- Email: [email protected]
Foliar pathogen and insect herbivore effects on two landslide tree species in Puerto Rico
Forest Ecology and Management 169 (2002) 231–242
Foliar pathogen and insect herbivore effects on two landslide tree species in Puerto Rico Randall W. Myster* Department of Biology, University of Central Oklahoma, Box 89, Edmond, OK 73034, USA Accepted 17 September 2001
Abstract To better understand pathogen/herbivore interactions and landslide regeneration, percent leaf area lost to disease and herbivory on two Puerto Rican trees over a 1-year period was sampled. Cecropia schreberiana saplings lost from 1 to 3% leaf area to pathogens and from 1 to 7% to herbivores. For Inga vera, both sapling and seedling losses to pathogens were minimal, but Inga herbivory losses reached 25% for saplings and 34% for seedlings. The most common fungi on Cecropia leaves were species in the genera Phoma and Phyllosticta, and on Inga leaves was Colletotrichum gloeosporioides. Percent survivorship after 1 year in the field varied among species and life-form (46% for Cecropia saplings, 15% for Inga saplings, 0% for Inga seedlings). There were no effects of pathogens or herbivores on survivorship or growth, but increased levels of herbivory did significantly correlate with total phenolics and condensed tannins in both Inga seedlings and saplings. For both seedlings and saplings of two trees on the neotropic island of Puerto Rico: (1) leaf herbivory was modest and leaf losses to pathogen disease were small; (2) these mechanisms did not affect survivorship or growth; (3) a neotropical tree (I. vera) displayed increased levels of secondary chemicals in its leaves, correlated with increased levels of insect herbivory. # 2002 Elsevier Science B.V. All rights reserved. Keywords: Cecropia schreberiana; Inga vera; Phenolics; Survivorship; Tannins
1. Introduction Whereas ecosystem function and structure may be largely dependent on biotic responses to disturbance (Watt, 1947; Brokaw, 1985; Pickett and White, 1985; Denslow, 1987; Brokaw and Walker, 1991), this relationship may be particularly strong after severe disturbances (Garwood et al., 1979; Sousa, 1984; Waide and Lugo, 1992). For example, landslides (Myster, 1993; Myster and Fernandez, 1995) may influence ecosystem functions such as biodiversity maintenance (e.g., creating regeneration sites for rare * Tel.: þ1-405-974-5725; fax: þ1-405-974-5726. E-mail address: [email protected] (R.W. Myster).
species [ferns: Walker, 1994] or adding species to less severely disturbed areas [hurricanes: Willig and Camilo, 1991]), nutrient cycling and material flow/ redistribution (Swanson et al., 1982; Guariguata, 1990). Because most landslide revegetation involves seeds, seedlings and saplings (advanced regeneration such as resprouting is rare), and because most previous landslide studies have been focused on seeds (Walker and Neris, 1993; Walker, 1994; Myster and Fernandez, 1995; Myster, 1997), studies of seedling and sapling ecology in landslides are needed (Dalling and Tanner, 1995). In addition, these studies can help to address the larger ecological issue of the role of herbivory and leaf disease both in communities and in individual
0378-1127/02/$ – see front matter # 2002 Elsevier Science B.V. All rights reserved. PII: S 0 3 7 8 - 1 1 2 7 ( 0 1 ) 0 0 7 5 7 - 5
232
R.W. Myster / Forest Ecology and Management 169 (2002) 231–242
plants. Many studies have documented patterns of these two mechanisms (e.g., Coley, 1983, 1986; Aide, 1993) but, whether or not they affect plants in an ecological meaningful way, e.g., causing mortality or changes in growth and allocation (Louda and Colling, 1992; Agrawal, 1997; Wold and Marquis, 1997) needs further investigation. This is especially true on neotropic islands, because studies have shown that these mechanisms do affect plant processes on the neotropic mainland (Augspurger, 1983, 1984). More specifically, because pathogens and herbivores often attack plants concurrently, they may: (1) affect the suitability of the plant host for each other (Benedict et al., 1991); (2) induce similar generalized plant responses (Augspurger and Kelly, 1984); (3) lead to related plant defense responses (Coley, 1993); (4) interact in time with herbivores consuming young leaves and pathogens damaging older leaves (Marquis et al., 1993). Therefore, the effect of these two mechanisms, herbivory and pathogenic disease, on the survival, growth and secondary chemistry of seedlings and saplings of two common landslide tree species with differing successional life histories were conducted. This included landslide field sampling and laboratory analysis to examine both the pattern of leaf pathogen and herbivore damage and their effects on landslide tree seedlings and saplings. Specifically, these questions were addressed: 1. Are saplings of Cecropia schreberiana or seedlings and saplings of Inga vera most susceptible to damage? And, what is the monthly variation in that damage in Puerto Rico over 1-year’s time? 2. What are the effects of these two biotic mechanisms on the number of seedling and sapling survivors, and their growth and secondary leaf chemistry?
2. Materials and methods The study was conducted in the Luquillo experimental forest (LEF), a long-term ecological research site of the National Science Foundation, located in the NE corner of Puerto Rico, USA (188200 N, 668000 W). Both study landslides (ES1 and ES3) are located in the lower montane wet forest of the LEF (Ewel and
Whitmore, 1973), which is dominated by tabonuco (Dacryodes excelsa: Waide and Lugo, 1992). Common vegetation occurring on landslides includes the ferns Cyathea arborea and Gleichinia bifida in the upper primary-soil areas, and trees C. schreberiana, Miconia racemosa, I. vera, and Nepsera acuatica in the lower debris areas (Myster and Fernandez, 1995; Myster and Walker, 1997). ES1 and ES3 are both between 10 and 15 years (time since sliding event), occur in the Rio Espiritu Santo watershed at 350 m and 450 m elevation, respectively, and have soils derived from volcanoclastic primary substrate that has weathered into clay Ultisols (Walker, 1994). The average yearly temperature in the LEF is 18 8C and the LEF gets between 2 and 5 m of rainfall a year with a dry season between November and May. In January 1995, 15 saplings (defined as greater than 1 cm basal diameter (bd)) of C. schreberiana (Cecropiaceae), 15 saplings of I. vera (Fabaceae: Mimosoideae; Little and Wadsworth (1989) was used as the taxonomic source for this study and for the nomenclature of all plants used) and 15 I. vera seedlings (defined as less than 1 cm bd) total from the two landslides were selected. Cecropia is a common woody early successional invader in LEF disturbed areas that does not form ant associations in Puerto Rico. Inga grows more slowly, is mid-successional and fixes nitrogen (Viera, 1986; Devoe, 1989), which may lead to nutrient-rich leaves that insects prefer. Consequently, any induction effects of herbivores on tropical tree species may be most easily seen on species like Inga. Pooling samples from both landslides was justified because the landslides are: (1) in the same watershed implying a common soil type and drainage system; (2) of similar size, aspect and slope; (3) located within a few 100 m of each other (Guariguata and Larsen, 1990). Cecropia seedlings were not included in the study, because not enough stems less than 1 cm bd could be found in the two landslides, perhaps due to the fast growth rate of this species (Aide, 1993). The 45 individual plants were found mainly in the lower landslide areas which have a partially closed canopy (from 14 to 30% of full light and between 0.3 and 0.4 red to far-red ratio) and large spatial variation in both nitrogen (from 0.04 to 0.40 kg/m2 to 9 cm depth) and phosphorus (from 0.001 to 0.052 kg/m2 to 9 cm depth) availability (Myster and Fernandez, 1995).
