Interspecific variation and ontogenetic change in antiherbivore defense in myrmecophytic Macaranga species

The present study examined whether or not coexisting congeneric plant species have different defense strategies against herbivores, and the intensity of defense changes ontogenetically. We focused on nine myrmecophytic Macaranga species and estimated the intensity of non-biotic and biotic defense by the degree of leaf damage in ant-free and ant-occupied plants, respectively. Ant colonization of myrmecophytic Macaranga species occurred in the early stage of plant development (5–50 cm-tall seedlings). Following the colonization, damage by leaf eaters was minimized and stable during the ontogenetic development of the host plants due to protection by ants. In ant-free trees, however, herbivore damage was immense in seedlings and decreased as trees grew. Interspecific comparison of leaf damage and herbivore fauna supported that coexisting congeneric plants differ in their types of non-biotic (chemical/structural) defense: without ant protection, Macaranga beccariana, for example, was somewhat resistant to leaf eaters but susceptible to gall-makers, Macaranga trachyphylla was heavily infested by generalist leaf eaters, and Macaranga winkleri was exploited by ant-predatory birds. Despite these variations in chemical/structural defense, ant-colonized plants were generally well defended by ants against all kinds of herbivores. This suggests that the individual host-specific ant mutualists are well adapted to deter the chemically or structurally adapted herbivores. These results imply that in the history of diversification in the Macaranga–ant–herbivore system, a sequence of mutual counter adaptation took place not only between plants and herbivores but also between ants and herbivores.     

A chloroplast genealogy of myrmecophytic Macaranga species (Euphorbiaceae) in Southeast Asia reveals hybridization, vicariance and long-distance dispersals

Macaranga (Euphorbiaceae) includes about 280 species with a palaeotropic distribution. The genus not only comprises some of the most prominent pioneer tree species in Southeast Asian lowland dipterocarp forests, it also exhibits a substantial radiation of ant-plants (myrmecophytes). Obligate ant-plant mutualisms are formed by about 30 Macaranga species and 13 ant species of the genera Crematogaster or Camponotus. To improve our understanding of the co-evolution of the ants and their host plants, we aim at reconstructing comparative organellar phylogeographies of both partners across their distributional range. Preliminary evidence indicated that chloroplast DNA introgression among closely related Macaranga species might occur. We therefore constructed a comprehensive chloroplast genealogy based on DNA sequence data from the noncoding ccmp2, ccmp6, and atpB-rbcL regions for 144 individuals from 41 Macaranga species, covering all major evolutionary lineages within the three sections that contain myrmecophytes. A total of 88 chloroplast haplotypes were identified, and grouped into a statistical parsimony network that clearly distinguished sections and well-defined subsectional groups. Within these groups, the arrangement of haplotypes followed geographical rather than taxonomical criteria. Thus, up to six chloroplast haplotypes were found within single species, and up to seven species shared a single haplotype. The spatial distribution of the chloroplast types revealed several dispersals between the Malay Peninsula and Borneo, and a deep split between Sabah and the remainder of Borneo. Our large-scale chloroplast genealogy highlights the complex history of migration, hybridization, and speciation in the myrmecophytes of the genus Macaranga. It will serve as a guideline for adequate sampling and data interpretation in phylogeographic studies of individual Macaranga species and species groups.     

Host‐plant dissections reveal contrasting distributions of Crematogaster ants and their symbionts in two myrmecophytic Macaranga species

