1 Effect of Herbivory on Succession of Forest Light Gaps Toby Jacobs Department of Biology, James Madison University ABSTRACT Effects of herbivory have been seen to vary accord ing to the particular growth form of a plant and its habitat. The idea that these factors can interact to determine the nature of gap succession has been suggested but has not yet been thoroughly explored. Leaves of pioneer, understory, and canopy plants were collected and analyzed to quantify herbivory le vels on each growth form. Herbivory was found to be higher in gaps (p = 0 .0015) , and this was true to varying degre es with respect to growth forms and single families. Results suggest that herbivory is not the main factor influencing instantaneous or eventual gap composition, but it could interact with other effects like competition for light and water. The study also does not rule out the possibility that gap composition is random. RESUMEN Se ha observado que l os efectos de la herbivor Ã a cambian con la forma de crecimiento y e l hÃ¡ bitat de una planta. E l concepto de que estos factores pueden interactuar para determinar la esencia de la suces iÃ³ n en un clar o de l bosque ha sido sugerido , pero n o ha sido estudiado en detalle . L as hojas de las plantas pione ras, del sotobosque y del d osel fueron colectadas y analizadas para cuantificar los niveles de la herbivorÃ a en cada forma de crecimiento. MÃ¡ s herbivorÃ a oc ur r iÃ³ dentro de los claros del bosque (p = 0 .0015 ) y el efecto particular de esta pat roAn fue dif erente de acuerdo a la famili a taxonÃ³ mica y a la forma de crecimiento. Los resultados sugieren que la herbivorÃ a no es el factor mÃ¡ s importante influye ndo la sucesiÃ³ n en los clar os del bosque , pero p odrÃ a interactuar con otros factore s como la competencia por el agua y la luz. AdemÃ¡ s, este estudi o no puede eliminar la posibilidad de que la composiciÃ³ n en los clar os del bosque sea un proceso aleatorio . INTRODUCTION Forest light gaps are formed when one or more large trees and any attached lianas or vines fall, creating an opening in the vegetation from the canopy to the forest floor. Location and frequency of gaps are thought to represent a n unpredi ctable chance event (Denslow & Hartshorn 1994 ), but are an essential phenomenon for the survival of many species. Gaps open a new light source and cause a large amount of organic matter to fall to the ground (Denslow & Hartshorn 1994 ). T hese are the main benefits for plants that colonize these areas. All gaps are not created equal, and considerable variance is shown
2 based on the specific size and shape of the opened area (Denslow & Hartshorn 1994 ; Denslow et. al 1998) G aps generally feature more light (higher availability and intensity ) , higher soil moisture, and higher temperature s than continuous forest. However, only large gaps consiste ntly offer constant and available ligh t and greater soil nutrients (Denslow 1980 ) Light resources are also maximize d nearer the center of a gap (Denslow 1987 ). These extra resources over a large, open area produce a significant dynamic, and it has been sug gested that gaps are the most important element in creating and maintaining diversity in a tropical forest (Connell 1978). Most tropical trees are completely dependent on gaps at least at so me point in their life cycle (Denslow 1980 ); one study has sugges ted that up to 75% of tree s emerge from gap succession (Denslow 1987 ). Clearly , a closer unders tanding of this process is needed . Two major viewpo ints with respect to the nature of gap s uccession have recently emerged. These state that g ap composition depe nds either upon resource use and competition or, like gap formation, is a random process (Denslow 1980 ) . However, the complexity and scope of succession has caused its details to be vastly understudied to date (Denslow 1987 ). Some factors which have be en s uggested to induce competition and therefore determine composition include light, water, nutrients, and herbivory (Denslow 1987; Nadkarni et. al 2000 ). H erbivory is the only one of these effects that is not known to have a positive effect within gaps. Ther efore, it seems entirely plausible that this could be the limiting factor causing individuals to persist or senesce within a forest gap . Yet o nly a handful of studies have researched the amount and effect of herbivory in gaps versus continuous forest (Janz en 1995). Herbivory, mainly the result of folivory by insects, may be the sole factor in determining the outcome of a competitive interaction. This interaction involves competition over quality and abundance of defense mechanisms, which require sign ificant energy input by the plant. H abitat quali ty is largely responsible for the amount of energy a vailable to a plant, so it should also affect herbivory levels (Coley 1983 ). In addition to habitat, the life history of a plant is also significant with re spect to herbivory . Pioneers, in general, suffer higher herbivory than understory and canopy plants (Coley & Barone 1996 ). This seems to occur because pioneer plants focus more resources on growth than defense (Coley 1983, Brokaw 1983 ). Pioneers and all ot her life forms sustain greater levels of herbivory on their young leaves compared to those that are mature , up to 70% in some cases (Coley & Barone 1996, Brokaw 1983 ). This is