R.W. Myster / Forest Ecology and Management 169 (2002) 231–242
Competition intensity for these resources has never been quantified in landslides. Plants were censused in the middle of each month during 1995, when all new leaves produced since the last sampling were marked with colored wire, and individual plants were scored as either alive or dead. At that time, bd was measured for saplings, and both bd and diameter at 10 cm from the ground was measured for seedlings. For all leaves (new and old) that were fully expanded, I estimated the percentage of the total leaf area that was lost to disease and to herbivory by placing a card divided into 1 cm squares under each leaf. Herbivory usually consisted of holes in the leaf, consistent with insect damage. In contrast pathogenic disease stained the leaf tissue which can lead to necrosis but, perhaps because of the size of the stems, the more severe damping-off fungus (Jarosz and Darelos, 1995) was not seen. Also, it should be remembered that these mechanisms might not be independent because, e.g., several insect species are known to act as a pathogen vector by transporting spores (De la Cruz and Dirzo, 1987). For almost all leaves, the first month of damage was known. In addition, leaves were scored as small, medium or large based on observation of other individuals of the same species. Statistical differences in damage between species, life-stage, biotic agent and leaf-size were investigated using analysis of variance and grouping leaves accordingly (i.e., by species then by life-stage then by leaf size: ANOVA: SAS, 1985). Also, because samplings are not independent among months, differences among months were investigated using repeated measures analysis (Hand and Taylor, 1987). Probability levels are given only for significant results. Microsite differences inside the landslides (e.g., center, edge) could not be investigated statistically because not enough natural seedlings or saplings not occurred in the individual microsites. After 1 year, at the end of 1995, all live leaves on the stems were collected and used for chemical analysis (20 leaves for Cecropia, 52 for Inga saplings, 66 for Inga seedlings), oven dried at 35 8C for 48 h and then ground to a powder (Dudt and Shure, 1993). This low drying temperature permitted more efficient tannin analysis (Swain, 1979). Then, total phenolics were assayed using the Folin Denis technique (Bryant et al., 1987), condensed tannins were estimated as proanthocyanidins using a butanol–HCl technique (Bate-smith,
233
1975, 1981; Porter et al., 1986) and hydrolyzable tannins (ellagitannins only) were assayed under a N2 environment using an acetic acid–sodium nitrate procedure (Bate-smith, 1972, 1977; Wilson and Hagerman, 1990). Fungal species on leaves were identified after incubation on water agar of surface-disinfected leaf samples taken from the leaves at the end of the experiment. In some cases, cultures were transferred to malt agar. An unbalanced, multivariate analysis of variance (MANOVA: SAS, 1985) was used to investigate the effects of pathogens and herbivores on seedling and sapling survivorship, growth, and concentration of secondary compounds. Lack of sufficient replication prevented interactions between pathogens and herbivores from being investigated. Five categories of damage both by pathogens and herbivores (1–20%, 21–40%, 41–60%, 61–80%, 81–100% leaf area lost) were used as the discrete treatments needed for the MANOVA. For the % survivor MANOVAs, the mean leaf loss percentage for all leaves on individual stems available at the end of the experiment was used, or at the last sampling if the stem died, in the treatment groups. For the growth MANOVAs, the mean leaf loss percentage for all the leaves that occurred on an individual stem was used, averaged over the 11-month period, in the treatment groups. The naturally occurring levels of herbivory and pathogenic disease were used instead of creating artificial treatments (e.g., by clipping leaves) in the field. The large number of replicates, in the form of leaves, created sufficient statistical power for the chemical results by adding enough replication for all damage categories. Tukey’s least significant difference (LSD) tests (p < 0:05 level) were used to locate pair wise differences when MANOVAs were significant. All growth rates were computed relative to the initial level of the characteristic scored (e.g., height growth rate ¼ (final height initial height)/initial height/year [Beadle, 1993]) and expressed in cm/cm/year. Because survivorship data may not fit a normal distribution, w2 were also calculated to investigate the effects of the treatments on survivorship (SAS, 1985). 3. Results Leaves of Cecropia saplings sustained little monthly damage from pathogens, having an average
234
R.W. Myster / Forest Ecology and Management 169 (2002) 231–242
of 2%, and a maximum of 15%, leaf area lost. However, leaves of Cecropia saplings had significantly more area lost to herbivores than pathogens (F ¼ 5:58; p < 0:05; mean ¼ 4%; Fig. 1). Leaf
losses to disease were lower for leaves of Inga saplings (mean levels of 1%) compared to Cecropia saplings, but Inga sapling herbivory was significantly greater than both Cecropia herbivory ðmean ¼ 18%Þ and Inga
Fig. 1. Mean disease and herbivory levels on Cecropia sapling leaves (percent of total leaf area lost) by leaf size class (small [S], medium [M], large [L]) measured monthly over 1995.
R.W. Myster / Forest Ecology and Management 169 (2002) 231–242
235
Fig. 2. Mean disease and herbivory levels on Inga sapling leaves (percent of total leaf area lost) by leaf size class measured monthly over 1995.
sapling pathogens (F ¼ 10:9; p < 0:01; Fig. 2). Inga seedlings lost significantly more leaf area to herbivores (30% on average) than Cecropia or Inga saplings ðF ¼ 4:2; p < 0:05Þ. In addition, leaf loss to pathogens on Inga seedlings was low (mean 1%; Fig. 3), where herbivores damaged significantly more leaf area than did pathogens ðF ¼ 13:45; p < 0:01Þ. Inga seedlings had two other significant patterns: (1) there was more leaf area lost to herbivory on larger leaves compared to medium or smaller leaves ðF ¼ 5:56; p < 0:05Þ; (2) there was significantly more leaf area lost to herbivory between the months of May–December compared to other months
(repeated measures analysis F ¼ 4:2; p < 0:05). However, this last result did not correlate with either the wet (June–November) or dry season in Puerto Rico. Pathogenic leaf infection and disease expression has also been sampled in both LEF pastures (unpublished data, author) and LEF gaps (Devoe, 1989), and found to be low suggesting that pathogen infection may not induce changes in secondary metabolites in pastures and gaps. The most common fungi on Cecropia leaves were species in the genera Phoma and Phyllosticta, but some Fusicladium cecropiae was also found. The most common pathogenic fungus on Inga leaves
236
R.W. Myster / Forest Ecology and Management 169 (2002) 231–242
Fig. 3. Mean disease and herbivory levels on Inga seedling leaves (percent of total leaf area lost) by leaf size class measured monthly over 1995.
was Colletotrichum gloeosporioides, but Phyllachora cecropiae was also present. In addition, Xylaria multiplex was isolated from Inga leaves as a nonpathogenic endophyte. All species except Xylaria are pathogenic fungi (D. Jean Lodge, pers. comm.), but not much is known about their effect except that they may vary in the strength of the responses they illicit in the host (Dewit, 1987). The majority of saplings and seedlings survived over the entire sampling period (Fig. 4) but there was large variation between species. Cecropia saplings had the greatest mortality (46%), which occurred mainly during the wet months of June and July, Inga lost two saplings (14% mortality of those stems with the smallest dbh) and no seedlings. Cecropia sapling bd
ranged between 1.13 and 5.45 cm over the study with a mean growth rate of 9.87 cm/cm/year bd, and Inga sapling bd ranged between 1.07 and 2.74 cm with a mean growth rate of 4.68 cm/cm/year bd (Table 1). Inga seedlings ranged between 0.25 and 0.94 cm bd Table 1 Mean growth rates per year (1 S.E.) for all sampled Cecropia saplings, Inga saplings and Inga seedlings Species/life-stage
Diameter (cm)
Height (cm)
Cecropia saplings Inga saplings Inga seedlings
basal: 9:87 0:11 basal: 4:68 0:05 basal: 6:13 0:01 10 cm from base: 8:09 0:02
– – 0:26 0:02 –
R.W. Myster / Forest Ecology and Management 169 (2002) 231–242
237
Fig. 4. Survivorship for Cecropia saplings, Inga saplings, Inga seedlings measured monthly over 1995.
with a mean growth rate of 6.125 cm/cm/year bd, and between 0.32 and 1.02 cm in diameter at 10 cm height with an average growth rate of 8.088 cm/cm/year. Inga seedlings also ranged between 14 and 107 cm in
height with a mean growth rate of 0.261 cm/cm/year. Species differences corresponded strongly with differences in survivorship, while life-stage (seedlings vs. saplings) differences dominated growth differ-
Fig. 5. Mean levels of total phenolics (% TAE) from leaves of Cecropia saplings, Inga saplings and Inga seedlings for each of the five categories (1–20% [black], 21–40% [crossed], 41–60% [reverse diagonal], 61–80% [diagonal], 81–100% [clear]) of leaf loss to herbivory and to pathogens. Different small letters above the histograms indicate significant differences (Tukey’s LSD, p < 0:05) from the other means.
238
R.W. Myster / Forest Ecology and Management 169 (2002) 231–242
Fig. 6. Mean levels of condensed tannins (% QTE) from leaves of Cecropia saplings, Inga saplings and Inga seedlings with the same indicators as in Fig. 5.
Fig. 7. Mean levels of hydrolyzable tannins (mg/g HHDP) from leaves of Cecropia saplings, Inga saplings and Inga seedlings with the same indicators as in Fig. 5.
R.W. Myster / Forest Ecology and Management 169 (2002) 231–242
ences. The results of the MANOVA ðF ¼ 1:2; p ¼ 0:54Þ and w2 analysis ðw2 ¼ 0:98; d:f: ¼ 1; p ¼ 0:56Þ showed that levels of disease or herbivory did not significantly correlate with any of these survivorship or growth results. The level of total phenolics in the leaves of Inga seedlings was greater than in the leaves of either Inga saplings or Cecropia saplings (F ¼ 4:51; p < 0:05; Fig. 5). Further, herbivory on Inga in the higher damage classes correlated with a significant increase in total phenolics at both the seedling and the sapling stages (using leaves with no damage as a control, F ¼ 3:44; p < 0:05) implicating induction. Condensed tannins (Fig. 6) showed many of the same patterns as total phenolics: (1) condensed tannin levels in Inga seedlings were greater (though non-significant) than both Cecropia and Inga saplings; (2) the higher herbivory leaf loss class induced a significant increase in condensed tannins in Inga saplings ðF ¼ 4:84; p < 0:05Þ and Inga seedlings ðF ¼ 5:12; p < 0:05Þ as it did for total phenolics. Hydrolyzable tannin concentrations were not significantly correlated with damage levels (Fig. 7).
