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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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Host successional patterns for Cecropia treelets.Host successional patterns for each Cecropia sapling monitored during the 3-year survey on the dirt road near the Montagne des singes. Dashes correspond to trees sheltering both caterpillars and A. alfari. Trees were grouped to ensure the legibility of the figure, and so do not correspond to their geographic distribution.
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pone-0020538-g003: Host successional patterns for Cecropia treelets.Host successional patterns for each Cecropia sapling monitored during the 3-year survey on the dirt road near the Montagne des singes. Dashes correspond to trees sheltering both caterpillars and A. alfari. Trees were grouped to ensure the legibility of the figure, and so do not correspond to their geographic distribution.

Mentions: Out of the 610 C. obtusa saplings studied near the Petit Saut dam, only 349 (57.2%) sheltered A. alfari or A. ovaticeps colonies. Among the others, 178 (29.2%) were totally unoccupied, while the remaining 83 (13.6%) sheltered three to six P. guianalis caterpillars at different larval stages (Fig. S1c). For the 64 C. obtusa surveyed during 3 years near the Montagne des singes, at the start of the survey the percentage of C. obtusa sheltering P. guianalis caterpillars was by far superior (39.1% or 25 trees out of 64; Fig. 3), illustrating that there are variations between areas. When present, caterpillars were also more numerous with some trees sheltering up to 12 caterpillars. Saplings were also associated with the two Cecropia-ant species typical of the area, A. alfari and A. ovaticeps, as well as, unexpectedly, the fire ant Solenopsis saevissima (tree N°7). Also, six trees were unoccupied at the start of the survey, and three of the 25 saplings bearing caterpillars were also occupied by A. alfari (trees N° 24, 43 and 52). This dual hosting was also observed later in the survey for two additional trees (trees N° 14 and 41), but after a few months, all five trees were occupied only by Azteca colonies. Note that, in the end, tree N° 52 was colonized by A. ovaticeps. Over the course of the different surveys, unoccupied trees were colonized by caterpillars (four cases) or directly by Azteca ants (trees N° 19 and 25). Although S. saevissima workers exploited the FBs and were aggressive towards flying insects landing on their host tree foliage, tree N°7 was colonized in the end by caterpillars (Fig. 3). While the two Azteca species occupied more and more trees over time, the number of trees sheltering P. guianalis caterpillars first increased and then decreased. They were replaced by A. alfari or A. ovaticeps colonies on 15 and 10 trees, respectively. At the end of the experiment-so 3 years after the beginning of the survey-six trees still sheltered caterpillars. During this entire lapse of time, the trees occupied by A. alfari or A. ovaticeps were never colonized by caterpillars. In July 2009, four Cecropia trees still sheltered caterpillars.


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

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

Host successional patterns for Cecropia treelets.Host successional patterns for each Cecropia sapling monitored during the 3-year survey on the dirt road near the Montagne des singes. Dashes correspond to trees sheltering both caterpillars and A. alfari. Trees were grouped to ensure the legibility of the figure, and so do not correspond to their geographic distribution.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0020538-g003: Host successional patterns for Cecropia treelets.Host successional patterns for each Cecropia sapling monitored during the 3-year survey on the dirt road near the Montagne des singes. Dashes correspond to trees sheltering both caterpillars and A. alfari. Trees were grouped to ensure the legibility of the figure, and so do not correspond to their geographic distribution.
Mentions: Out of the 610 C. obtusa saplings studied near the Petit Saut dam, only 349 (57.2%) sheltered A. alfari or A. ovaticeps colonies. Among the others, 178 (29.2%) were totally unoccupied, while the remaining 83 (13.6%) sheltered three to six P. guianalis caterpillars at different larval stages (Fig. S1c). For the 64 C. obtusa surveyed during 3 years near the Montagne des singes, at the start of the survey the percentage of C. obtusa sheltering P. guianalis caterpillars was by far superior (39.1% or 25 trees out of 64; Fig. 3), illustrating that there are variations between areas. When present, caterpillars were also more numerous with some trees sheltering up to 12 caterpillars. Saplings were also associated with the two Cecropia-ant species typical of the area, A. alfari and A. ovaticeps, as well as, unexpectedly, the fire ant Solenopsis saevissima (tree N°7). Also, six trees were unoccupied at the start of the survey, and three of the 25 saplings bearing caterpillars were also occupied by A. alfari (trees N° 24, 43 and 52). This dual hosting was also observed later in the survey for two additional trees (trees N° 14 and 41), but after a few months, all five trees were occupied only by Azteca colonies. Note that, in the end, tree N° 52 was colonized by A. ovaticeps. Over the course of the different surveys, unoccupied trees were colonized by caterpillars (four cases) or directly by Azteca ants (trees N° 19 and 25). Although S. saevissima workers exploited the FBs and were aggressive towards flying insects landing on their host tree foliage, tree N°7 was colonized in the end by caterpillars (Fig. 3). While the two Azteca species occupied more and more trees over time, the number of trees sheltering P. guianalis caterpillars first increased and then decreased. They were replaced by A. alfari or A. ovaticeps colonies on 15 and 10 trees, respectively. At the end of the experiment-so 3 years after the beginning of the survey-six trees still sheltered caterpillars. During this entire lapse of time, the trees occupied by A. alfari or A. ovaticeps were never colonized by caterpillars. In July 2009, four Cecropia trees still sheltered caterpillars.

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