because young leaves contain more water and are less tough, making them both mor e accessible and more nutritious to herbivores (Rundall & Gibson 1996) . There is some contention over how much defense is used in young versus mature leaves, but it is widely accepted that pioneers reduce defenses in their mature leaves as they toughen (Co ley & Barone 1996 ). Patterns of herbivory on pioneers also tend t o be variable from leaf to leaf; this is probably a result of c onstant leaf production, ensuring that young leaves are a lways present (Coley & Barone 1996 ). Persistent plant s, understory an d canopy trees , suffer a higher cost of herbivory in both young and mature leaves because of their relatively slow growth (Coley & Barone 1996 ). They flush a new set of leaves all at once instead of constantly producing new leaves. This is potentially used as a means of herbivore satiation (Brokaw 1983 ). They also may feature greater chemical defenses to protect their i nvestment in leaves (Rundall & Gibson 1996). Overall, leaves of these species are observed to be fairly evenly
3 damaged across various habita ts and suffer less herbivory than pioneers (Brokaw 1983 ). Thus, though understory plants are evolved to compete in a low light, low resource environment, they may also be effective gap competitors (Coley 1983). An understanding of various trends and fact ors, a major one potentially being herbivory, h as many ramifications for ecology and human activities. Many valuable timb er trees are understory species bene fit ing from small gaps (Denslow & Hartshorn 1994 ) and could represent new or sustainable sources of commercial wood (Vandermeer & Perfecto 1995). In addition, the process and eventual result of artificial forest regeneration depends entirely on gap processes and those that regulate them. The potentially large role of herbivory in this paradigm will have major consequences in each of these areas. This study sought to determine the effects of herbivory on gap composition through an analys is of the leaves of five plants, Melastomataceae (genus Centronia ) , a pioneer, Arecaceae (genus Chamaedorea ) , Pip eraceae (genus Piper ) , and Rubiaceae (genus Elaegia ) , understory plants, and Lauraceae (genus Stauranthus ) , a canopy plant. D ifferences in level of herbivory were then observed based on presence in a gap or continuous forest (non gap) environment and tree s ize. MATERIALS AND METHODS Research for this study was conducted in Monteverde, Costa Rica in tw o areas in a lower montane moist forest (1300 m elevation). Data were collected from November 5 through November 10, involving four full days in the field . A site of constant elevation was located approximately 200 meters west of the junc tion of the Caminata Nocturnal t rails with the nearest road (Fig. 1) continuous forest 500 meters further west represente defined as an area un shaded by canopy containing no trees more than 10 meters in height . I t seemed necessary to find a fallen tree or other evidence of natural gap formation in each considered area due to the proximity to hu man establishment . T he largest appropriate site (approximately 900 m 2 ) was subsequently selected for study. A preliminary census of the gap and continuous forest areas yielded five suitable families, representing the three different life forms (pioneer, understory, canopy), individuals of which could be found at each desired size : 0 1 m, 1 5 m, and 5 10 m . Individuals that were nearest the center of the gap and most exposed to direct sunlight were us ed . This, in conjunction with the large gap size, was de signed to maximize the apparentness of gap effects on observed trees. Each tree was then divided into vertical thirds (Fig. 2) and marked with flagging tape for sampling. From each third, the five most damaged leaves, five most intact leaves, and five mode rately damaged leaves were collected. This was largely done visually with quick measurements, involving no real quantitative analysis. Some trees, namely the 0 1 m Arecaceae and Rubiaceae, had fewer than 45 leaves, so all available leave s were taken and ad justed sample size was recorded . Thi s process was completed with a tree of each height of all five families in the gap area and in the continuous forest . Leaves were analyzed using an herbivory grid (1 square = 0 .262 cm 2 ) to measure the total leaf area, an d the total area removed by herbivory. Percent herbivory was calculated and was recorded along with leaf size. Data analysis relating herbivory, location, and tree size was conducted with several 2 way