4. Discussion The basic leaf pattern results were that (1) Inga leaves generally had more damage than Cecropia leaves, (2) damage from herbivory was more pronounced than from disease, (3) sapling and seedling leaf losses were comparable within species, (4) there was a pattern of larger leaves being preferred over medium and smaller leaves by herbivores and (5) leaf losses to herbivores were greater during the months of May–December compared to other months of the year. Schowalter’s (1994) Puerto Rican study found two of the same patterns: (1) more herbivory on later successional species (Inga in our study) compared to early successional species (Cecropia) and (2) greater species variation than temporal or leaf size variation in tree leaf loss. Inga had the only fungus (Colletotrichum sp.) on its leaves that was also found on LEF landslide seeds (on Palicouria riparia seeds; Myster, 1997) suggesting that few LEF pathogen species attack both seeds and seedlings. Herbivory was assumed to be due to insects because of the lack of native non-volant mammals on the island of Puerto
239
Rico (Waide and Lugo, 1992) and because a variety of Puerto Rican insect taxa and structural groups (Schowalter, 1994; Myster, 1994) were observed on leaves of seedlings and saplings. Although the levels of leaf loss had no effect on survivorship or growth, level of herbivory did correlate with an increase in total phenolics and condensed tannins in both Inga saplings and Inga seedlings. Because Inga fixes nitrogen and has nutrient-rich leaves (Scatena et al., 1993), insects may prefer it and this could help in explaining these species differences and the induction. This may be the first time induction that has been shown for a neotropical species. Although cause and effect cannot be proved, because of the same Inga induction for both total phenolics and condensed tannins, and the multitude of studies showing plants responding to herbivory by increasing levels of secondary compounds (e.g., Swain, 1979; Rhodes, 1983; Agrawal, 1997; Karban et al., 1997; Wold and Marquis, 1997), it is unlikely that these results could be due to something associated with herbivory (e.g., herbivores choosing leaves with high levels of secondary compounds) and not the herbivory itself. Important comparisons can be made between these island results and those dealing with Cecropia spp. and Inga spp. disease and herbivory in disturbed areas on the neotropic mainland, where biotic interactions are supposed to be stronger (Janzen, 1973; Myster, 1997) and, therefore, have a greater effect on ecosystems. The annual levels of Cecropia herbivory were similar to levels found in Mexican gaps (25% on C. obtusifolia; Nunez-farfan, 1989), but higher than the 5.9% herbivory for C. obtusifolia in a Mexican forest (De la Cruz and Dirzo, 1987), and the 5% herbivory in Panama gaps for C. insignis whose mortality rate was also lower compared to this study (Coley, 1983). This reduced herbivory in Panama may reflect a stronger mutualistic defensive relationship between the Azteca ant and Cecropia (Putz and Holbrook, 1988) in Panama compared to Puerto Rico where there is no Cecropia-ant mutualism. Alternatively, even though the levels of hydrolyzable tannins found here in C. schreberiana were similar to those reported by Coley (1986) in Panama, the leaves with these tannin levels did not show reduced insect herbivory. In Costa Rica gaps the level of herbivory on Inga spp. is often greater than these levels but lower in a Mexican forest
240
R.W. Myster / Forest Ecology and Management 169 (2002) 231–242
(6.5%; De la Cruz and Dirzo, 1987), but the amount of Inga sapling total phenolics is similar to these Puerto Rico results (I. densiflora, I. punctata: Koptur, 1984, 1985). Furthermore, both the total phenolic and the condensed tannin levels for Inga seedlings in Puerto Rico were greater than for I. oerstediana in Costa Rica gaps (Nichols-orians, 1991). The same pattern of larger pathogen or herbivore effects on the mainland compared to Puerto Rico holds when comparing the results with those in the mainland understorey, the leaf losses to pathogens here in Puerto Rico were very low (however, damage may be more severe earlier in a seedlings life), but 37% of seedling leaf area can be lost to disease in Brazil (Marquis et al., 1993) and disease can cause up to 81% mortality of seedlings in Panama (damping-off fungal species: Augspurger, 1983, 1984). The results support Dudt and Shure’s (1993, 1994) findings that herbivory levels were unrelated to levels of disease, hydrolyzable tannin and condensed tannin levels were slightly higher in leaves showing moderate pathogen infection leaves (their genus was Cornus), and shade-tolerant species (Inga for us, Cornus for them) had higher levels of total phenolics in their leaves than shade-intolerant species (Cecropia in this study, Liriodendron in theirs). In addition, there was support in total phenolics and condensed tannins (but not in hydrolyzable tannins) for the theory (Coley et al., 1985) that early successional species (i.e., Cecropia) have lower secondary compound levels than later successional species (i.e., Inga). However, there was not supporting evidence in the results for (1) an inverse relationship between levels of condensed and hydrolyzable tannins (Dudt and Shure, 1994), (2) an increase of phenolics or tannins associated with levels of pathogens, (3) an increase of hydrolyzable tannins induced by herbivores (some evidence for Cornus in Dudt and Shure, 1993), (4) herbivores preferring young leaves while pathogens preferring mature ones (Marquis et al., 1993), (5) most damage occurring during the first month after expansion, (6) the percentage of leaf lost influencing growth rate (Aide, 1993), or (7) pathogen levels affect plant host preference by herbivores or visa versa (Dudt and Shure, 1993), which could reflect the food value of the host species (Clay et al., 1993). Finally, pathogen levels were probably too low in this study (similar to another LEF study by Devoe, 1989 and unpublished
data in pastures by the primary author) to test whether light-seeded early successional species lack resistance to seedling pathogens (Augspurger and Kelly, 1984). The results show an average mortality rate of 20% per year for the sampled seedlings and saplings, similar to landslide seedlings and saplings in Jamaica (Dalling and Tanner, 1995). Although results suggest a relatively minor role for herbivory and pathogenesis in LEF landslides compared to other mechanisms in determining survivorship, they may be important by acting indirectly and changing competitive hierarchies among plants (Crawley, 1983; Schowalter, 1985; Myster and McCarthy, 1989; Clay et al., 1993). Indeed, plant–plant competition may be a key successional landslide regeneration mechanism for a number of reasons: (1) landslides have extreme spatial variation and patchiness in both the nutrients which plants compete for and in the availability of the VA-mycorrhizae which influences their nutrient uptake (Myster and Fernandez, 1995), (2) field experiments show that landslide trees compete for patchy distributions of soil nutrients and light (Fetcher et al., 1996), (3) field studies suggest that landslide ferns (e.g., Dicranopteris pectinata) inhibit tree seedling growth (e.g., Tabebuia heterophylla) through light competition (Walker, 1994) and (4) Cecropia and Inga are common competitors with other species and may inhibit many of them during succession (author, unpublished data).
Acknowledgements First, I thank Liz A. Sanchez for her help in laboratory analysis and D. Jean Lodge for her help in identifying fungal genera. I also wish to thank Maria Aponte for field assistance, Ligia Lebron for laboratory assistance and Albert Muniz for help with the figures. Finally, I thank J. Thompson, D.J. Lodge, C. Augspurger, R. Marquis, P. Coley and D. Shure for commenting on earlier drafts of the manuscript. This research was performed under grant BSR-8811902 from the National Science Foundation to the Institute for Tropical Ecosystem Studies, University of Puerto Rico, and the International Institute of Tropical Forestry as part of the Long-term Ecological Research Program in the Luquillo Experimental Forest. Additional support was provided by the Forest Service
R.W. Myster / Forest Ecology and Management 169 (2002) 231–242
(US Department of Agriculture) and the University of Puerto Rico. References Agrawal, A.A., 1997. The benefits of induced plant responses: fitness effects of induction in the presence and absence of herbivores. Bull. Ecol. Soc. Am. 78, 43. Aide, T.M., 1993. Patterns of leaf development and herbivory in a tropical understory community. Ecology 74, 455–466. Augspurger, C.K., 1983. Offspring recruitment around tropical trees: changes in cohort distance with time. Oikos 40, 189–196. Augspurger, C.K., 1984. Seedling survival of tropical tree species: interactions of dispersal distance, light-gaps and pathogens. Ecology 65, 1705–1712. Augspurger, C.K., Kelly, C.K., 1984. Pathogen mortality of tropical tree seedlings: experimental studies of the effects of dispersal distance, seedling density, and light conditions. Oecologia 61, 211–217. Bate-smith, E.C., 1972. Detection and determination of ellagitannins. Phytochemistry 11, 1153–1156. Bate-smith, E.C., 1975. Phytochemistry of proanthocyanidins. Phytochemistry 14, 1107–1113. Bate-smith, E.C., 1977. Astringent tannins of Acer species. Phytochemistry 16, 1421–1426. Bate-smith, E.C., 1981. Astringent tannins of the leaves of Geranium species. Phytochemistry 20, 211–216. Beadle, C.L., 1993. Growth analysis. Photosynthesis and production in a changing environment. In: Hall, D.D., Scurlock, J.M.O., Bolhar-Nordenkampf, H.R., Leegood, R.C., Lang, S.P. (Eds.), A Field and Laboratory Manual. Chapman & Hall, London, pp. 85–98. Benedict, J.B., Chang, J.F., Bird, L.S., 1991. Influence of plant microflora on insect–plant relationships in Gossypium hirsutum. In: Barbosa, P., Krischik, V.A., Jones, C.G. (Eds.), Microbial Mediation of Plant–Herbivore Interactions. Wiley, New York, pp. 273–303. Brokaw, N.V.L., 1985. Treefalls, regrowth and community structure in tropical forests. In: Pickett, S.T.A., White, P.S. (Eds.), The Ecology of Natural Disturbance and Patch Dynamics. Academic Press, Orlando, FL, pp. 53–69. Brokaw, N.V.L., Walker, L.R., 1991. Summary of the effects of Caribbean hurricanes on vegetation. Biotropica 23, 442–447. Bryant, J.P., Chapin III, F.S., Reichardt, P.B., Clausen, T.P., 1987. Responses of winter chemical defense in Alaska paper birch and green alder to manipulation of plant carbon-nutrient balance. Oecologia 72, 510–514. Clay, K., Marks, S., Cheplick, G.P., 1993. Effects of insect herbivory and fungal endophyte infection on competitive interactions among grasses. Ecology 74, 1767–1777. Coley, P.D., 1983. Intraspecific variation in herbivory on two tropical tree species. Ecology 64, 426–433. Coley, P.D., 1986. Costs and benefits of defense by tannins in a neotropical tree. Oecologia 70, 238–241. Coley, P.D., 1993. Gap size and plant defenses. TREE 8, 12–16.
