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Especies de produccin especficos del cuerpo Mlleriano y defensas anti-herbvoro en el mutualismo Azteca-Cecropia
Species specific Mllerian body production and anti-herbivore defense in the Azteca- Cecropia mutualism
In Monteverde Costa Rica there are five species of Azteca (Formicidae) that inhabit Cecropia (Cecropiaceae) in a facultative ant-plant mutualism (Longino 1989). Azteca provide Cecropia protection from herbivory while Cecropia provide a home for Azteca in trunk internodes as well as glycogen and
protein-rich Mllerian bodies (Janzen 1973). Because some Azteca show more aggressive behavior when Cecropia is disturbed (Longino 1996), it would be expected that their host Cecropia would suffer lower herbivory than Cecropia inhabited by less aggressive Azteca. In this study, herbivory and Mllerian body production were examined in Cecropia with their Azteca mutualists. Although correlations between Azteca
species and herbivory and Mllerian body production were not found to be statistically significant, the trends shown by the data indicate that the differential production does indeed occur in that Cecropia with lower herbivory produce comparatively more Mllerian bodies than Cecropia that have received more herbivory The data presented in this study indicate niche partitioning wherein Azteca that are more heavily invested in Cecropia protection are rewarded in higher Mllerian body production on the host Cecropia.
En este estudio, examin el nivel de herbivora y la produccin de los cuerpos Mllerianos examinados en Cecropia con sus mutualistas azteca.
Text in English.
Tropical Ecology 2007
Mllerian body production
Ecologa Tropical 2007
Produccin del cuerpo Mulleriano
t Monteverde Institute : Tropical Ecology
1 Species specific MÂŸllerian body production and anti herbivore defense in the Azteca Cecropia mutualism Eric Lawyer Department of Biology, University of Oregon Abstract In Monteverde Costa Rica there are five species of Azteca (Formicidae) that inhabit Cecropia (Cecropiaceae) in a facultative ant plant mutualism (Longino 1989). Azteca provide Cecropia protection from herbivory while Cecropia provide a home for Azteca in trunk internodes as well as glycogen and protein rich MÂŸllerian bodies (Janzen 1973). Because some Azteca show more aggressive behavior when Cecropia is disturbed (Longino 1996), it would be expected that their host Cecropia would suffer lower herbivory than Cecropia inhabited by less aggressive Azteca In this study, herbivory and MÂŸlleri an body production were examined in Cecropia with their Azteca mutualists. Although correlations between Azteca species and herbivory and MÂŸllerian body production were not found to be statistically significant, the trends shown by the data indicate that t he differential production does indeed occur in that Cecropia with lower herbivory produce comparatively more MÂŸllerian bodies than Cecropia that have received more herbivory The data presented in this study indicate niche partitioning wherein Azteca tha t are more heavily invested in Cecropia protection are rewarded in higher MÂŸllerian body production on the host Cecropia Resumen En Monteverde Costa Rica hay cinco especies de Azteca (Formicidae) que vive con la especie Cecropia ( Cecropia ceae) en un relaciÂ—n mutualtica (Longino 1989). Las especies de Azteca dan protecciÂ—n a las especies de Cecropia de herbivoro mientras la especie Cecropia hogar a la especie por Azteca en el tronco y los cuerpos MÂŸllerianos que tienen glicogenia y proteÂ’na. Algunas es pecies de Azteca tienen un comportamiento mÂ‡s agresivo que otros y es probable que las especies de Cecropia con las especies de Azteca mÂ‡s agresivo tendrÂ’a menos herbivoro que Cecropia con Azteca menos agresivo (Longino 1996). En este estudio, examinÂŽ el n ivel de herboro y la pruducciÂ—n de cuerpos MÂŸllerianos examinÂ’a en Cecropia con Azteca Aunque los correlociÂ—nes entre Azteca especies y herbivoro y la producciÂ—n de cuerpos MÂŸllerian no eran estadisticamente significativas, las tendencias muestran que las especies Cecropia producen mÂ‡s cuerpos MÂŸllerian cuando hay menos herbivoros. Los datos en este estudio muestran un divisiÂ—n del nicho, las especies Azteca que tiene mÂ‡s inversiÂ—n en las especies de Cecropia recibe mÂ‡s cuerpos MÂŸllerianos de parte de la e specie de Cecropia hospedera. Introduction In the Neotropics, one of the most conspicuous ant plant mutualisms is Cecropia ( Cecropia ceae) and the Azteca ant genus. Azteca queens colonize Cecropia saplings by chewing a hole through the thin prostoma wh ich allows them access to the hollow
