Rare species advantage against herbivory among epiphyte Peperomia spp. Piperaceae Nichole M. Tiernan Department of Biology, University of Connecticut ABSTRACT Herbivory is often a greater problem for tropical plants than for temperate plants. With higher herbivore pressures, tropical plants have more defense mechanisms than temperate plants. This drives host specialization and helps to explain why the tropics are so diverse. One premise that attempts to explain how the tropics can be so diverse i s the rare species advantage. Two theories that help to explain the rare species advantage are those of density dependence and frequency dependence. The purpose of this study is to see if there is density or frequency dependent herbivory in species of th e epiphytic genus Peperomia . By looking at herbivory rates of Peperomia in Monteverde, Costa Rica, this study has deduced that mean percent abundance is positively correlated with percent herbivory p = 0.008 and thus suggests that density dependency is an active theory in tropical forests. Frequency dependence however was non significant when correlated with mean percent herbivory p = 0.181. The rare species advantage has important implications for the maintenance of biodiversity as it drives speciat ion and helps keep host plants genetically and morphologically varied. Density dependence offers an explanation as to why Peperomia is such a species diverse genus in Monteverde. RESUMEN La herbivorÃa es a menudo un problema mayor para plantas tropica les que para plantas de clima templado. Las plantas tropicales tienen mÃ¡s mecanismos de defensa que las plantas de climas templados ya que la presiÃ³n de los herbÃvoros es mayor; impulsa a la especializaciÃ³n del anfitriÃ³n y ayuda a explicar por quÃ© los trÃ³ picos son tan diversos. Una premisa que procura explicar cÃ³mo los trÃ³picos pueden ser tan diversos es la ventaja de las especies poco comunes. Dos teorÃas que ayudan a explicar la ventaja de las especies poco comunes son las de dependencia de densidad y d e dependencia de frecuencia. El propÃ³sito de este estudio fue determinar si la herbivorÃa en las especies del gÃ©nero epifÃtico Peperomia dependen de la densidad o de la frecuencia. Este estudio concluyÃ³, utilizando las tasas de herbivorÃa en Peperomia en Monteverde Costa Rica, que el porcentaje de abundancia promedio se correlaciona positivamente con el porcentaje de herbivorÃa p = 0.008, y por lo tanto sugiriÃ³ que la dependencia de densidad es una teorÃa activa en bosques tropicales. La dependencia d e la frecuencia, sin embargo, no fue significativa cuando se correlacionÃ³ con el porcentaje promedio de herbivorÃa p = 0.181.. La ventaja de las especies poco co munes tiene implicaciones importantes para la conservaciÃ³n de la biodiversidad ya que impu lsa la especiaciÃ³n y ayuda a mantener a las plantas anfitrionas genÃ©tica y morfolÃ³gicamente diversas. La dependencia de la densidad ofrece una explicaciÃ³n del porquÃ© el gÃ©nero Peperomia es tan diverso en especies en Monteverde. INTRODUCTION Herbivory i s a major problem for plants in tropical forests. Herbivores eat 14.9% of leaf material, and they can damage a plant in many other ways. Eating shoot tips from the terminal axis and the rolling of leaves are both very harmful to a plant Janzen 1983. In
addition, seedling survival is hindered, and recruitment is greatly reduced when herbivores eat seed material Janzen 1983. Tropical forests experience more herbivore damage than temperate forests. High herbivore pressures provide a reasonable explanat ion for these patterns. This is a logical suggestion because tropical plants are slow growers and therefore spend more time as seeds, seedlings, and saplings, which is a very vulnerable state for a plant. Tropical plants also sustain herbivores with thei r year round supply of leaves. As a result of high herbivory in the tropics, tropical plants have more advanced defense mechanisms than temperate plants Coley and Aide, 1991. This has allowed more plant animal co evolution, and most importantly, host s pecificity. Many insect herbivores are host specific. Plant defenses are evolutionary significant in the co evolution of host specificity. Host specificity among tropical plants and their herbivores is one of the factors that need to be present in orde r for herbivory to promote species co existence. Another contingency is that herbivores must favor common species of plants. In order for an herbivore to attack a common species, the most rare species are managing to remain somewhat invisible. Therefore , the abundance of a species may be related to herbivory rates Coley 1983 Janzen 1970 develops density dependence theory based on the idea that many herbivores are host specific. He looks at how seeds fall close to the host tree, forming