241
Coley, P.D., Bryant, J.P., Chapin, F.S., 1985. Resource availability and plant antiherbivore defense. Science 230, 895–899. Crawley, M.J., 1983. Herbivory: The Dynamics of Animal–Plant Interactions. University of California Press, Los Angeles, CA. Dalling, J.W., Tanner, E.V.J., 1995. An experimental study of regeneration on landslides in montane rain forest in Jamaica. J. Ecol. 83, 55–64. De la Cruz, M., Dirzo, R., 1987. A survey of the standing levels of herbivory in seedlings from a Mexican rainforest. Biotropica 19, 98–106. Denslow, J.S., 1987. Tropical rainforest gaps and tree species diversity. Ann. Rev. Ecol. Syst. 18, 431–451. Devoe, N.N., 1989. Differential seedling and regeneration in openings and beneath closed canopy in sub-tropical wet forest. Ph.D. Dissertation. School of Forestry and Environmental Studies, Yale University, New Haven, CT. Dewit, P.J.G.M., 1987. Specificity of active resistance mechanisms in plant–fungus interactions. In: Pegg, G.F., Ayers, P.G. (Eds.), Fungal Infections of Plants. Cambridge University Press, New York, pp. 1–22. Dudt, J.F., Shure, D.J., 1993. The effect of anthracnose (Discula destructiva) infection on plant–herbivore interactions in dogwood (Cornus florida). Oecologia 96, 108–113. Dudt, J.F., Shure, D.J., 1994. The influence of light and nutrients on foliar phenolics and insect herbivory. Ecology 75, 86–98. Ewel, J.J., Whitmore, J.L., 1973. The ecological life zones of Puerto Rico and the Virgin islands. United States Forest Service Research Paper ITF-18. Institute of Tropical Forestry, Rio Piedras, PR. Fetcher, N., Haines, B.L., Cordero, R.A., Lodge, D.J., Walker, L.R., Fernandez, D.S., Lawrence, W.T., 1996. Responses of tropical plants to mineral nutrients on a landslide in Puerto Rico. J. Ecol. 84, 123–134. Garwood, N.C., Janos, D.P., Brokaw, N.V.L., 1979. Earthquake caused landslides: a major disturbance to tropical forests. Science 205, 997–999. Guariguata, M.R., 1990. Landslide disturbance and forest regeneration in the upper Luquillo mountains of Puerto Rico. J. Ecol. 78, 814–832. Guariguata, M.R., Larsen, M.C., 1990. Preliminary map showing locations of landslides in El Yunque Quadrangle, Puerto Rico. US Geological Survey Open File Report 89-257. Hand, D.J., Taylor, C.C., 1987. Multivariate Analysis of Variance and Repeated Measures. Chapman & Hall, New York. Janzen, D.H., 1973. Sweep samples of tropical foliage insects: effects of season, vegetation types, elevation, time of day and insularity. Ecology 54, 687–701. Jarosz, A.M., Darelos, A.L., 1995. Effects of disease in wild plant populations and the evolution of pathogen aggressiveness. New Phytol. 129, 371–387. Karban, R., Agarawal, A.A., Mangel, M., 1997. The benefits of induced defences against herbivores. Ecology 78, 1351–1355. Koptur, S., 1984. Experimental evidence for defense of Inga (Mimosoideae) saplings by ants. Ecology 65, 1787–1793. Koptur, S., 1985. Alternative defenses against herbivores in Inga (Mimosoideae) over an elevational gradient. Ecology 66, 1639–1650.
242
R.W. Myster / Forest Ecology and Management 169 (2002) 231–242
Little, E.L., Wadsworth, F.H., 1989. Common trees of Puerto Rico and the Virgin Islands. Agriculture Handbook No. 249. US Department of Agriculture, Washington, DC. Louda, S.M., Colling, S.K., 1992. Plant resistance to insect herbivores: a field test of the environmental stress hypothesis. Ecology 73, 153–169. Marquis, R.J., Diniz, I.R., Morais, H.C., 1993. Interspecific patterns in folivory and pathogen attack for Brazilian cerrado trees. Bull. Ecol. Soc. Am. 74, 344. Myster, R.W., 1993. Spatial heterogeneity of seed rain, seed pool and vegetative cover on two Monteverde landslides, Costa Rica. Brenesia 39–40, 137–145. Myster, R.W., 1994. Landslide insects show small differences between an island (Puerto Rico) and the mainland (Costa Rica). Acta Cientifia 8, 105–113. Myster, R.W., 1997. Seed predation, disease and germination on landslides in neotropical lower montane wet forest. J. Veg. Sci. 8, 55–64. Myster, R.W., Fernandez, D.S., 1995. Spatial gradients and patch structure on two landslides in Puerto Rico. Biotropica 27, 149–159. Myster, R.W., McCarthy, B.C., 1989. Effects of herbivory and competition on survival of Carya tomentosa (Juglandaceae) seedlings. Oikos 56, 145–148. Myster, R.W., Walker, L.R., 1997. Plant successional pathways on Puerto Rican landslides. J. Trop. Ecol. 13, 165–173. Nichols-orians, C.M., 1991. The effects of light on foliar chemistry growth and susceptibility of seedlings of a canopy tree to an Attine ant. Oecologia 86, 552–560. Nunez-farfan, J., 1989. Leaf survival in relation to herbivory in two tropical pioneer species. Oikos 55, 71–74. Pickett, S.T.A., White, P.S., 1985. The Ecology of Natural Disturbance and Patch Dynamics. Academic Press, New York. Porter, L.J., Hrstich, L.N., Chan, B.G., 1986. The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry 25, 223–230. Putz, F.E., Holbrook, N.M., 1988. Further observations on the dissolution of mutualism between Cecropia and its ants: the Malaysian case. Oikos 53, 121–125. Rhodes, D.F., 1983. Herbivore population dynamics and plant chemistry. In: Denno, R.F., McClure, B. (Eds.), Variable Plants and Herbivores in Natural and Managed Systems, Academic Press, New York, pp. 155–220.
SAS Institute, 1985. User’s Guide: Statistics, 5th Edition. SAS Institute, Inc., Cary, NC. Scatena, F.N., Silver, W., Siccama, T., Johnson, A., Sanchez, M.J., 1993. Biomass and nutrient content of the Bisley experimental watersheds, Luquillo experimental forest, Puerto Rico, before and after hurricane hugo, 1989. Biotropica 25, 15–27. Schowalter, T.D., 1994. Invertebrate community structure and herbivory in a tropical rain forest canopy in Puerto Rico following hurricane hugo. Biotropica 26, 312–319. Sousa, W.P., 1984. The role of disturbance in natural communities. Ann. Rev. Ecol. Syst. 15, 353–391. Swain, T., 1979. Tannins and lignins. In: Rosenthal, G.A., Janzen, D.H. (Eds.), Herbivores: Their Interactions with Secondary Plant Metabolites. Academic Press, New York, pp. 657– 682. Swanson, F.J., Fredriksen, R.L., McCorison, P., 1982. Material transfer in a western Oregon forested watershed. Analysis of Coniferous Forest Ecosystems in the Western United States. US/IBP Synthesis Ser. 14. Hutchinson Ross Publishing Co., Stroudsburg, PA (Chapter 8). Viera, I.E.P., 1986. Tree regeneration in two tropical rain forests. MS Thesis. Department of Biology, University of Puerto Rico, Rio Piedras. Waide, R.B., Lugo, A.E., 1992. A research perspective on disturbance and recovery of a tropical montane forest. Tropical Forests in Transition, Birkhauser, Basel/Switzerland, pp. 173– 190. Walker, L.R., 1994. Effects of fern thickets on woodland development on landslides in Puerto Rico. J. Veg. Sci. 5, 525–532. Walker, L.R., Neris, L.E., 1993. Post-hurricane seed rain dynamics in Puerto Rico. Biotropica 25, 408–418. Watt, A.S., 1947. Pattern and process in the plant community. J. Ecol. 35, 1–22. Willig, M.R., Camilo, G.R., 1991. The effect of hurricane hugo on six invertebrate species in the Luquillo experimental forest of Puerto Rico. Biotropica 23, 455–461. Wilson, T.C., Hagerman, A.E., 1990. Quantitative determinates of ellagic acid. J. Agric. Food Chem. 38, 1678–1683. Wold, E.N., Marquis, R.J., 1997. Induced defense in white oak: effects on herbivores and consequences for the plant. Ecology 78, 1356–1369.