1. Ant–plant mutualisms are among the most widespread and ecologically important insect–plant interactions in the tropics. The multitrophic mutualism involving Macaranga plants (Euphorbiaceae) and Crematogaster ants (Formicidae) is the most diverse in Southeast Asia. This interaction also includes trophobiotic scale insects (Coccidae) and nematodes inhabiting ant refuse piles. 2. Here two myrmecophytic systems were compared, Macaranga trachyphylla with Crematogaster captiosa (Mt + Cc) and Macaranga beccariana with Crematogaster decamera (Mb + Cd), using a fine‐scale dissection of the stems. For the two plant species, for each internode, both contents (ants, coccids, refuse piles) and structure (internode height, numbers of open and occluded ant holes) were recorded. 3. There were significant patterns in the vertical distribution of ant colonies and their symbionts in the plant stems. Most coccids were kept in the highest sections of both systems, although Mb + Cd hosted a broader range of coccid species than Mt + Cc. Three nematode species were recorded, but with a rather low specificity to plant or ant species. Furthermore, the fine‐scale distribution showed aggregation of closed holes with ant brood and separation of nematode‐infested refuse piles from eggs. 4. The results of this study indicate that ants manipulate spatial colony structure via distribution of brood, holes and the symbionts. It is suggested that ants optimise the location of refuse piles and occluded holes via spatial heterogeneity in their distribution among internodes. This paper discusses the protective role of occluded holes and demonstrates some general interactions with other symbiotic fauna.     

Evolution of myrmecophytism in western Malesian Macaranga (Euphorbiaceae)

Plants inhabited by ants (myrmecophytes) have evolved in a diversity of tropical plant lineages. Macaranga includes approximately 300 paleotropical tree species; in western Malesia there are 26 myrmecophytic species that vary in morphological specializations for ant association. The origin and diversification of myrmecophytism in Macaranga was investigated using phylogenetic analyses of morphological and nuclear ITS DNA characters and studies of character evolution. Despite low ITS variation, the combined analysis resulted in a well-supported hypothesis of relationships. Mapping myrmecophytism on all most parsimonious trees resulting from the combined analysis indicated that the trait evolved independently between two and four times and was lost between one and three times (five changes). This hypothesis was robust when tested against trees constrained to have three or fewer evolutionary transformations, although increased taxon sampling for the ITS analysis is required to confirm this. Mapping morphological traits on the phylogeny indicated that myrmecophytism was not homologous among lineages; each independent origin involved a suite of different specializations for ant-plant association. There was no evidence that myrmecophytic traits underwent sequential change through evolution; self-hollowing domatia evolved independently from ant-excavated domatia, and different food-body production types evolved in different lineages. The multiple origins of myrmecophytism in Macaranga were restricted to one small, exclusively western Malesian lineage of an otherwise large and nonmyrmecophytic genus. Although the evolution of aggregated food-body production and the formation of domatia coincided with the evolution of myrmecophytism in all cases, several morphological, ecological, and biogeographic factors appear to have facilitated and constrained this radiation of ant-plants.     

The diversity of ant–plant interactions in the rainforest understorey tree, Ryparosa (Achariaceae): food bodies, domatia, prostomata, and hemipteran trophobionts

Ant–plant relationships, with variability in both intimacy and the trophic structure of associations, are described for the Austro-Malesian rainforest tree genus Ryparosa (Achariaceae). The range of associations involves opportunistic interactions between plants and foraging ants, mediated by food bodies, and tighter associations in which ant colonies, tending hemipteran trophobionts, reside permanently in plant structures with different degrees of adaptation to house ants. Our study provides strong baseline data to suggest that Ryparosa could become a new model system for examining the evolutionary radiation of ant-related traits. To define the diversity of ant–plant associations in Ryparosa , we first present a review of ant-plant terminology and an outline of its use in this study. Field studies of ant interactions with food bodies in myrmecotrophic R. kurrangii from Australia and the association between myrmecoxenic R. fasciculata and two Cladomyrma plant-ant species on the Malay Peninsula provide detailed examples of ant–plant interactions. An examination of herbarium material revealed a diverse range of ant–plant associations in other Ryparosa taxa. All 27 species had evidence of food body production, seven species had evidence of stem inhabitation by ants, five species had specialized stem domatia, and the domatia of R. amplifolia featured prostomata. Variation in the specificity of Ryparosa ant–plant interactions is discussed in relation to known ant partners and other ant–plant associations.  © 2007 The Linnean Society of London, Botanical Journal of the Linnean Society , 2007, 154 , 353–371.     