a ring aroun d the tree. Herbivores then single out these common seeds for a food source, and in turn, have a negative effect on the host tree s population recruitment. The relationship between the herbivores and their food source is reliant on density dependence. A nother way to evaluate the rare species advantage is through frequency dependency. Frequency dependency does not take into account area, but rather only looks at the number of times a species appears. A study, done by Wills et al. 2006 on tropical fore sts in Barro Colorado Island, Panama, determined that frequency dependency theory is one of the main components contributing to tropical forest diversity. This has important implications for the maintenance of biodiversity. The epiphyte Peperomia Piperac eae is a species rich genus, containing 43 species in Monteverde Haber 2000. It is also a poorly known genus, so how co existence occurs remains mysterious. It is in the same family as Piper, in which herbivory is well studied. A study done by Marquis 1991 concluded that two common Piper herbivores, weevils and geometrid moths, have highly variable host specificity within the genus Piper. Thus, Peperomia may be hosts to their own specialist fauna. This study asks whether Peperomia experiences rare species advantage, due to frequency or density dependent herbivory. This study can thus provide insights into the role of herbivore pressures in maintaining the high species richness of this genus in Monteverde. It may also provide further evidence for t he role of species interactions in promoting co existence. MATERIALS AND METHODS This study was done on the Pacific slope of the cloud forest of Monteverde, Costa Rica from April 10 April 30, 2006, on the banks of the Quebrada MÃ¡quina, between 1500 to 1600 m. twenty rocks harboring Peperomia , were examined. Peperomia individuals were identified to morphospecies, and with the help of botanist, Willow Zuchowski, four
species were identified as, P. deppeana, P. angustata, P. costaricensis, and P. hernandi iafolia. The other four were assigned number identifications Appendix A. The twenty rocks each harbored between one and seven species of Peperomia. Sometimes there was more than one patch of a similar species on a rock, measurements were taken for eac h patch, and later combined. For each patch of Peperomia the circumference was measured with a measuring tape. Choosing Leaves for Study A sample of ten leaves was collected from each patch of Peperomia . Leaves from each of the cardinal directions wer e sampled to obtain leaves from all parts of the patch. No terminal leaves were sampled so that young leaves, which may not have defense compounds yet, were avoided Coley 1983. Each site was labeled with flagging tape to prevent repeat samplings. Qua ntifying Plant Size and Percent Herbivory In the lab, each leaf was placed on a two millimeter by two millimeter grid and the number of blocks with leaf present was documented. Then the outside edge of the leaf was estimated and a count was made of the nu mber of grids missing from herbivory. Leaf damage considered for herbivore damage included holes that took up at least half of a square, and missing edges assumed to be caused by insects. Herbivory was measured for a total of 310 leaves. Calculations of Average Herbivory and Frequency of Occurrence Percent herbivory was calculated for each of the eight species as a percent of the ratio for each leaf. The mean was taken of any species occurring in more than one patch on a rock, and then a total mean wa s taken for each species. Percent abundance and frequency of occurrence were then calculated across the eight species. A spearman rank correlation test was used with percent herbivory as the independent variable, and mean percent abundance and frequency each as dependent variables. RESULTS A total of 310 leaves were sampled from 20 rocks. The total number of Peperomia species sampled was eight. The Spearman rank correlation test showed that the relationship between average percent herbivory and fre quency of occurrence is non significant Figure 1.
y = -0.0555x + 6.0671 R 2 = 0.0021 2 3 4 5 6 7 8 9 0 2 4 6 8 frequency mean percent herbivory Figure 1: Mean percent herbivory across the eight species of Peperomia is compared with frequency of occurrence across the eight species of Peperomia . The correlation is stati stically non significant. rho = 0.5, p = 0.181, n = 8. As the Peperomia species occur more often, or become more frequent there is no change in herbivory. However, the correlation between percent herbivory and percent abundance is significant Figure 2. This shows that as herbivory increases, the abundance is increasing as well. Meaning, that as a species becomes denser, covering more area, herbivores are eating more.