Foliar pathogen and insect herbivore effects on two landslide tree species in Puerto Rico Randall W. Myster* Department of Biology, University of Central Oklahoma, Box 89, Edmond, OK 73034, USA Accepted 17 September 2001
Abstract To better understand pathogen/herbivore interactions and landslide regeneration, percent leaf area lost to disease and herbivory on two Puerto Rican trees over a 1-year period was sampled. Cecropia schreberiana saplings lost from 1 to 3% leaf area to pathogens and from 1 to 7% to herbivores. For Inga vera, both sapling and seedling losses to pathogens were minimal, but Inga herbivory losses reached 25% for saplings and 34% for seedlings. The most common fungi on Cecropia leaves were species in the genera Phoma and Phyllosticta, and on Inga leaves was Colletotrichum gloeosporioides. Percent survivorship after 1 year in the field varied among species and life-form (46% for Cecropia saplings, 15% for Inga saplings, 0% for Inga seedlings). There were no effects of pathogens or herbivores on survivorship or growth, but increased levels of herbivory did significantly correlate with total phenolics and condensed tannins in both Inga seedlings and saplings. For both seedlings and saplings of two trees on the neotropic island of Puerto Rico: (1) leaf herbivory was modest and leaf losses to pathogen disease were small; (2) these mechanisms did not affect survivorship or growth; (3) a neotropical tree (I. vera) displayed increased levels of secondary chemicals in its leaves, correlated with increased levels of insect herbivory. # 2002 Elsevier Science B.V. All rights reserved. Keywords: Cecropia schreberiana; Inga vera; Phenolics; Survivorship; Tannins
1. Introduction Whereas ecosystem function and structure may be largely dependent on biotic responses to disturbance (Watt, 1947; Brokaw, 1985; Pickett and White, 1985; Denslow, 1987; Brokaw and Walker, 1991), this relationship may be particularly strong after severe disturbances (Garwood et al., 1979; Sousa, 1984; Waide and Lugo, 1992). For example, landslides (Myster, 1993; Myster and Fernandez, 1995) may influence ecosystem functions such as biodiversity maintenance (e.g., creating regeneration sites for rare * Tel.: þ1-405-974-5725; fax: þ1-405-974-5726. E-mail address: [email protected] (R.W. Myster).
species [ferns: Walker, 1994] or adding species to less severely disturbed areas [hurricanes: Willig and Camilo, 1991]), nutrient cycling and material flow/ redistribution (Swanson et al., 1982; Guariguata, 1990). Because most landslide revegetation involves seeds, seedlings and saplings (advanced regeneration such as resprouting is rare), and because most previous landslide studies have been focused on seeds (Walker and Neris, 1993; Walker, 1994; Myster and Fernandez, 1995; Myster, 1997), studies of seedling and sapling ecology in landslides are needed (Dalling and Tanner, 1995). In addition, these studies can help to address the larger ecological issue of the role of herbivory and leaf disease both in communities and in individual
0378-1127/02/$ – see front matter # 2002 Elsevier Science B.V. All rights reserved. PII: S 0 3 7 8 - 1 1 2 7 ( 0 1 ) 0 0 7 5 7 - 5
232
R.W. Myster / Forest Ecology and Management 169 (2002) 231–242
plants. Many studies have documented patterns of these two mechanisms (e.g., Coley, 1983, 1986; Aide, 1993) but, whether or not they affect plants in an ecological meaningful way, e.g., causing mortality or changes in growth and allocation (Louda and Colling, 1992; Agrawal, 1997; Wold and Marquis, 1997) needs further investigation. This is especially true on neotropic islands, because studies have shown that these mechanisms do affect plant processes on the neotropic mainland (Augspurger, 1983, 1984). More specifically, because pathogens and herbivores often attack plants concurrently, they may: (1) affect the suitability of the plant host for each other (Benedict et al., 1991); (2) induce similar generalized plant responses (Augspurger and Kelly, 1984); (3) lead to related plant defense responses (Coley, 1993); (4) interact in time with herbivores consuming young leaves and pathogens damaging older leaves (Marquis et al., 1993). Therefore, the effect of these two mechanisms, herbivory and pathogenic disease, on the survival, growth and secondary chemistry of seedlings and saplings of two common landslide tree species with differing successional life histories were conducted. This included landslide field sampling and laboratory analysis to examine both the pattern of leaf pathogen and herbivore damage and their effects on landslide tree seedlings and saplings. Specifically, these questions were addressed: 1. Are saplings of Cecropia schreberiana or seedlings and saplings of Inga vera most susceptible to damage? And, what is the monthly variation in that damage in Puerto Rico over 1-year’s time? 2. What are the effects of these two biotic mechanisms on the number of seedling and sapling survivors, and their growth and secondary leaf chemistry?
2. Materials and methods The study was conducted in the Luquillo experimental forest (LEF), a long-term ecological research site of the National Science Foundation, located in the NE corner of Puerto Rico, USA (188200 N, 668000 W). Both study landslides (ES1 and ES3) are located in the lower montane wet forest of the LEF (Ewel and
Whitmore, 1973), which is dominated by tabonuco (Dacryodes excelsa: Waide and Lugo, 1992). Common vegetation occurring on landslides includes the ferns Cyathea arborea and Gleichinia bifida in the upper primary-soil areas, and trees C. schreberiana, Miconia racemosa, I. vera, and Nepsera acuatica in the lower debris areas (Myster and Fernandez, 1995; Myster and Walker, 1997). ES1 and ES3 are both between 10 and 15 years (time since sliding event), occur in the Rio Espiritu Santo watershed at 350 m and 450 m elevation, respectively, and have soils derived from volcanoclastic primary substrate that has weathered into clay Ultisols (Walker, 1994). The average yearly temperature in the LEF is 18 8C and the LEF gets between 2 and 5 m of rainfall a year with a dry season between November and May. In January 1995, 15 saplings (defined as greater than 1 cm basal diameter (bd)) of C. schreberiana (Cecropiaceae), 15 saplings of I. vera (Fabaceae: Mimosoideae; Little and Wadsworth (1989) was used as the taxonomic source for this study and for the nomenclature of all plants used) and 15 I. vera seedlings (defined as less than 1 cm bd) total from the two landslides were selected. Cecropia is a common woody early successional invader in LEF disturbed areas that does not form ant associations in Puerto Rico. Inga grows more slowly, is mid-successional and fixes nitrogen (Viera, 1986; Devoe, 1989), which may lead to nutrient-rich leaves that insects prefer. Consequently, any induction effects of herbivores on tropical tree species may be most easily seen on species like Inga. Pooling samples from both landslides was justified because the landslides are: (1) in the same watershed implying a common soil type and drainage system; (2) of similar size, aspect and slope; (3) located within a few 100 m of each other (Guariguata and Larsen, 1990). Cecropia seedlings were not included in the study, because not enough stems less than 1 cm bd could be found in the two landslides, perhaps due to the fast growth rate of this species (Aide, 1993). The 45 individual plants were found mainly in the lower landslide areas which have a partially closed canopy (from 14 to 30% of full light and between 0.3 and 0.4 red to far-red ratio) and large spatial variation in both nitrogen (from 0.04 to 0.40 kg/m2 to 9 cm depth) and phosphorus (from 0.001 to 0.052 kg/m2 to 9 cm depth) availability (Myster and Fernandez, 1995).