Carbon and nitrogen contents of food bodies in three myrmecophytic species of Macaranga: implications for antiherbivore defense mechanisms

In Macaranga myrmecophytes, differences in the production of the food bodies (FBs), on which symbiont ants feed, may relate to the intensity of antiherbivore defense by the ants. Interspecific comparisons among Macaranga species on such a mutualistic cost give important information on their strategies and evolution of antiherbivore defense. In this study, the carbon and nitrogen contents of FBs as well as the production rate of FBs were measured in three Macaranga species, M. winkleri, M. trachyphylla, and M. beccariana. There were significant differences in the production rates of FBs among species; the investment in FBs was greater in the Macaranga species in which ant defenses were more intensive. The carbon and nitrogen contents of FBs were significantly different among the three species, although they did not match the intensity of ant defense; the nitrogen content, especially, was greatest in the species of least intensive ant defense. It is suggested that Macaranga plants may have differentiated in the dependence on ant defense by controlling the total amount of nitrogen of FBs, not simply by nitrogen content.     

Production of food bodies on the reproductive organs of myrmecophytic Macaranga species (Euphorbiaceae): effects on interactions with herbivores and pollinators

In protective ant–plant mutualisms, plants offer ants food (such as extrafloral nectar and/or food bodies) and ants protect plants from herbivores. However, ants often negatively affect plant reproduction by deterring pollinators. The aggressive protection that mutualistic ants provide to some myrmecophytes may enhance this negative effect in comparison to plant species that are facultatively protected by ants. Because little is known about the processes by which myrmecophytes are pollinated in the presence of ant guards, we examined ant interactions with herbivores and pollinators on plant reproductive organs. We examined eight myrmecophytic and three nonmyrmecophytic Macaranga species in Borneo. Most of the species studied are pollinated by thrips breeding in the inflorescences. Seven of eight myrmecophytic species produced food bodies on young inflorescences and/or immature fruits. Food body production was associated with increased ant abundance on inflorescences of the three species observed. The exclusion of ants from inflorescences of one species without food rewards resulted in increased herbivory damage. In contrast, ant exclusion had no effect on the number of pollinator thrips. The absence of thrips pollinator deterrence by ants may be due to the presence of protective bracteoles that limit ants, but not pollinators, from accessing flowers. This unique mechanism may account for simultaneous thrips pollination and ant defense of inflorescences.     

Variation in juvenile survival and related physiological traits among dipterocarp species co‐existing in a Bornean forest

Question: What environmental factors and physiological traits determine the juvenile survival rates of 11 dipterocarp species (Dipterocarpaceae) co-occurring in a Bornean tropical rain forest? Location: Tropical northwestern Borneo. Methods: In 248 quadrats, distributed over 12 ha, the juvenile (height< 2.0 m) survival of 11 shade-tolerant dipterocarp species was monitored for one year. The probability of survival for each species was expressed as a logistic function of plant height and three environmental factors: canopy openness, soil water potential and conspecific individual density. The correlation between survival under shaded conditions and several physiological traits of juveniles was tested by normal Pearson correlation and a phylogeny based manner using independent contrasts. Results: Seven species had increased survival under more open canopies, one species had increased and two species had decreased survival at drier sites. Six species had higher survival as the density of conspecifics increased, whereas two species had lower survival. The magnitudes of the effects for the three environmental factors were similar. However, the interspecific difference in survival was largely determined by a dependence of small seedlings on the light environment. Survival under low light was correlated positively with root dry mass and negatively with total leaf area of juveniles. Conclusions: Responses of seedlings to the fine-scale gradient of light availability were considerably different among the 11 species. Species that suffered increased mortality under low light had a set of structural traits that would potentially allow rapid growth under bright conditions. Differential performance along the light gradient may contribute to the stable coexistence of these species.     