2 domatia in the trunk (Janzen 1973). Before they ever forage, queens raise a brood of workers who emerge through the previously made prostoma (Longino 1989). The young workers quickly forage for MÂŸllerian bodies, glycoge n and protein rich food sources produced by the Cecropia which project from the trichilum, a fuzzy pad at the base of the petiole (Rickson 1977, Janzen 1973). In this mutualism, Azteca provide Cecropia protection from herbivory while being supplied with a food source and a home in the internodes. Of the hundreds of species of Azteca ants in Costa Rica there are five that are mutualistic with 3 species of Cecropia : C. peltata C. obtusifolia and C. insignis in the Monteverde area (Longino 1989). Queens hav e been found to unsuccessfully colonize a fourth species, C. polyphlebia This species of Cecropia inhabit a hybrid zone above 1400m, where long hairs cover and obscure trichilia (Longino 2000). The five obligate Azteca mutualists inhabit well defined elev ational gradients. There is an almost clear elevational boundary separating the A. muelleri complex comprised of A. xanthochroa and A. constructor and the A. alfari complex of A. alfari and A. ovaticeps complexes. These complexes are morphologically and be haviorally similar species that occupy almost the same feeding niche, elevational ranges, and habitat types (Longino 1989, Mazzei 2003). Their coexistence is perplexing and there has been little examination of this phenomenon. Azteca muelleri complex is ty pically found between 1100 and 1400m and typically shows more aggressive behavior when Cecropia has been disturbed (Mazzei 2003, Longino 1996). Azteca alfari complex inhabit a range of 900 1100m and are more docile even when Cecropia has induced great leaf damage (Mazzei 2003, Lonino 1996). The fifth, A. coruleipennis is abundant in typically lower Pacific Dry Forests of Costa Rica. Azteca coruleipennis exhibits protective behavior much more similar to A. muelleri than that of A. alfari (Longino 1997). Ther e has been no record of these Azteca inhabiting habitats other than the aforementioned Cecropia (Longino 1989). In Monteverde, these Azteca have been found to inhabit specific Cecropia (Longino 2000). Cecropia peltata are more common below 1000m in dry fo rests and commonly have A. alfari complex and A. coruleipennis colonies (Longino 2000). Cecropia obtusifolia are common between 1000 and 1400m and are typically inhabited by A. muelleri complex (Longino 2000). Cecropia insignis is typically found below 110 0m and is colonized by A. muelleri complex. Various hypotheses have been proposed as to reasons for host specificity in this mutualism. The light availability hypothesis proposes that A. alfari are better competitors in Cecropia saplings, but require high resource input such as in disturbed habitats or edges (Davidson and Fisher 1991). According to this hypothesis, A. muelleri would be better suited to more mature trees in closed habitats (Davidson and Fisher 1991). Longino has proposed a disturbance hypo thesis that may be co occuring with the light availability hypothesis proposed (1991). According to this hypothesis, A. alfari complex, the better competitors in saplings, would be more successful in disturbed habitats. Because of the poor defenses offered by the A. alfari complex, their host Cecropia would be less successful, while that of A. muelleri complex be better suited to grow to maturity (Longino 1991). Although A. muelleri complex may be at a competitive disadvantage in colonizing Cecropia at the sapling stage, they are able to produce more colonizing queens because of the longer lives of their host Cecropia (Lonino 2000). There is little literature hypothesizing the reasons for host specificity and ranges of A. coruleipennis
3 Azteca are an effect ive defense against herbivory and are a substantial investment for Cecropia (Bronstein 1998). In fact, Azteca have been shown to recruit workers to defend leaves when leaf damage has occurred (Agrawal 1998). Greater numbers of Azteca are directly correlate d to lower residence time of herbivores on leaves, leading to reduced herbivory (Bronstein 1998). Between the Azteca mutualists, A. muelleri and A. alfari complex show the most noticeable differences in behavior while A. coruleipennis exhibits protective behavior observed to be closer to that of A. muelleri comlex (Longino 1996). In the mutualism displayed between these species of Azteca and Cecropia stronger mutualistic behavior (e.g. protection