R.W. Myster / Forest Ecology and Management 169 (2002) 231–242
Competition intensity for these resources has never been quantified in landslides. Plants were censused in the middle of each month during 1995, when all new leaves produced since the last sampling were marked with colored wire, and individual plants were scored as either alive or dead. At that time, bd was measured for saplings, and both bd and diameter at 10 cm from the ground was measured for seedlings. For all leaves (new and old) that were fully expanded, I estimated the percentage of the total leaf area that was lost to disease and to herbivory by placing a card divided into 1 cm squares under each leaf. Herbivory usually consisted of holes in the leaf, consistent with insect damage. In contrast pathogenic disease stained the leaf tissue which can lead to necrosis but, perhaps because of the size of the stems, the more severe damping-off fungus (Jarosz and Darelos, 1995) was not seen. Also, it should be remembered that these mechanisms might not be independent because, e.g., several insect species are known to act as a pathogen vector by transporting spores (De la Cruz and Dirzo, 1987). For almost all leaves, the first month of damage was known. In addition, leaves were scored as small, medium or large based on observation of other individuals of the same species. Statistical differences in damage between species, life-stage, biotic agent and leaf-size were investigated using analysis of variance and grouping leaves accordingly (i.e., by species then by life-stage then by leaf size: ANOVA: SAS, 1985). Also, because samplings are not independent among months, differences among months were investigated using repeated measures analysis (Hand and Taylor, 1987). Probability levels are given only for significant results. Microsite differences inside the landslides (e.g., center, edge) could not be investigated statistically because not enough natural seedlings or saplings not occurred in the individual microsites. After 1 year, at the end of 1995, all live leaves on the stems were collected and used for chemical analysis (20 leaves for Cecropia, 52 for Inga saplings, 66 for Inga seedlings), oven dried at 35 8C for 48 h and then ground to a powder (Dudt and Shure, 1993). This low drying temperature permitted more efficient tannin analysis (Swain, 1979). Then, total phenolics were assayed using the Folin Denis technique (Bryant et al., 1987), condensed tannins were estimated as proanthocyanidins using a butanol–HCl technique (Bate-smith,
233
1975, 1981; Porter et al., 1986) and hydrolyzable tannins (ellagitannins only) were assayed under a N2 environment using an acetic acid–sodium nitrate procedure (Bate-smith, 1972, 1977; Wilson and Hagerman, 1990). Fungal species on leaves were identified after incubation on water agar of surface-disinfected leaf samples taken from the leaves at the end of the experiment. In some cases, cultures were transferred to malt agar. An unbalanced, multivariate analysis of variance (MANOVA: SAS, 1985) was used to investigate the effects of pathogens and herbivores on seedling and sapling survivorship, growth, and concentration of secondary compounds. Lack of sufficient replication prevented interactions between pathogens and herbivores from being investigated. Five categories of damage both by pathogens and herbivores (1–20%, 21–40%, 41–60%, 61–80%, 81–100% leaf area lost) were used as the discrete treatments needed for the MANOVA. For the % survivor MANOVAs, the mean leaf loss percentage for all leaves on individual stems available at the end of the experiment was used, or at the last sampling if the stem died, in the treatment groups. For the growth MANOVAs, the mean leaf loss percentage for all the leaves that occurred on an individual stem was used, averaged over the 11-month period, in the treatment groups. The naturally occurring levels of herbivory and pathogenic disease were used instead of creating artificial treatments (e.g., by clipping leaves) in the field. The large number of replicates, in the form of leaves, created sufficient statistical power for the chemical results by adding enough replication for all damage categories. Tukey’s least significant difference (LSD) tests (p < 0:05 level) were used to locate pair wise differences when MANOVAs were significant. All growth rates were computed relative to the initial level of the characteristic scored (e.g., height growth rate ¼ (final height initial height)/initial height/year [Beadle, 1993]) and expressed in cm/cm/year. Because survivorship data may not fit a normal distribution, w2 were also calculated to investigate the effects of the treatments on survivorship (SAS, 1985). 3. Results Leaves of Cecropia saplings sustained little monthly damage from pathogens, having an average
234
R.W. Myster / Forest Ecology and Management 169 (2002) 231–242
of 2%, and a maximum of 15%, leaf area lost. However, leaves of Cecropia saplings had significantly more area lost to herbivores than pathogens (F ¼ 5:58; p < 0:05; mean ¼ 4%; Fig. 1). Leaf
losses to disease were lower for leaves of Inga saplings (mean levels of 1%) compared to Cecropia saplings, but Inga sapling herbivory was significantly greater than both Cecropia herbivory ðmean ¼ 18%Þ and Inga
Fig. 1. Mean disease and herbivory levels on Cecropia sapling leaves (percent of total leaf area lost) by leaf size class (small [S], medium [M], large [L]) measured monthly over 1995.
R.W. Myster / Forest Ecology and Management 169 (2002) 231–242
235
Fig. 2. Mean disease and herbivory levels on Inga sapling leaves (percent of total leaf area lost) by leaf size class measured monthly over 1995.
sapling pathogens (F ¼ 10:9; p < 0:01; Fig. 2). Inga seedlings lost significantly more leaf area to herbivores (30% on average) than Cecropia or Inga saplings ðF ¼ 4:2; p < 0:05Þ. In addition, leaf loss to pathogens on Inga seedlings was low (mean 1%; Fig. 3), where herbivores damaged significantly more leaf area than did pathogens ðF ¼ 13:45; p < 0:01Þ. Inga seedlings had two other significant patterns: (1) there was more leaf area lost to herbivory on larger leaves compared to medium or smaller leaves ðF ¼ 5:56; p < 0:05Þ; (2) there was significantly more leaf area lost to herbivory between the months of May–December compared to other months
(repeated measures analysis F ¼ 4:2; p < 0:05). However, this last result did not correlate with either the wet (June–November) or dry season in Puerto Rico. Pathogenic leaf infection and disease expression has also been sampled in both LEF pastures (unpublished data, author) and LEF gaps (Devoe, 1989), and found to be low suggesting that pathogen infection may not induce changes in secondary metabolites in pastures and gaps. The most common fungi on Cecropia leaves were species in the genera Phoma and Phyllosticta, but some Fusicladium cecropiae was also found. The most common pathogenic fungus on Inga leaves
236
R.W. Myster / Forest Ecology and Management 169 (2002) 231–242
Fig. 3. Mean disease and herbivory levels on Inga seedling leaves (percent of total leaf area lost) by leaf size class measured monthly over 1995.
was Colletotrichum gloeosporioides, but Phyllachora cecropiae was also present. In addition, Xylaria multiplex was isolated from Inga leaves as a nonpathogenic endophyte. All species except Xylaria are pathogenic fungi (D. Jean Lodge, pers. comm.), but not much is known about their effect except that they may vary in the strength of the responses they illicit in the host (Dewit, 1987). The majority of saplings and seedlings survived over the entire sampling period (Fig. 4) but there was large variation between species. Cecropia saplings had the greatest mortality (46%), which occurred mainly during the wet months of June and July, Inga lost two saplings (14% mortality of those stems with the smallest dbh) and no seedlings. Cecropia sapling bd
ranged between 1.13 and 5.45 cm over the study with a mean growth rate of 9.87 cm/cm/year bd, and Inga sapling bd ranged between 1.07 and 2.74 cm with a mean growth rate of 4.68 cm/cm/year bd (Table 1). Inga seedlings ranged between 0.25 and 0.94 cm bd Table 1 Mean growth rates per year (1 S.E.) for all sampled Cecropia saplings, Inga saplings and Inga seedlings Species/life-stage
Diameter (cm)
Height (cm)
Cecropia saplings Inga saplings Inga seedlings
basal: 9:87 0:11 basal: 4:68 0:05 basal: 6:13 0:01 10 cm from base: 8:09 0:02
– – 0:26 0:02 –
R.W. Myster / Forest Ecology and Management 169 (2002) 231–242
237
Fig. 4. Survivorship for Cecropia saplings, Inga saplings, Inga seedlings measured monthly over 1995.
with a mean growth rate of 6.125 cm/cm/year bd, and between 0.32 and 1.02 cm in diameter at 10 cm height with an average growth rate of 8.088 cm/cm/year. Inga seedlings also ranged between 14 and 107 cm in
height with a mean growth rate of 0.261 cm/cm/year. Species differences corresponded strongly with differences in survivorship, while life-stage (seedlings vs. saplings) differences dominated growth differ-
Fig. 5. Mean levels of total phenolics (% TAE) from leaves of Cecropia saplings, Inga saplings and Inga seedlings for each of the five categories (1–20% [black], 21–40% [crossed], 41–60% [reverse diagonal], 61–80% [diagonal], 81–100% [clear]) of leaf loss to herbivory and to pathogens. Different small letters above the histograms indicate significant differences (Tukey’s LSD, p < 0:05) from the other means.
238
R.W. Myster / Forest Ecology and Management 169 (2002) 231–242
Fig. 6. Mean levels of condensed tannins (% QTE) from leaves of Cecropia saplings, Inga saplings and Inga seedlings with the same indicators as in Fig. 5.
Fig. 7. Mean levels of hydrolyzable tannins (mg/g HHDP) from leaves of Cecropia saplings, Inga saplings and Inga seedlings with the same indicators as in Fig. 5.
R.W. Myster / Forest Ecology and Management 169 (2002) 231–242
ences. The results of the MANOVA ðF ¼ 1:2; p ¼ 0:54Þ and w2 analysis ðw2 ¼ 0:98; d:f: ¼ 1; p ¼ 0:56Þ showed that levels of disease or herbivory did not significantly correlate with any of these survivorship or growth results. The level of total phenolics in the leaves of Inga seedlings was greater than in the leaves of either Inga saplings or Cecropia saplings (F ¼ 4:51; p < 0:05; Fig. 5). Further, herbivory on Inga in the higher damage classes correlated with a significant increase in total phenolics at both the seedling and the sapling stages (using leaves with no damage as a control, F ¼ 3:44; p < 0:05) implicating induction. Condensed tannins (Fig. 6) showed many of the same patterns as total phenolics: (1) condensed tannin levels in Inga seedlings were greater (though non-significant) than both Cecropia and Inga saplings; (2) the higher herbivory leaf loss class induced a significant increase in condensed tannins in Inga saplings ðF ¼ 4:84; p < 0:05Þ and Inga seedlings ðF ¼ 5:12; p < 0:05Þ as it did for total phenolics. Hydrolyzable tannin concentrations were not significantly correlated with damage levels (Fig. 7).