Seasonality and vertical structure of light-attracted insect communities in a dipterocarp forest in Sarawak

Nocturnal flying insects were collected monthly for 13 months using ultra violet light-traps set at various vertical levels in a weakly-seasonal, tropical lowland dipterocarp forest in Sarawak, Malaysia. Abundance, faunal composition, size distribution and guild structure of these samples were analyzed with respect to temperal and vertical distributions. The nocturnal flying insect community in the canopy level was highly dominated by fig wasps (84%) in individual number, and by scarabaeid beetles (28%) in weight. A principal component analysis on monthly catches detected non-random, seasonal trends of insect abundance. The first two principal trends were an alternation of wetter (September to January) and less wet seasons (February to August) and an alternation between the least wet (January to March) and the other seasons. Many insect groups were less abundant in the least wet season than the other seasons, whilst inverse patterns were found in Scarabaeidae and Tenebrionidae. Significantly positive and negative correlations between monthly catch and rainfall were detected only in ovule-feeders and in phloem-feeders, respectively. Delayed, significant negative correlations between monthly catch and 1–3 month preceding rainfall were more frequently detected in phytophages, phloem-feeders, seed-feeders, wood-borers and scavengers. The peak in abundance along vertical levels were found at the canopy level (35 m) for phloem-, ovule-, seed-, root-, fungal-feeders and nectar collectors, at an upper subcanopy level (25 m) for scavengers and aquatic predators, and at a middle subcanopy level (17 m) for ants. Catches at the emergent level (45 m) did not exceed those at the canopy level.     

温带森林阔叶植物幼苗叶经济谱及其与防御性状的关系

植物叶片功能性状之间的权衡关系一直是生态学研究的热点问题。其中叶经济谱相关性状的研究较多, 但叶片防御性状方面的研究, 尤其是幼苗阶段的研究较少。该研究以黑龙江凉水国家级自然保护区典型阔叶红松(Pinus koraiensis)林和谷地云冷杉林内共有的8种阔叶乔木和11种阔叶灌木物种的幼苗叶片为研究对象, 通过测定5个叶经济谱性状和4个叶片防御性状, 分析了叶性状在不同生活型、林型间的差异以及性状之间的协调关系。结果表明: 所有叶片性状在乔木和灌木幼苗之间不存在显著差异, 谷地云冷杉林中的幼苗的叶总酚含量和单宁含量显著高于阔叶红松林中的幼苗, 其原因为谷地云冷杉林林下光照强度弱于阔叶红松林, 且空气和土壤湿度较高, 该环境更有利于自然天敌的聚集, 可能有更强的天敌破坏效应, 而这种更强的生物相互作用反过来驱动幼苗提高其防御能力; 幼苗叶绿素含量与比叶面积呈极显著正相关关系, 与叶氮含量、叶磷含量呈显著正相关关系; 幼苗叶氮含量与叶磷含量呈显著正相关关系; 幼苗叶防御性状之间呈显著正相关关系; 幼苗叶绿素含量与叶总酚含量、单宁含量和类黄酮含量呈显著负相关关系, 叶氮含量与叶总酚含量、单宁含量呈显著负相关关系, 与类黄酮含量呈极显著负相关关系; 说明幼苗叶经济谱性状与防御性状之间存在权衡关系, 即对叶片碳代谢性状的更多投资意味着对叶防御性状更少的投资; 乔、灌木幼苗具有相似的资源利用策略。     

Various population fluctuation patterns of light-attracted beetles in a tropical lowland dipterocarp forest in Sarawak

The population fluctuation pattern of light-attracted beetles was studied from August 1992 to September 1998 (for 73 months) using ultraviolet light-traps set at three vertical levels in a tropical lowland dipterocarp forest in Sarawak, Malaysia. During our study, a general flowering occurred from April to July in 1996, and flowering on a small scale in 1997 and 1998. We analyzed the data for eight scarabaeid and six meloid species, some of which were anthophilous species. Various fluctuation patterns were observed among the beetle species in aspects of both seasonality and correlation with the supraannual phenological pattern. Three large chafer species (Scarabaeidae, Melolonthini) showed a clear seasonal fluctuation pattern with a peak once from March to May every year, the peak monthly catch greatly fluctuating annually. Other scarabaeid beetles did not show such a clear seasonal population pattern and hardly fluctuated annually. Populations of an anthophilous scarabaeid species, Parastasia bimaculata, a specific pollinator of Homalomena propinqua (Araceae), hardly fluctuated, probably because of its response to the constant flowering of its floral hosts. Monthly catches of an anthophilous scarabaeid, Anomala sp., and meloid beetles showed clear supraannual patterns in response to the general flowering and were significantly correlated with the flowering intensity with or without a lag of a month. The fluctuation pattern of meloids suggests a supraannual population fluctuation pattern of their hosts, i.e., megachilid/anthophorid bees. Received: November 9, 1999 / Accepted: February 8, 2000     