y = 3.8779x + 5.2788 R 2 = 0.136 2 3 4 5 6 7 8 9 0 0.1 0.2 0.3 0.4 0.5 percent abundance mean percent herbivory Figure 2: Effect of relative abundance on percent h erbivory. The correlation is statistically significant rho = 1.0, p = 0.008, n = 8. As abundance, or area, of Peperomia increases, herbivory does as well. DISCUSSION The findings assess both frequency dependence and density dependence in relation to mean percent herbivory. This study shows that density dependence is present between Peperomia and its herbivores, but that frequency dependence is absent. Percent abundance looks at the amount of area covered by one species of Peperomia in relation to t he total area covered by all species of Peperomia. Frequency dependence only looks at the number of times a species of Peperomia occurred, and not at the area covered. The positive correlation between mean percent herbivory and percent abundance demonstr ates the rare species advantage. Common species cover more area with density dependence, and in turn are targeted by herbivores. However, it must be noted that this correlation does not necessarily imply cause and effect Ambrose and Ambrose 1987. The correlation simply shows a positive trend that where there is a higher density, there is usually a higher herbivory rate. Likely herbivores to Peperomia are those that are specific to Piper , possibly weevils and geometrid moths. These herbivores are mos t likely feeding on the Peperomia that is most abundant, although future studies are needed to determine whether they are host specific herbivores, or generalist herbivores. Peperomia is also very abundant on trees in addition to rocks, and I observed the communities to be very similar in their assembly. The rocks seemed to be as tightly packed, and with the same
average number of species as the trees were. Therefore, a safe conclusion is that herbivores to Peperomia are offered the same choices on rocks as well as on trees. The rare species advantage is important to tropical biodiversity. Density dependence can affect migration in addition to birth and death rates. This offers an explanation for why certain plants survive, while others are phased out Hubbell 1990. This is important to the composition of tropical forests. As long as herbivores keep favoring common species, and rare species are allowed to grow to the status of a common species, a cycle of diversity will perpetuate. The natural selec tion of density dependency helps to maintain physical and genetic differences among host species and in the long run drives speciation Wills 2006. This is important to Peperomia because density dependence offers an explanation as to why the genus is so species rich while being so evidently similar ecologically. ACKNOWLEDGMENTS I would like to thank Maria Jost, and Ollie Hymen for their willingness to help with everything, and at all times. I would also like to thank Karen Masters for troubleshooting in the beginning and helping me find the perfect project, and then for advising me to the end. Thanks to Javier Mendez for the help with stats and the translation of my resumen, and to Willow Zuchowski for help in identifying my plants. Thanks to Kristen Becklund and Caroline Farrior for revising my first draft. Lastly, I would like to thank Alan Masters for his guidance and advice from the beginning. Thanks also to the EstaciÃ³n BiolÃ³gica for the beautiful forest to work in. LITERATURE CITED Ambrose, H . W., K. P. Ambrose. 1987. A Handbook of Biological Investigation . Hunter Textbooks, Inc., North Carolina, p 39. Coley, P. 1983. Herbivory and Defensive Characteristics of Tree Species in a Lowland Tropical Forest. Ecological Monographs 53 :209 233. Coley, P. and T. M. Aide. 1991. Comparison of Herbivory and Plant Defenses in Temperate and Tropical Broad Leaved Forests. In: Plant Animal Interactions: Evolutionary Ecology in Tropical and Temperate Regions . ed. Peter Price et al. John Wiley and Sons, New York, pp. 125 49 Haber, H. A. 2000. Vascular Plants of Monteverde. In: Monteverde: Ecology and Conservation of a Tropical Cloud Forest . Ed. Nadkarni, N. M. and Wheelwright, N. T. Oxford University Press, New York, pp. 489 490. Hubbell, S. P. et al. 1990. Presence and absence of density dependence in a neotropical tree community. Philosophical Transactions of the Royal Society of London 330 : 269 281.. Janzen, D. H. 1970. Herbivores and the number of tree species in tropical forests. The Ame rican Naturalist 940 501 507. Janzen, D H. 1983. Food webs: Who eats what, why, how, and with what effects in a tropical forest? Pp. 167 82 in Tropical rain forest ecosystems . Ed. F.B. Golley. New York: Elsevier Scientific.
Marquis, R. J. 1991. H erbivore Fauna of Piper Piperaceae in a Costa Rican Wet Forest: Diversity, Specificity, and Impact. In: Plant Animal Interactions: Evolutionary Ecology in Tropical and Temperate Regions . ed. Peter Price et al. John Wiley and Sons, New York, pp. 179 196. Wills, C. et al., 2006. Nonrandom processes maintain diversity in tropical forests. Science 311 :527 532.
APPENDIX A : Taxonomy of the eight species of Peperomia Peperomia deppeana Peperomia angustata Morpho Species #2 Peperomia costaricensis
Morpho Species #5 Peperomia hernand iiafolia Morpho Species #6 Morpho Species #8
APPENDIX B % Mean Herbivory, Freq uency of Occurrence, and % Mean Abundance across the Eight Species of Peperomia Species % Mean Herbivory Frequency of occurrence % Mean Abundance P. deppeana 6.69 6 0.38 Morpho #2 3.54 5 0.18 P. angustata 7.21 3 0.34 P. costaricensis 4.44 4 0.05 Mo rpho #5 4.70 3 0.05 Morpho #6 1.79 4 0.03 P. hernandiiafolia 7.95 4 0.15 Morpho #8 5.73 2 0.00