4. Discussion The basic leaf pattern results were that (1) Inga leaves generally had more damage than Cecropia leaves, (2) damage from herbivory was more pronounced than from disease, (3) sapling and seedling leaf losses were comparable within species, (4) there was a pattern of larger leaves being preferred over medium and smaller leaves by herbivores and (5) leaf losses to herbivores were greater during the months of May–December compared to other months of the year. Schowalter’s (1994) Puerto Rican study found two of the same patterns: (1) more herbivory on later successional species (Inga in our study) compared to early successional species (Cecropia) and (2) greater species variation than temporal or leaf size variation in tree leaf loss. Inga had the only fungus (Colletotrichum sp.) on its leaves that was also found on LEF landslide seeds (on Palicouria riparia seeds; Myster, 1997) suggesting that few LEF pathogen species attack both seeds and seedlings. Herbivory was assumed to be due to insects because of the lack of native non-volant mammals on the island of Puerto
239
Rico (Waide and Lugo, 1992) and because a variety of Puerto Rican insect taxa and structural groups (Schowalter, 1994; Myster, 1994) were observed on leaves of seedlings and saplings. Although the levels of leaf loss had no effect on survivorship or growth, level of herbivory did correlate with an increase in total phenolics and condensed tannins in both Inga saplings and Inga seedlings. Because Inga fixes nitrogen and has nutrient-rich leaves (Scatena et al., 1993), insects may prefer it and this could help in explaining these species differences and the induction. This may be the first time induction that has been shown for a neotropical species. Although cause and effect cannot be proved, because of the same Inga induction for both total phenolics and condensed tannins, and the multitude of studies showing plants responding to herbivory by increasing levels of secondary compounds (e.g., Swain, 1979; Rhodes, 1983; Agrawal, 1997; Karban et al., 1997; Wold and Marquis, 1997), it is unlikely that these results could be due to something associated with herbivory (e.g., herbivores choosing leaves with high levels of secondary compounds) and not the herbivory itself. Important comparisons can be made between these island results and those dealing with Cecropia spp. and Inga spp. disease and herbivory in disturbed areas on the neotropic mainland, where biotic interactions are supposed to be stronger (Janzen, 1973; Myster, 1997) and, therefore, have a greater effect on ecosystems. The annual levels of Cecropia herbivory were similar to levels found in Mexican gaps (25% on C. obtusifolia; Nunez-farfan, 1989), but higher than the 5.9% herbivory for C. obtusifolia in a Mexican forest (De la Cruz and Dirzo, 1987), and the 5% herbivory in Panama gaps for C. insignis whose mortality rate was also lower compared to this study (Coley, 1983). This reduced herbivory in Panama may reflect a stronger mutualistic defensive relationship between the Azteca ant and Cecropia (Putz and Holbrook, 1988) in Panama compared to Puerto Rico where there is no Cecropia-ant mutualism. Alternatively, even though the levels of hydrolyzable tannins found here in C. schreberiana were similar to those reported by Coley (1986) in Panama, the leaves with these tannin levels did not show reduced insect herbivory. In Costa Rica gaps the level of herbivory on Inga spp. is often greater than these levels but lower in a Mexican forest
240
R.W. Myster / Forest Ecology and Management 169 (2002) 231–242
(6.5%; De la Cruz and Dirzo, 1987), but the amount of Inga sapling total phenolics is similar to these Puerto Rico results (I. densiflora, I. punctata: Koptur, 1984, 1985). Furthermore, both the total phenolic and the condensed tannin levels for Inga seedlings in Puerto Rico were greater than for I. oerstediana in Costa Rica gaps (Nichols-orians, 1991). The same pattern of larger pathogen or herbivore effects on the mainland compared to Puerto Rico holds when comparing the results with those in the mainland understorey, the leaf losses to pathogens here in Puerto Rico were very low (however, damage may be more severe earlier in a seedlings life), but 37% of seedling leaf area can be lost to disease in Brazil (Marquis et al., 1993) and disease can cause up to 81% mortality of seedlings in Panama (damping-off fungal species: Augspurger, 1983, 1984). The results support Dudt and Shure’s (1993, 1994) findings that herbivory levels were unrelated to levels of disease, hydrolyzable tannin and condensed tannin levels were slightly higher in leaves showing moderate pathogen infection leaves (their genus was Cornus), and shade-tolerant species (Inga for us, Cornus for them) had higher levels of total phenolics in their leaves than shade-intolerant species (Cecropia in this study, Liriodendron in theirs). In addition, there was support in total phenolics and condensed tannins (but not in hydrolyzable tannins) for the theory (Coley et al., 1985) that early successional species (i.e., Cecropia) have lower secondary compound levels than later successional species (i.e., Inga). However, there was not supporting evidence in the results for (1) an inverse relationship between levels of condensed and hydrolyzable tannins (Dudt and Shure, 1994), (2) an increase of phenolics or tannins associated with levels of pathogens, (3) an increase of hydrolyzable tannins induced by herbivores (some evidence for Cornus in Dudt and Shure, 1993), (4) herbivores preferring young leaves while pathogens preferring mature ones (Marquis et al., 1993), (5) most damage occurring during the first month after expansion, (6) the percentage of leaf lost influencing growth rate (Aide, 1993), or (7) pathogen levels affect plant host preference by herbivores or visa versa (Dudt and Shure, 1993), which could reflect the food value of the host species (Clay et al., 1993). Finally, pathogen levels were probably too low in this study (similar to another LEF study by Devoe, 1989 and unpublished
data in pastures by the primary author) to test whether light-seeded early successional species lack resistance to seedling pathogens (Augspurger and Kelly, 1984). The results show an average mortality rate of 20% per year for the sampled seedlings and saplings, similar to landslide seedlings and saplings in Jamaica (Dalling and Tanner, 1995). Although results suggest a relatively minor role for herbivory and pathogenesis in LEF landslides compared to other mechanisms in determining survivorship, they may be important by acting indirectly and changing competitive hierarchies among plants (Crawley, 1983; Schowalter, 1985; Myster and McCarthy, 1989; Clay et al., 1993). Indeed, plant–plant competition may be a key successional landslide regeneration mechanism for a number of reasons: (1) landslides have extreme spatial variation and patchiness in both the nutrients which plants compete for and in the availability of the VA-mycorrhizae which influences their nutrient uptake (Myster and Fernandez, 1995), (2) field experiments show that landslide trees compete for patchy distributions of soil nutrients and light (Fetcher et al., 1996), (3) field studies suggest that landslide ferns (e.g., Dicranopteris pectinata) inhibit tree seedling growth (e.g., Tabebuia heterophylla) through light competition (Walker, 1994) and (4) Cecropia and Inga are common competitors with other species and may inhibit many of them during succession (author, unpublished data).
Acknowledgements First, I thank Liz A. Sanchez for her help in laboratory analysis and D. Jean Lodge for her help in identifying fungal genera. I also wish to thank Maria Aponte for field assistance, Ligia Lebron for laboratory assistance and Albert Muniz for help with the figures. Finally, I thank J. Thompson, D.J. Lodge, C. Augspurger, R. Marquis, P. Coley and D. Shure for commenting on earlier drafts of the manuscript. This research was performed under grant BSR-8811902 from the National Science Foundation to the Institute for Tropical Ecosystem Studies, University of Puerto Rico, and the International Institute of Tropical Forestry as part of the Long-term Ecological Research Program in the Luquillo Experimental Forest. Additional support was provided by the Forest Service
R.W. Myster / Forest Ecology and Management 169 (2002) 231–242
(US Department of Agriculture) and the University of Puerto Rico. References Agrawal, A.A., 1997. The benefits of induced plant responses: fitness effects of induction in the presence and absence of herbivores. Bull. Ecol. Soc. Am. 78, 43. Aide, T.M., 1993. Patterns of leaf development and herbivory in a tropical understory community. Ecology 74, 455–466. Augspurger, C.K., 1983. Offspring recruitment around tropical trees: changes in cohort distance with time. Oikos 40, 189–196. Augspurger, C.K., 1984. Seedling survival of tropical tree species: interactions of dispersal distance, light-gaps and pathogens. Ecology 65, 1705–1712. Augspurger, C.K., Kelly, C.K., 1984. Pathogen mortality of tropical tree seedlings: experimental studies of the effects of dispersal distance, seedling density, and light conditions. Oecologia 61, 211–217. Bate-smith, E.C., 1972. Detection and determination of ellagitannins. Phytochemistry 11, 1153–1156. Bate-smith, E.C., 1975. Phytochemistry of proanthocyanidins. Phytochemistry 14, 1107–1113. Bate-smith, E.C., 1977. Astringent tannins of Acer species. Phytochemistry 16, 1421–1426. Bate-smith, E.C., 1981. Astringent tannins of the leaves of Geranium species. Phytochemistry 20, 211–216. Beadle, C.L., 1993. Growth analysis. Photosynthesis and production in a changing environment. In: Hall, D.D., Scurlock, J.M.O., Bolhar-Nordenkampf, H.R., Leegood, R.C., Lang, S.P. (Eds.), A Field and Laboratory Manual. Chapman & Hall, London, pp. 85–98. Benedict, J.B., Chang, J.F., Bird, L.S., 1991. Influence of plant microflora on insect–plant relationships in Gossypium hirsutum. In: Barbosa, P., Krischik, V.A., Jones, C.G. (Eds.), Microbial Mediation of Plant–Herbivore Interactions. Wiley, New York, pp. 273–303. Brokaw, N.V.L., 1985. Treefalls, regrowth and community structure in tropical forests. In: Pickett, S.T.A., White, P.S. (Eds.), The Ecology of Natural Disturbance and Patch Dynamics. Academic Press, Orlando, FL, pp. 53–69. Brokaw, N.V.L., Walker, L.R., 1991. Summary of the effects of Caribbean hurricanes on vegetation. Biotropica 23, 442–447. Bryant, J.P., Chapin III, F.S., Reichardt, P.B., Clausen, T.P., 1987. Responses of winter chemical defense in Alaska paper birch and green alder to manipulation of plant carbon-nutrient balance. Oecologia 72, 510–514. Clay, K., Marks, S., Cheplick, G.P., 1993. Effects of insect herbivory and fungal endophyte infection on competitive interactions among grasses. Ecology 74, 1767–1777. Coley, P.D., 1983. Intraspecific variation in herbivory on two tropical tree species. Ecology 64, 426–433. Coley, P.D., 1986. Costs and benefits of defense by tannins in a neotropical tree. Oecologia 70, 238–241. Coley, P.D., 1993. Gap size and plant defenses. TREE 8, 12–16.