Forest Structure and Primary Productivity in a Bornean Heath Forest

Aboveground forest structure, biomass, and primary productivity in a tropical heath forest in Central Kalimantan (Indonesian Borneo) were examined using data from 1-ha plots and stand-level allometric equations developed from harvested tree samples. The study site experienced a severe drought in 1997–1998 associated with the El Niño Southern Oscillation event. The drought effect on heath forest productivity was also assessed by evaluating changes in wood mass increment rates. Allometric relationships suggested that heath forest trees had leaves with smaller specific leaf area (SLA), and large heath forest trees allocate more to leaf mass compared to mixed dipterocarp forest trees. Aboveground biomass (for trees ≥ 4.8 cm DBH) in two 1-ha plots, P1 and P4, totaled 244.8 and 232.0 Mg/ha. Aboveground wood mass increment rate was –0.1 and 4.7 Mg/ha/yr in P1 and P4 during the drought period (from February to August 1998), while it quickly recovered to 8.1 and 8.5 Mg/ha/yr during the post-drought period (from August 1998 to August 1999 for P1 and from August 1998 to November 1999 for P4). This suggests a severe impact of the drought on heath forest productivity. Leaf characteristics of heath forest such as small SLA and long-lived leaves probably play a significant role in effective assimilation and maintenance of heath forest productivity under stressful conditions.     

Effects of fires on butterfly assemblages in lowland dipterocarp forest in East Kalimantan

The post‐fire butterfly fauna in lowland dipterocarp forest of the Bukit Soeharto Education Forest (BSEF), East Kalimantan, Indonesia, was assessed during the period November 1998–April 2000 by means of consecutive Malaise trap samples, with supplementary field observations for March–April 1999. A total of 514 butterflies belonging to 61 species and representing six families were caught in the traps. Melanitis leda (Nymphalidae: Satyrinae), Charaxes bernardus (Nymphalidae: Charaxinae), and Danaus genutia (Nymphalidae: Danainae) were the species most frequently caught (60, 52 and 47 individuals, respectively), representing 31% of the total. These three species are generalists and “disturbance indicators” for tropical rainforest, being characteristic of disturbed or secondary forests, being distributed widely, and having larvae that feed on a wide range of host plants. In contrast, other species, such as Trogonoptera brookiana and Troides amphrysus, were recorded before the fires but were not recorded again afterwards. The pre‐ and post‐fire butterfly fauna of East Kalimantan were compared on the basis of butterfly specimens deposited in the Tropical Rain Forest Research Center that were collected in and around the Bukit Soeharto Education Forest before the fires (1988–1995). On the basis of the post‐fire survey, based on Malaise trap samples and field observations, only 43% of the butterfly species (not including Lycaenidae and Hesperiidae) were confirmed to have persisted. The data suggest that refugia that are not affected by fire are necessary for the conservation of specialist butterflies, as well as many other forms of wildlife.     

Species number, species abundance and body length relationships of arboreal beetles in Bornean lowland rain forest trees

ABSTRACT.

• 1 The relationships between number of species, abundance per species, and body length are examined for 859 species of beetles in samples of arthropods collected from ten Bornean lowland forest trees by insecticide fogging. Similar relationships are examined for different feeding guilds of these beetles, and for those beetles from different species of trees.
• 2 The data are used to construct four interrelated graphs, namely species: abundance, species: body length, population abundance: body length and total number of individuals: body length distributions.
• 3 In contrast to a number of previous studies, no consistent linear relationship between population density and body length was found for the Bornean beetles and it is suggested that, as in birds, the added dispersal ability of flight reduces critical population densities necessary for persistence in small species. Previous relationships between body weight and population abundance may also be artefacts of the way in which data were gathered.
• 4 Despite large samples, we failed to locate the mode in plots of the number of species in each abundance category (species: abundance distribution).
• 5 Species: body length and total number of individuals: body length plots were similar to those found in previous studies, although using data for Coleoptera alone may have produced a steeper decline in the total number of individuals as body size increases than is apparent in samples of all arthropods.
• 6 We present the first three-dimensional graph relating numbers of species, body lengths and population abundances. The surface of this three-dimensional relationship is relatively simple.