4 ANOVA tests and a t test, and herbivory and leaf size were compared using a simple regression. RESULTS In a broad habitat analysis (Figure 2) , herbivory effects on gap species were shown to be significantly greater ( 2 way ANOVA , p = 0 .0015) than those on trees in continuous forest . An interaction analysi s of the independent effect on different families (life forms) sho wed significance, as well ( 2 way ANOVA, p < .001), but the interacting effect of family and location was not significant. This does not discount the fact that each variable involved in the i nteraction was significant when considered independently, but merely states that their association did not compound the se effects. S pecific re sults were then analyzed (Fig. 3) to determine herbivory effects on each family with respect to both size and lo cation. Arecaceae, an understory plant, showed no trends for either variable. The lone canopy tree, Lauraceae, showed significance for tree size ( 2 way ANOVA, p = 0 .027) but not for location. Melastomataceae, a pioneer plant, showed location to be highly s ignificant ( 2 way ANOVA, p = 0 .0018), but showed no effect of size . An analysis of Rubiaceae, another understory representative, yielded very strong significance for size ( 2 way ANOVA p = 0 .0009), but none for location. The last family, Piperaceae, an und e rstory tree, showed significant differences for both location and size ( 2 way ANOVA, p = 0 .0031 and p = 0 .0003, respectively). All the families but Arecaceae and Melastomataceae showed strong support for increased damage to smaller trees (as a result of significant differences with respect to size discussed above ) . No significant increase in herbivory was f ound in the transition from 1 5 m to the 5 10 m trees in these families. Additionally, all families except Arecaceae showed significant herbivory on s maller leav es ( Simple Regression, average p = 0 .002, average r 2 = 0. 35 ) A display of the average values for each tree and family wide averages shows th e absolute amounts of percentages of herbivory . Melastomataceae suffered the highest percentage damage i n both gaps and continuous forest, while Lauraceae was preyed upon the least of all families in both habitats . ANOVA tests rely on adequately large , and more importantly, independent sample sizes. This analysis, however, included only 15 total trees. Ther efore, throughout these tests, especially when single trees were compared to each other, pseudo replication of data may have influenced the results. Ultimately, this was unavoidable based on the types of available trees, but the effect was countered by trea ting each leaf as a separate data point to increase the sample size and create a workable data set. DISCUSSION These trends should provide enough information to judge the extent to which herbivory is the deciding factor in gap composition. Gaps hav e been shown to feature a higher variety and number of herbivores (Janzen 1995), s o it makes sense that they also generally feature high overall herbivory levels compared to those of continuous forest. Discussion
5 of each growth form, however can offer more valuable evidence for how measurable an effect results from the gap habitat. The pio neer, Melastomataceae, showed the most drastic increase in damage on individuals located in gaps. This seems counter intuitive as open areas with available light represe nt its preferred habitat. It must be inferred then that pioneers are able to use plentiful resources to grow at a rate that keeps leaf damage in check with respect to the overall wellness of the plant . Some have suggested that rapid leaf growth is an effec tive defense against herbivores because they are provided only a small window before the leaf acquires chemical or m orphological defenses (Coley & Barone 1996 ). However, the level of damage on all sizes of Melastome trees was high, implying that even durin g later growth the same growth before defense strategy is employed. Arecaceae, an understory plant, was unaffected by any study factors, and its overall low herbivory levels show that it is very well adapted to protecting its (relatively few) leaves an d surviving to adult stature. This was supported by the evident, but admittedly su bjective and unreported, results that this plant was extremely common and grew in patches of several individuals in both areas. The other two understory plants, Rubiaceae and Piperaceae, were both hurt more by herbivory in gaps, but the overall percentage of herbivory was much lower than that of Melastomes. Thus, these trees are probably allocating resources to defense (exact levels and types of defense could be explored in fu rther research), and at least temporarily compromising biomass production to do so. T hese understory plants showed a strong effect of size unlike pioneers . The increased effect on small leaves and small trees, translates into the following: young leaves of all understory plants were eaten, and, because all leaves on a sufficiently young plant are young, these were highly affected as well. Lauraceae, the representative of canopy plants, took this trend even further. It was only affected by size, and enjoyed equally low herbivory levels regardless of habitat. This is consistent with the great need of canopy plants to protect their leaves. However, as with the others , younger trees of Lauraceae were m ore damaged than the larger ones. These patterns offer some v ery specific and telling evidence for the nature of gap succession. It appears that with respect to herbivory, all non pioneers are more effective competitors in a gap environment. Pioneers tend to pour all available energy into rapid growth and reproduct ion, a strategy that has clearly ensured the survival of the li fe form. H owever, considering defenses do not appear to increase as a pioneer tree ages, at some point the combined effects of heavy herbivory and competition from more efficient (and eventuall y larger) trees will result in their demise. N on pioneers show effective defenses but are still affected heavily when young as discussed above . This suggests that herbivory plays the