241
Coley, P.D., Bryant, J.P., Chapin, F.S., 1985. Resource availability and plant antiherbivore defense. Science 230, 895–899. Crawley, M.J., 1983. Herbivory: The Dynamics of Animal–Plant Interactions. University of California Press, Los Angeles, CA. Dalling, J.W., Tanner, E.V.J., 1995. An experimental study of regeneration on landslides in montane rain forest in Jamaica. J. Ecol. 83, 55–64. De la Cruz, M., Dirzo, R., 1987. A survey of the standing levels of herbivory in seedlings from a Mexican rainforest. Biotropica 19, 98–106. Denslow, J.S., 1987. Tropical rainforest gaps and tree species diversity. Ann. Rev. Ecol. Syst. 18, 431–451. Devoe, N.N., 1989. Differential seedling and regeneration in openings and beneath closed canopy in sub-tropical wet forest. Ph.D. Dissertation. School of Forestry and Environmental Studies, Yale University, New Haven, CT. Dewit, P.J.G.M., 1987. Specificity of active resistance mechanisms in plant–fungus interactions. In: Pegg, G.F., Ayers, P.G. (Eds.), Fungal Infections of Plants. Cambridge University Press, New York, pp. 1–22. Dudt, J.F., Shure, D.J., 1993. The effect of anthracnose (Discula destructiva) infection on plant–herbivore interactions in dogwood (Cornus florida). Oecologia 96, 108–113. Dudt, J.F., Shure, D.J., 1994. The influence of light and nutrients on foliar phenolics and insect herbivory. Ecology 75, 86–98. Ewel, J.J., Whitmore, J.L., 1973. The ecological life zones of Puerto Rico and the Virgin islands. United States Forest Service Research Paper ITF-18. Institute of Tropical Forestry, Rio Piedras, PR. Fetcher, N., Haines, B.L., Cordero, R.A., Lodge, D.J., Walker, L.R., Fernandez, D.S., Lawrence, W.T., 1996. Responses of tropical plants to mineral nutrients on a landslide in Puerto Rico. J. Ecol. 84, 123–134. Garwood, N.C., Janos, D.P., Brokaw, N.V.L., 1979. Earthquake caused landslides: a major disturbance to tropical forests. Science 205, 997–999. Guariguata, M.R., 1990. Landslide disturbance and forest regeneration in the upper Luquillo mountains of Puerto Rico. J. Ecol. 78, 814–832. Guariguata, M.R., Larsen, M.C., 1990. Preliminary map showing locations of landslides in El Yunque Quadrangle, Puerto Rico. US Geological Survey Open File Report 89-257. Hand, D.J., Taylor, C.C., 1987. Multivariate Analysis of Variance and Repeated Measures. Chapman & Hall, New York. Janzen, D.H., 1973. Sweep samples of tropical foliage insects: effects of season, vegetation types, elevation, time of day and insularity. Ecology 54, 687–701. Jarosz, A.M., Darelos, A.L., 1995. Effects of disease in wild plant populations and the evolution of pathogen aggressiveness. New Phytol. 129, 371–387. Karban, R., Agarawal, A.A., Mangel, M., 1997. The benefits of induced defences against herbivores. Ecology 78, 1351–1355. Koptur, S., 1984. Experimental evidence for defense of Inga (Mimosoideae) saplings by ants. Ecology 65, 1787–1793. Koptur, S., 1985. Alternative defenses against herbivores in Inga (Mimosoideae) over an elevational gradient. Ecology 66, 1639–1650.
242
R.W. Myster / Forest Ecology and Management 169 (2002) 231–242
Little, E.L., Wadsworth, F.H., 1989. Common trees of Puerto Rico and the Virgin Islands. Agriculture Handbook No. 249. US Department of Agriculture, Washington, DC. Louda, S.M., Colling, S.K., 1992. Plant resistance to insect herbivores: a field test of the environmental stress hypothesis. Ecology 73, 153–169. Marquis, R.J., Diniz, I.R., Morais, H.C., 1993. Interspecific patterns in folivory and pathogen attack for Brazilian cerrado trees. Bull. Ecol. Soc. Am. 74, 344. Myster, R.W., 1993. Spatial heterogeneity of seed rain, seed pool and vegetative cover on two Monteverde landslides, Costa Rica. Brenesia 39–40, 137–145. Myster, R.W., 1994. Landslide insects show small differences between an island (Puerto Rico) and the mainland (Costa Rica). Acta Cientifia 8, 105–113. Myster, R.W., 1997. Seed predation, disease and germination on landslides in neotropical lower montane wet forest. J. Veg. Sci. 8, 55–64. Myster, R.W., Fernandez, D.S., 1995. Spatial gradients and patch structure on two landslides in Puerto Rico. Biotropica 27, 149–159. Myster, R.W., McCarthy, B.C., 1989. Effects of herbivory and competition on survival of Carya tomentosa (Juglandaceae) seedlings. Oikos 56, 145–148. Myster, R.W., Walker, L.R., 1997. Plant successional pathways on Puerto Rican landslides. J. Trop. Ecol. 13, 165–173. Nichols-orians, C.M., 1991. The effects of light on foliar chemistry growth and susceptibility of seedlings of a canopy tree to an Attine ant. Oecologia 86, 552–560. Nunez-farfan, J., 1989. Leaf survival in relation to herbivory in two tropical pioneer species. Oikos 55, 71–74. Pickett, S.T.A., White, P.S., 1985. The Ecology of Natural Disturbance and Patch Dynamics. Academic Press, New York. Porter, L.J., Hrstich, L.N., Chan, B.G., 1986. The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry 25, 223–230. Putz, F.E., Holbrook, N.M., 1988. Further observations on the dissolution of mutualism between Cecropia and its ants: the Malaysian case. Oikos 53, 121–125. Rhodes, D.F., 1983. Herbivore population dynamics and plant chemistry. In: Denno, R.F., McClure, B. (Eds.), Variable Plants and Herbivores in Natural and Managed Systems, Academic Press, New York, pp. 155–220.
SAS Institute, 1985. User’s Guide: Statistics, 5th Edition. SAS Institute, Inc., Cary, NC. Scatena, F.N., Silver, W., Siccama, T., Johnson, A., Sanchez, M.J., 1993. Biomass and nutrient content of the Bisley experimental watersheds, Luquillo experimental forest, Puerto Rico, before and after hurricane hugo, 1989. Biotropica 25, 15–27. Schowalter, T.D., 1994. Invertebrate community structure and herbivory in a tropical rain forest canopy in Puerto Rico following hurricane hugo. Biotropica 26, 312–319. Sousa, W.P., 1984. The role of disturbance in natural communities. Ann. Rev. Ecol. Syst. 15, 353–391. Swain, T., 1979. Tannins and lignins. In: Rosenthal, G.A., Janzen, D.H. (Eds.), Herbivores: Their Interactions with Secondary Plant Metabolites. Academic Press, New York, pp. 657– 682. Swanson, F.J., Fredriksen, R.L., McCorison, P., 1982. Material transfer in a western Oregon forested watershed. Analysis of Coniferous Forest Ecosystems in the Western United States. US/IBP Synthesis Ser. 14. Hutchinson Ross Publishing Co., Stroudsburg, PA (Chapter 8). Viera, I.E.P., 1986. Tree regeneration in two tropical rain forests. MS Thesis. Department of Biology, University of Puerto Rico, Rio Piedras. Waide, R.B., Lugo, A.E., 1992. A research perspective on disturbance and recovery of a tropical montane forest. Tropical Forests in Transition, Birkhauser, Basel/Switzerland, pp. 173– 190. Walker, L.R., 1994. Effects of fern thickets on woodland development on landslides in Puerto Rico. J. Veg. Sci. 5, 525–532. Walker, L.R., Neris, L.E., 1993. Post-hurricane seed rain dynamics in Puerto Rico. Biotropica 25, 408–418. Watt, A.S., 1947. Pattern and process in the plant community. J. Ecol. 35, 1–22. Willig, M.R., Camilo, G.R., 1991. The effect of hurricane hugo on six invertebrate species in the Luquillo experimental forest of Puerto Rico. Biotropica 23, 455–461. Wilson, T.C., Hagerman, A.E., 1990. Quantitative determinates of ellagic acid. J. Agric. Food Chem. 38, 1678–1683. Wold, E.N., Marquis, R.J., 1997. Induced defense in white oak: effects on herbivores and consequences for the plant. Ecology 78, 1356–1369.