from herbivory) could be reciprocated by stronger mutualist ic behavior by the host tree in the form of higher MÂŸllerian body production. Niche partitioning theory could explain the ranges and host specificity of Azteca in that more competitively fit Azteca inhabit Cecropia that produce greater amounts of MÂŸllerian bodies. It is difficult to predict wether more comptetively fit Azteca inhabit Cecropia with proportionally higher MÂŸllerian body production through niche partitioning or if there is an induced response by the Cecropia wherein reduced herbivory allows the tree to invest in greater production of MÂŸllerian bodies. Overall, I expected to find that lower herbivory induces greater MÂŸllerian body production because this rewards greater protection from the Azteca in the Cecropia Azteca mutualism. Methods Herb ivory, MÂŸllerian body production, height, DBH, and elevation were measured for 58 Cecropia in Cerro Plano, Monteverde, and the San Luis valley in Monteverde, Costa Rica from 950 1400m altitude. Percent herbivory was measured by cutting the lowest green lea f of the Cecropia with pruning shears and laying the leaf against a transparent grid with 1cm 2 squares. All squares with over 50% missing area were counted. In order to measure MÂŸllerian body production, the Azteca had to be isolated from the trichilia. Th is was accomplished by brushing the adhesive Tanglefoot around the trichilia. One trichilium was studied per tree, and the highest trichilium of each tree was studied. The trees were checked after two days and the number of visible MÂŸllerian bodies counted Height and DBH were measured to examine if the Cecropia followed the light availability and disturbance hypothesis (Davidson and Fisher 1991, Longino 1991). Height was either measured by simply measuring the base to top with a tape measure, or calculated with the help of a clinometer. DBH measured with a tape measure. A Casio Pro 2147 altimeter watch was used to measure elevation. The regions with the highest number of Cecropia sampled were the Santuario Ecologica in Cerro Plano, the upper San Luis Rive r, and a farm owned by Victor Jiminez in lower San Luis. Initially, habitat type was noted as to wether the Cecropia were inhabiting an open or closed habitat. Because all the Cecropia examined were in disturbed open habitats, this was not a condition exam ined statistically. Ants were captured by simply brushing them with a leaf or twig into an isopropyl alcohol filled vial. Ants were identified to species complexes in the case of A. muelleri and A. alfari complexes, and to species in the case of A. corulei pennis Because both Azteca complexes exhibit similar protective behavior and inhabit the same elevational range and
4 Cecropia species, they were treated as one species in this study. Azteca identification was accomplished through the use of an online ident ification guide and photographs by Jack Longino (Longino 1997). The easiest defining characteristics of the Azteca were the presence or absence of conspicuous setae on scapes and tibia (Longino 1997). In order to see the setae, the ants were first dried by allowing them to sit under the lights of a dissecting scope for several minutes. Cecropia species were identified by a field guide and drawings by Jack Longino (Haber et al 2000, Longino 1997). Results Azteca muelleri complex, A. alfari complex, and A coruleipennis all showed significantly defined altitudinal ranges. Azteca muelleri complex inhabiting an average of 1224m, A. alfari inhabiting 987m on average, and A. coruleipennis inhabiting 974m on average (Figure 1. ANOVA F = 48.3843 df = 45 p = <0.0 001). A ratio was taken comparing leaf size to measure herbivory. There was no significant correlation between herbivory and Azteca species (ANOVA F = 0.1875 df = 38 p = 0.8298). Also, no significant correlation was found for Azteca species and number of M ÂŸllerian bodies produced on the trees that they inhabited (ANOVA F = 2.9363 df = 36 p = 0.0659). MÂŸllerian body production and Cecropia species was not statistically correlated (ANOVA F = 3.0171 df = 38 p = 0.0608). Data showed no significant correlation b etween the MÂŸllerian body production and herbivory (Linear regression R 2 = 0.053568 p = 0.1261 n = 44). A chi square goodness of fit test correlating Azteca species with Cecropia species was highly significant in that it showed host plant relationship ( 2 < .001). Azteca muelleri complex showed highest host specificity with C. obtusifolia A. alfari complex and A. coruleipennis was most commonly found on C. peltata.