largest role in determining gap composition s oon after gap formation wh en colonizers of all life forms (the only plants initially present in the gap) are young. However, whether this effect is ever large enough to elimi nate understory and canopy individuals and not pioneers seems suspect. Despite the high leaf damage sustaine d by pioneers, large individuals were still present. A more likely scheme seems to be the following: pioneers grow quickly, complete their life cycle and senesce. The apparent increased conce ntration of herbivores on pioneers probably lessens h erbivore dam age on non pioneers. Thus, understory and canopy plants, after sustaining minor damage as saplings , are able to shrug off these effects as adults. T his study suggests that succession is random with respect to herbivory , given that gap
6 formation is random a nd all persistent trees appear to survive. The other distinct possibility is that herbivory is independent or a subordinate part of one or more other effects that do play a real role in non random succession Factors a ffecting dispersal and germination pr obably play a larger role in determining gap composition than competition over herbivory defense based on these results and conclusions . Pioneers may have gained a slight advantage in this area, as they tend to germinate in response to light, whereas seeds of persistent plants wait for an increase in formed. This allows q uick initial growth and may briefly delay out competition by persistents. Future studies should test whether this pattern holds true in other habitats and other types of gaps , as each light gap does present a legitimately and significantly different habitat. These other effects, dispe rsal and germination, as well as factors influencing their success, should also be studied in relation to the apparently weak effect of herbivory on survival. In addition, a slightly improved version of this study would also be valuable. This would involve the same type of methodology but include one or more of the following: more than one gap and non gap site, more than one individual per family per habit at, and more families representing each growth form. This could control for differences (both abiotic and biotic) between gaps, provide a larger sample size, and provide a data set that could be analyzed without pseudoreplication confounding the underlying trends and significance. ACKNOWLEDGEMENTS I would like to thank M. Jost and O. Hyman for their statistical expertise and patience in all matters of logistical inquiry . I am deeply indebted to the owners and operators of the Caminata Nocturnal trails , whoever you are. Critical commentary by G. Burkard, M. Warner, and M. Tsupros greatly increased the quality of this manuscript. Without the wisdom and guidance of A. and K. Masters, this study would not have been possible. Thanks to Kathy for doing all s lady. R. LaVal would have been extremely helpful had my project remained in its original form, which had I extend a heartfelt congratulations and farewell to all students in this Thanks are in order to alcohol for obvious reasons. I graciously salute all members of genus in Lachesis for not eating me. Brownie Deligh ts, provided in part by Helados Sabores proved an indispensable resource and rema ined both delicious and nutritious throughout the duration of this project. I do not want to thank members of the family Melastomataceae which were the l e ast badass plants observed at any point in the semester: they suck. To balance out their statistically significantly low levels of everything, I am obligated to balance it out by thank ing Rocky (only I the Russian then the Cold War would never have ended and the Estacion Biologica may not have been available for my use as a lab and literature studio. Lastly, seriously super big ups to Porkfish and the Bottom Feeders. LITERATURE CITED Brokaw, N.V. 1982. The definition of treefall gap and its effect on measures of forest dynamics. Biotropica 14(2): 159 160. Coley, P.D. 1983. Herbivory and defensive characteristics of tree species in lowland tropical forest. Ecological Monographs. 53(2): 209 233.
7 Coley, P.D. and J.A. Barone. 1996. Herbivory and plant defenses in tropical forests. Annual Review of Ecological Syst ems. 27: 305 335 Denslow, J.S. 1987. Tropical rainforest gaps and tree species diversity. Annual Review of Ecological Systems. 18: 431 451. Sagers, C.L. and P.D. Coley. 1995. Benefits and costs of defense in a neotropical shrub. Ecology. 76(6): 1835 18 43 Janzen, D.H. 1975. Ecology of plants in the tropics. Edward Arnold Ltd., London. Nadkarni, M. Nalini & Nathaniel T. Wheelwright. 2000. Monteverde. Oxford University Press, New York, pp. 310 315. Denslow, J.S. & A.M. Ellison & R.E. Sanford. 1998. T reefall gap size effects on above and below ground processes in a tropical wet forest. Ecology 86: 597 609. Denslow, J.S. 1980. Gap partitioning among tropical rainforest trees. Tropical Succession: pp. 47 55. Denslow, J.S., & G. S. Hartshorn. 1994. T ree fall gap environments and forest dynamic processes, In McDade, L.A. & K.S. Bawa & H.A. Hespenheide & G.S. Hartshorn (Ed.) La Selva, pp. 120 127. University of Chicago Press, Chicago. Coley, P.D. 1985. Rates of herbivory on different tropical trees, In The Ecology of a Tropical Forest, pp. 123 128. Smithsonian Institution Press, Washington, D.C.
