F. moniliforme (arrows) inside a food body (FB). E–F. moniliforme spreading throughout a food body (FB and black arrows). The cells of the trichilium at the base of the FB seem to react to the presence of fungus (white arrow).
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pone-0020538-g001: Trichilium of Cecropia.A- Azteca alfari workers removing food bodies (arrow) from a Cecropia obtusa trichilium. B- Pseudocabima guianalis caterpillars occupying the upper part of a C. obtusa. They gnawed an entrance hole into the prostomata (p) in order to enter into the hollow internodes. Secreted strands of silk cover the trichilium and keep the withered stipules (DS) from falling. C- Trichilium of C. obtusa infested by Fusarium moniliforme. D- Penetration by a filament of F. moniliforme (arrows) inside a food body (FB). E–F. moniliforme spreading throughout a food body (FB and black arrows). The cells of the trichilium at the base of the FB seem to react to the presence of fungus (white arrow).

Mentions: We conducted this study between 2000 and 2009 in French Guiana near the Petit Saut dam (5°03′39″ N-53°02′36″W) and near the Montagne des singes (5°04′19.6″N-52°41′42.5″W). We selected and tagged C. obtusa that were ca. 1.15 m to 1.30 m tall (N = 610) between 2000 and 2006 in a cleared 1.5 ha zone situated near the dam, and on plants growing along a straight, recently-opened dirt road near the Montagne des singes (N = 64) between 2006 and 2009. In these areas, C. obtusa is mostly associated with Azteca alfari and A. ovaticeps whose colonies exploit Müllerian bodies (Fig. 1A), tend hemipterans in the host tree domatia and prey on insects landing on the leaves [42].


Caterpillars and fungal pathogens: two co-occurring parasites of an ant-plant mutualism.

Roux O, Céréghino R, Solano PJ, Dejean A - PLoS ONE (2011)

Trichilium of Cecropia.A- Azteca alfari workers removing food bodies (arrow) from a Cecropia obtusa trichilium. B- Pseudocabima guianalis caterpillars occupying the upper part of a C. obtusa. They gnawed an entrance hole into the prostomata (p) in order to enter into the hollow internodes. Secreted strands of silk cover the trichilium and keep the withered stipules (DS) from falling. C- Trichilium of C. obtusa infested by Fusarium moniliforme. D- Penetration by a filament of F. moniliforme (arrows) inside a food body (FB). E–F. moniliforme spreading throughout a food body (FB and black arrows). The cells of the trichilium at the base of the FB seem to react to the presence of fungus (white arrow).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3105098&req=5

pone-0020538-g001: Trichilium of Cecropia.A- Azteca alfari workers removing food bodies (arrow) from a Cecropia obtusa trichilium. B- Pseudocabima guianalis caterpillars occupying the upper part of a C. obtusa. They gnawed an entrance hole into the prostomata (p) in order to enter into the hollow internodes. Secreted strands of silk cover the trichilium and keep the withered stipules (DS) from falling. C- Trichilium of C. obtusa infested by Fusarium moniliforme. D- Penetration by a filament of F. moniliforme (arrows) inside a food body (FB). E–F. moniliforme spreading throughout a food body (FB and black arrows). The cells of the trichilium at the base of the FB seem to react to the presence of fungus (white arrow).
Mentions: We conducted this study between 2000 and 2009 in French Guiana near the Petit Saut dam (5°03′39″ N-53°02′36″W) and near the Montagne des singes (5°04′19.6″N-52°41′42.5″W). We selected and tagged C. obtusa that were ca. 1.15 m to 1.30 m tall (N = 610) between 2000 and 2006 in a cleared 1.5 ha zone situated near the dam, and on plants growing along a straight, recently-opened dirt road near the Montagne des singes (N = 64) between 2006 and 2009. In these areas, C. obtusa is mostly associated with Azteca alfari and A. ovaticeps whose colonies exploit Müllerian bodies (Fig. 1A), tend hemipterans in the host tree domatia and prey on insects landing on the leaves [42].

Bottom Line: This probable temporal priority effect also allows female moths to lay new eggs on trees that already shelter caterpillars, and so to occupy the niche longer and exploit Cecropia resources before colonization by ants.Although no higher herbivory rates were noted, these caterpillars are ineffective in protecting their host trees from a pathogenic fungus, Fusarium moniliforme (Deuteromycetes), that develops on the trichilium in the absence of mutualistic ants.The cost of greater FB production plus the presence of the pathogenic fungus likely affect tree growth.

View Article: PubMed Central - PubMed

Affiliation: CNRS, Écologie des Forêts de Guyane (UMR-CNRS 8172), Campus Agronomique, Kourou, France. olivier.roux@ird.fr

ABSTRACT
In mutualisms, each interacting species obtains resources from its partner that it would obtain less efficiently if alone, and so derives a net fitness benefit. In exchange for shelter (domatia) and food, mutualistic plant-ants protect their host myrmecophytes from herbivores, encroaching vines and fungal pathogens. Although selective filters enable myrmecophytes to host those ant species most favorable to their fitness, some insects can by-pass these filters, exploiting the rewards supplied whilst providing nothing in return. This is the case in French Guiana for Cecropia obtusa (Cecropiaceae) as Pseudocabima guianalis caterpillars (Lepidoptera, Pyralidae) can colonize saplings before the installation of their mutualistic Azteca ants. The caterpillars shelter in the domatia and feed on food bodies (FBs) whose production increases as a result. They delay colonization by ants by weaving a silk shield above the youngest trichilium, where the FBs are produced, blocking access to them. This probable temporal priority effect also allows female moths to lay new eggs on trees that already shelter caterpillars, and so to occupy the niche longer and exploit Cecropia resources before colonization by ants. However, once incipient ant colonies are able to develop, they prevent further colonization by the caterpillars. Although no higher herbivory rates were noted, these caterpillars are ineffective in protecting their host trees from a pathogenic fungus, Fusarium moniliforme (Deuteromycetes), that develops on the trichilium in the absence of mutualistic ants. Therefore, the Cecropia treelets can be parasitized by two often overlooked species: the caterpillars that shelter in the domatia and feed on FBs, delaying colonization by mutualistic ants, and the fungal pathogen that develops on old trichilia. The cost of greater FB production plus the presence of the pathogenic fungus likely affect tree growth.

Show MeSH
Related in: MedlinePlus