     

AFLP analysis of phylogenetic relationships among myrmecophytic species of Macaranga (Euphorbiaceae) and their allies

The palaeotropic pioneer tree genus Macaranga Thouars (Euphorbiaceae) is characterized by various types of mutualistic interactions with specific ant partners (mainly Crematogaster spp.). About 30 species are obligate ant-plants (myrmecophytes). We used amplified fragment length polymorphism (AFLP) markers to assess phylogenetic relationships among 108 Macaranga specimens from 43 species, including all available taxa from the three sections known to contain myrmecophytes. Eight primer combinations produced 426 bands that were scored as presence/absence characters. Banding patterns were analyzed phenetically, cladistically and by principal coordinates analysis. Monophyly of section Pruinosae is clearly supported. There is also good evidence for a monophyletic section Pachystemon that includes the puncticulata group. The monophyly of section Winklerianae and relationships between the three sections remain ambiguous. Section Pachystemon is subdivided into four well-supported monophyletic subclades that presumably correspond to taxonomic entities.We acknowledge the support by the Deutsche Forschungsgemeinschaft (DFG Fi606/4-1, DFG We1830/2-1, 4-1 and 4-2), which in part was granted in the frame of the DFG-SPP 1127 Radiations: origins of biological diversity. Part of the plant material was kindly supplied by Dr. H. Feldhaar (University of Würzburg), Dr. U. Moog (University of Kassel) and Dr. F. Slik (Leiden University Branch, Nationaal Herbarium Nederland). We thank the University of Malaysia (Dr. Rosli b. Hashim) and Taman Taman Sabah (Datuk Lamri Ali; Dr. J. Nais) for permits and logistic support, and EPU for permission to conduct research in Malaysia.     

Distance-dependence in herbivory and foliar condition for juvenile Shorea trees in Bornean dipterocarp rain forest

We assessed density- and distance-dependence in herbivore effects and juvenile condition for four species of Shorea, the most speciose genus in the dominant canopy family of southeast Asian rain forest trees (Dipterocarpaceae). Herbivore damage was quantified as partial leaf loss on young leaves, and whole plant foliar condition as the product of the fraction of leaf nodes containing leaves and the fraction of tissue remaining on extant leaves. Adults of the four species were centers of high total, as well as conspecific, density of juveniles (<1 m tall). For two species, S. hopeifolia and S. pinanga, herbivore damage declined significantly with distance, decreasing by 40% and 51% respectively, between 5 m and 35 m from the parent. For the same two species, foliar condition improved significantly between 5 m and 35 m, increasing by 45% for S. hopeifolia and 24% for S. pinanga. If foliar condition influences juvenile survival and growth, more widely dispersed seeds of these species are more likely to recruit to the canopy. In contrast, there was no significant distance-dependence for S. parvifolia or S. longisperma. Among species, herbivore damage was greatest in those species with greatest local juvenile abundances, i.e., those with highest densities, leaf size, juvenile foliar mass and/ or foliar mass/m² ground area, but was unrelated to the toughness of mature leaves. However, distance was a better predictor of herbivore damage than was conspecific juvenile density, as evaluated by backward elimination regressions, for both S. hopeifolia and S. pinanga. For foliar condition, the best predictor was distance for S. pinanga, but conspecific density for S. hopeifolia, whose juveniles were smallest and occurred at the highest densities. Total juvenile density (all woody plants) was eliminated as a factor in all cases. The species-specificity of effects (i.e., their dependence on conspecific distance or density), together with the marked differences among congeneric species, caution against generalizations regarding distance-dependent effects in diverse forests. Received: 21 April 1998 / Accepted: 8 July 1998     