8 = North 1 cm = 711 m Figure 1. Topographical Map of Montever de, Costa Rica and surrounding area. The light gap site (1300 m) is marked by a red dot, and the continuous forest site (1300 m) is marked with a blue dot. The size s of dots do not represent the scale size of the study sites.
9 ________________________ _________________ ________________________ __________ _________________ __________ A. B. C. Figure 2. P re collection logistics. A represents a 0 1 m tree, B a 1 5 m tree, and C a 1 10 m tree. The horizontal lines show division of t he tree into vertical thirds. Fifteen total leaves were taken from each section. Monteverde, Costa Rica, November 5 10, 2005. Figure 3. Interaction relation of percent herbivory with location and family, based on herbivory levels measured from leaf samples of trees in three size categories in the shown families within and outside of a forest ligh t gap. N = number of leaves sampled per family per habitat. Monteverde, Costa Rica, November 5 10, 2005.
10 Figure 4. Herbivory levels by size and location for each family. Blue corresponds to 0 1 m trees, violet to 1 5 m, and yellow to 5 10 m. A repres ents Arecaceae, B Lauraceae , C Melastomataceae, D Rubiaceae, and E shows results for Piperaceae. N = 15 leaves in all cases, except: A (0 1) = 8 leaves and D (0 1) = 12 leaves. Note the difference in scales of each graph, which give some indication of the a bsolute percent herbivory per family. This is clarified and further illustrated in Table 1. Monteverde, Costa Rica, November 5 10, 2005.
11 GAP CONTINUOUS Family 0 1 m 1 5 m 5 10 m Average 0 1 m 1 5 m 5 10 m Average Melastomataceae 0.231 0.249 0.2 0.227 0.1258 0.158 0.203 0.162 Areca cea e 0 0.0704 0.1221 0.064 0.1322 0.0609 0.0977 0.097 Piper aceae 0.176 0.1038 0.083 0.121 0.1072 0.073 0.054 0.0781 Rubiacea e 0.139 0.1152 0.0679 0.107 0.1308 0.0694 0.0404 0.0802 Lauracea e 0.0549 0.091 0.0345 0.0601 0.0643 0.0739 0.0674 0.069 Table 1. Mean percentages herbivory per family per tree size and overall family averages separated by location. Individuals of Melastomataceae, a pioneer plant, were most damaged while those of Lauraceae, a canopy tree, were least affected. Sample sizes are the same as those in Figure 1. Monteverde, Costa Rica, November 5 10, 2005.
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Efecto de la herbivora en la sucesin de la luz del bosque
Effect of herbivory on succession of forest light gaps
Effects of herbivory have been seen to vary according to the particular growth form of a plant and its habitat. The idea that these factors can interact to determine the nature of gap succession has been suggested but has not yet been thoroughly explored. Leaves of pioneer, understory, and canopy plants were collected and analyzed to quantify herbivory levels on each growth form. Herbivory was found to be higher in gaps (p = 0.0015), and this was true to varying degrees with respect to growth forms and single families. Results suggest that herbivory is not the main factor influencing instantaneous or eventual gap composition, but it could interact with other effects like competition for light and water. The study also does not rule out the possibility that gap composition is random.
Se ha observado que los efectos de la herbivora cambian con la forma de crecimiento y el hbitat de una planta. El concepto de que estos factores pueden interactuar para determinar la esencia de la sucesin en un claro del bosque ha sido sugerido, pero no ha sido estudiado en detalle. Las hojas de las plantas pioneras, del sotobosque y del dosel fueron colectadas y analizadas para cuantificar los niveles de la herbivora en cada forma de crecimiento. Ms herbivora ocurri dentro de los claros del bosque (p = 0.0015) y el efecto particular de este patrn fue diferente de acuerdo a la familia taxonmica y a la forma de crecimiento. Los resultados sugieren que la herbivora no es el factor ms importante influyendo la sucesin en los claros del bosque, pero podra interactuar con otros factores como la competencia por el agua y la luz. Adems, este estudio no puede eliminar la posibilidad de que la composicin en los claros del bosque sea un proceso aleatorio.
Text in English.
Plants--Effect of browsing on
Costa Rica--Puntarenas--Monteverde Zone--Monteverde
Bosque de sucesion
Plantas--Efecto de una ojeada en
Costa Rica--Puntarenas--Zona de Monteverde--Monteverde
Tropical Ecology Fall 2005
Ecologa Tropical Otoo 2005
t Monteverde Institute : Tropical Ecology