5 A. alfari A. coruleipennis A. muelleri Figure 1. Elevational ra nges of A. alfari, A. coruleipennis, and A. muelleri. The ranges are congruent with recent examinations of Monteverde Azteca species (Mazzei 2003). Smaller sample size is attributed to more limited representations of range. Figure 2. Her bivory of host Cecropia leaves corresponding to Azteca species in Monteverde. The percentage of herbivory of host Cecropia of leaves was the lowest in the trees inhabited by A. muelleri complex (0.017862) which suggests the greatest protection from herbivo ry. Azteca coruleipennis complex showed the second best defense against herbivory (0.022324) while. Azteca alfari showed the worst protection from herbivory (0.022026). The results are statistically insignificant (p = 0.8298). Standard error bars are shown 0 0.005 0.01 0.015 0.02 0.025 0.03 0.035 A. muelleri A. alfari A. coruleipennis Azteca species Mean Herbivory Percentage
6 Figure 3. Mean MÂŸllerian body production by Cecropia in trees inhabited by A. alfari A. coruleipennis and A. muelleri This is a measure of the average MÂŸllerian bodies produced in host Cecropia for each of the Azteca species. Azteca muelleri co mplex inhabited Cecropia show considerably higher mean MÂŸllerian body production (110.75) than that of both A. alfari complex (60.077) and A. coruleipennis (58.2). Standard error bars are shown. 0 20 40 60 80 100 120 140 A. alfari A. coruleipennis A. muelleri Azteca species Mean MÂŸllerian Body Production
7 0 0.02 0.04 0.06 0.08 0.1 0.12 0.0000 100.0000 200.0000 300.0000 400.0000 MÂŸllerian Body Production Herbivory Figure 4. MÂŸllerian body produ ction and the herbivory for all the Cecropia samples. A regression analysis was used for the correlation. Although a clear trend is visible the data is insignificant (p = 0.1261). Discussion Protection from herbivory was not significantly correlated to Azteca species. However, a trend is visible in that the host Cecropia of A. muelleri complex showed lower hervivory than the other Azteca examined (Figure 2). Surprisingly, host Cecropia of A. alfari complex showed lower herbivory than that of Cecropia inhabited by the more aggressive A. coruleipennis Another comparison with interesting trends is the comparison of MÂŸllerian body production on host Cecropia for the Azteca species studied. Cecropia inhabited by A. muelleri complex showed considerably high er MÂŸllerian body production. Cecropia inhabited by Azteca alfari complex and A. coruleipennis showed nearly identical MÂŸllerian body production. Figure 4 showed a clear trend between reduced MÂŸllerian body production with higher herbivory. This may either show niche partitioning in that more aggressive Azteca are inhabiting Cecropia that offer a higher reward or that more aggressive Azteca allow Cecropia to be healthier and thus produce greater amounts of Muellerian bodies. Both hypotheses are not exclusiv e and may be ocurring at the same time. No correlation was found between height and DBH of Cecropia samples and Azteca inhabitance (p = 0.4528 and p = 0.6216, respectively). Although A. muelleri complex has been found to become more well established in l ow light growing mature trees, and A. alfari in Cecropia saplings in disturbed areas, there was no significant
8 pattern to the size of tree and its resulting Azteca population (Longino 2000). This is most likely attributed to the sampling of smaller and mor e manageable Cecropia Although there is some overlap in elevational ranges and host Cecropia species, Azteca species can be expected to inhabit certain Cecropia at certain elevations more than others (Longino 2000). Results from this study clearly show i nherent host specificity between Azteca and Cecropia This can be explained by the light availability hypothesis which proposes that A. muelleri complex are more successful in establishing Cecropia in relatively closed or secondary forests (Longino 2000). Azteca alfari and A. coruleipennis were found more typically in Cecropia species that become established in disturbed areas with high light availability ( C. peltata ). Because Cecropia in closed habitats are typically more mature, they could not be examined in this study. Smaller Cecropia and saplings were sampled because I needed to be able to reach the trichilia at the top of the tree. The study of Cecropia in habitats of varying light availability would be open for future study and could lend more support to the light availability hypothesis. Production of the glycogen and protein rich MÂŸllerian bodies is costly for Cecropia (Folgarait 1994). This implies a great investment taken by the Cecropia in recruiting the Azteca for protection. Because of this, th e results from this study indicate what would be expected by Cecropia maximizing its survival and minimizing the energetic cost (Fig 4). It would not make evolutionary sense for Cecropia to provide greater rewards that are energetically expensive despite i nferior protection offered by their mutualist. In fact, Cecropia have been found to lose trichilia completely in the absence of mutualistic ants, in that its typically velvety texture is overrun with firm hairs (Janzen 1973, Rickson 1977). Merely providing the domatia and MÂŸllerian bodies for Azteca has a higher energetic cost than producing secondary compounds in the leaves (Davidson and Fisher 1991). With this in mind, Cecropia are invested highly in their mutualism with Azteca It is clear that Cecropia are able to respond directly to variation in herbivory. MÂŸllerian body production was not correlated to specific Cecropia. This further lends support to the hypothesis that MÂŸllerian body production is related to levels of herbivory. What may be unclear is wether this is an induced response to the protection the Azteca provide or if MÂŸllerian body production is correlated to the health of the tree. Acknowledgements First and foremost I would like to thank Alan and Karen Masters for their dedication to a n amazing educational experience. Thanks to Camryn Pennington for her patience and advice on any problems I encountered. I would also like to thank Tom McFarland for always being available for help no matter the hour or circumstance. I would like to thank the Santuario EcolÂ—gica for allowing me free entry to their land as well as Victor Jimenez for letting me study the many Cecropia growing on his farm. Literature Cited Agrawal A.A., Dubin Thaler, B.J. 1998. "Induced Responses to Herbivory in the Neotr opical Ant Plant Association Between Azteca ants to Cecropia Trees: Response of Ants to Potential Inducing Cues" Behavioral Ecological Sociobiology 45. 47 54. Bronstein J.L. 1998. "The Contribution of Ant Plant Protection Studies to Our Understanding of Mutualism" Biotropica 30(2) 150 161.
9 Davidson, DW and Fisher BL. 1991. "Symbiosis of ants with Cecropia as a function of light regime" in Huxley CR and Cutler DF. Ant Plant Interactions Oxford University Press, Oxford, pp 289 309. Folgarait, P.J., H.L. Johnson, D.W. Davidson. 1994. "Responses of Cecropia to Experimental Removal of Mullerian bodies" Functional Ecology Vol 8, No. 1. 22 28 Haber, W.A., W. Zuchowski, and E. Bello. 2000. An Introduction To Cloud Forest Trees, Monteverde, Costa Rica Mou ntain Gem Publications, Monteverde de Puntarenas, Costa Rica Janzen, DH. 1973. "Dissolution of Mutualism between Cecropia and Its Azteca Ants" Biotropica 5(1): 15 28. Longino, John T. 1989. "Geographic Variation and Community Structure in an Ant Plant M utualism: Azteca and Cecropia in Costa Rica" Biotropica 21(2) 126 132. Longino, John T. 1991. Azteca ants in Cecropia trees: taxonomy, colony structure, and behavior." Pgs. 271 288 in C. Huxley and D. Cutler. Ant Plant Interactions. Oxford University Press, Oxford. Longino, John. 1997. www.evergreen.edu/ Azteca Longino, John T. in N Adkarni, Nalini M., and N.T. Wheelwright. 2000. Monteverde: Ecology and Conservation of a Tropical Cloud Forest. Oxford University Press, New York. Mazzei, P. 2003. CI EE Fall 2003 Tropical Ecology & Conservation Rickson, F.R. 1977. "Progressive Loss of Ant Related Traits of Cecropia peltata on Selected Caribbean Islands" American Journal of Botany 64(5) 585 592