Relationships between sclerophylly,leaf biomechanical properties and leaf anatomy in some Australian heath and forest species

ABSTRACT

A previous study of 19 south-east Australian heath and forest species with a range of leaf textures showed that they varied considerably in leaf biomechanical properties. By using an index of sclerophylly derived from botanists' rankings (botanists' sclerophylly index, BSI) we determined that leaves considered by botanists to be sclerophyllous generally had both high strength and work to fracture (particularly in punching and tearing tests), both at the level of leaf and per unit leaf thickness. In the current study we have shown that leaves from the same species also varied considerably in leaf specific mass (46–251 g m^-2), neutral detergent fibre concentration (20–59% on a dry weight basis) and in leaf anatomy. Multiple regression indicated a very strong correlation between BSI and the first two components of a principal components analysis (PCA) of leaf anatomy (R ² = 0.91). In addition, there was strong correlation between the first component of a PCA of the mechanical properties (correlated with BSI) and the two axes derived from anatomical characteristics (R ² = 0.66). The anatomical properties contributing most to the significant component axes were thickness of palisade mesophyll and upper cuticle (axis 1) and percentage fibre (neutral detergent fibre) and lower epidermis thickness (axis 2). However, whether these relationships are causal, or reflect correlations with characteristics not measured in this study, such as vascularization and sclerification, is not clear. At a finer scale, however, there is evidence that there are various ways to be sclerophyllous, both in terms of anatomical and mechanical properties. This is illustrated by comparison of two of the sclerophyllous species, Eucalyptus baxteri and Banksia marginata.     

High abscission rates of damaged expanding leaves: field evidence from seedlings of a Bornean rain forest tree

Herbivore damage is known to cause the premature loss of mature leaves. However, the effects of herbivory on abscission during the early stages of leaf development remain unexplored, even though herbivores frequently prefer unlignified, immature leaves. In a field experiment, we removed 50% of the tissue from leaves at various stages of development on seedlings of Shorea hopeifolia (Dipterocarpaceae), a dominant rain forest tree in Indonesian Borneo. Four weeks following simulated herbivory, >88% of unlignified expanding leaves had been abscised, compared to only 20% of fully expanded, unlignified leaves and 0% of recently lignified, mature leaves. In a separate experiment over 9 wk, simulated herbivory did not increase abscission rates of mature leaves, even when 75% of leaf tissue was removed. Because most (58%) of S. hopeifolia seedlings under natural conditions had lost 1% or less of the tissue from their mature leaves, herbivore damage probably has little effect on the abscission of mature leaves. In contrast, the tendency for damaged expanding leaves to abscise may explain why 49% of S. hopeifolia seedlings had already lost their youngest leaf. If similar patterns occur in other species, herbivore attacks on developing leaves may contribute substantially to both leaf loss and the cumulative impact of herbivory on the growth and survival of whole plants.     

Two Mallotus species of different life histories adopt different defense strategies in relation to leaf age

Plants defend their leaves using multiple defense traits that change functions with leaf age. We examined the effects of leaf age on the development of multiple defense traits in two related Mallotus (Euphorbiaceae) species: young plants of the fast‐growing Mallotus japonicus (Spreng.) Müll. Arg. and the slow‐growing Mallotus philippensis (Lam.) Müll. Arg. Sequential leaves of the two species were measured for their leaf area, leaf mass/area, densities of trichomes and pellucid dots, extrafloral nectar volume, and the numbers of extrafloral nectaries and pearl bodies. Mallotus japonicus shifted its defense tactics from direct defense using trichomes and pellucid dots in young leaves to biotic defense using extrafloral nectar and pearl bodies in middle‐aged leaves. In contrast, M. philippensis used direct, chemical defense throughout all leaf ages, together with the shift from indirect, biotic defense using extrafloral nectar in young leaves to direct, physical defense using leaf toughness in middle‐aged leaves. These results strongly suggest that, in relation to life history, plants can alter optimal combinations of multiple defense traits with leaf age.