Journal of Experimental Botany, Vol. 52, No. 363, pp. 2057-2065,
October 1, 2001
© 2001 Oxford University Press
Original Papers |
Adaptations to biotic and abiotic stress: Macaranga-ant plants optimize investment in biotic defence
1 Lehrstuhl für Tierökologie und Tropenbiologie (Zoologie III), Theodor-Boveri-Institut, Biozentrum, Am Hubland, D-97074 Würzburg, Germany
2 Lehrstuhl für Molekulare Pflanzenphysiologie und Biophysik (Botanik I), Julius-von-Sachs-Institut, Julius-von-Sachs-Platz 2, D-97082 Würzburg, Germany
3 Max-Planck-Institut für chemische Ökologie, Carl Zeiss-Promenade 10, D-07745 Jena, Germany
Received 12 February 2001; Accepted 21 June 2001
 |
Abstract |
|---|
 Top Abstract IntroductionCosts of food body...Benefits of defenceRegulation of FB productionRegulation of EFN productionConclusions and directions for...References |
|---|
Obligate ant plants (myrmecophytes) in the genus Macaranga produce energy- and nutrient-rich food bodies (FBs) to nourish mutualistic ants which live inside the plants. These defend their host against biotic stress caused by herbivores and pathogens. Facultative, ‘myrmecophilic’ interactions are based on the provision of FBs and/or extrafloral nectar (EFN) to defending insects that are attracted from the vicinity. FB production by the myrmecophyte, M. triloba, was limited by soil nutrient content under field conditions and was regulated according to the presence or absence of an ant colony. However, increased FB production promoted growth of the ant colonies living in the plants. Ant colony size is an important defensive trait and is negatively correlated to a plant's leaf damage. Similar regulatory patterns occurred in the EFN production of the myrmecophilic M. tanarius. Nectar accumulation resulting from the absence of consumers strongly decreased nectar flow, which increased again when consumers had access to the plant. EFN flow could be induced via the octadecanoid pathway. Leaf damage increased levels of endogenous jasmonic acid (JA), and both leaf damage and exogenous JA application increased EFN flow. Higher numbers of nectary visiting insects and lower numbers of herbivores were present on JA-treated plants. In the long run, this decreased leaf damage significantly. Ant food production is controlled by different regulatory mechanisms which ensure that costs are only incurred when counterbalanced by defensive effects of mutualistic insects.
Key words: Ant plant, anti-herbivore defence, mutualism, myrmecophyte, tropics.
|
Introduction |
|---|
|
TopAbstractIntroductionCosts of food body...Benefits of defenceRegulation of FB productionRegulation of EFN productionConclusions and directions for...References |
|---|
Many tropical plants of different taxonomic groups have evolved mutualisms with ants (Beattie, 1985
; Buckley, 1982; Hölldobler and Wilson, 1990; McKey and Davidson, 1993). In most cases, ants are used as an indirect (Price et al., 1980), ‘biotic’ defence mechanism. Obligate ‘ant plants’ (myrmecophytes) of the genus Macaranga (Euphorbiaceae) house specific ant colonies in their hollow shoots (Fig. 1a). The ants feed on so-called food bodies (FBs, Fig. 1b), cellular structures which are produced by the plant and which contain large amounts of lipids, proteins and carbohydrates (see below, and Fiala and Maschwitz, 1992a, b; Heil et al., 1998). The ants (mostly belonging to the genus Crematogaster) live symbiotically in specific Macaranga trees (Fiala et al., 1999; Fiala and Maschwitz, 1990). They patrol the plant surface (Fig. 1c, d), remove all kinds of foreign material, and thereby defend their host against various forms of biotic stress caused by herbivores, by competing and parasitic plants, and by fungal pathogens (Fiala et al., 1994, 1989; and below). Other forms of ant–plant interaction in the genus Macaranga are less specific. ‘Myrmecophilic’ plants do not house species-specific ant colonies. However, they produce FBs (Fig. 2a) and extrafloral nectar (EFN) on their leaf blades (Fiala and Maschwitz, 1991). Insects such as ants (Fig. 2b), wasps and flies (Fig. 2c) from the vicinity are attracted to these rewards and defend the plants facultatively against herbivores (Koptur, 1992).
|
|
Both strategies enable these plants to cope with the severe biotic stress resulting from high herbivore and pathogen pressure which is characteristic for many secondary forests. In the tropics, nutrients are often limiting for plant growth and reproduction, this holds true especially for the heavily degraded soils occurring in many open, secondary systems. FB production consumes important resources such as nitrogen and energy (see below), and EFN contains carbohydrates and amino acids and thus consumes resources as well. Mechanisms controlling the investment in ant rewards should therefore provide selective advantages. The present paper reviews recently discovered mechanisms regulating the production of FBs and EFN. Two species were chosen. M. triloba (Bl.) Muell. Arg. represents the obligate myrmecophytes, while M. tanarius (L.) Muell. Arg. has evolved the facultative, myrmecophilic strategy. Most experiments were conducted under field conditions at the plants' natural growing sites on Peninsular Malaysia (see Fiala et al., 1989
; Heil, 1998; Heil et al., 2001b for descriptions of the study sites).
|
Costs of food body and extrafloral nectar production |
|---|
|
TopAbstractIntroductionCosts of food body...Benefits of defenceRegulation of FB productionRegulation of EFN productionConclusions and directions for...References |
|---|
Ants associated with Macaranga myrmecophytes do not use any of the material which they find on their host plants as food (Fiala and Maschwitz, 1990
). Even insect eggs and small larvae are only removed and thrown off the plant surface. The ants therefore seem to rely fully on the FBs provided by their host plants. In contrast, FBs produced by myrmecophilic species are only a kind of bait for opportunistic ants and other insects living in the vicinity of the plants. These are not likely to rely solely on food produced by one single plant species. Analyses of main nutrient classes in FBs were conducted with HPLC (carbohydrates and proteins) and GC-MS (lipids). They demonstrated that Macaranga FBs meet these different requirements (Heil et al., 1998). FBs produced by obligate myrmecophytes were rich in lipids and proteins and had a comparably high N/C-ratio (Fig. 3). FBs produced by the myrmecophilic M. tanarius had lower contents of lipids and much lower contents of proteins, while the contents of carbohydrates were higher than in FBs of myrmecophytes (Heil et al., 1998). These trends were even more obvious when regarding FBs of other myrmecophilic species belonging to the familiy of Vitaceae (Heil et al., 1998). Further characteristic differences between FBs from myrmecophytic and myrmecophilic species occurred with respect to the ratio of soluble to polymeric carbohydrates and the ratio of free amino acids to proteins. In both classes of main nutrients, the relative content of monomeric or dimeric, soluble components was much higher in FBs of myrmecophilic species (Fig. 3). It is likely that these soluble components are easier to detect chemotactically by feeding insects than polymeric carbohydrates or proteins (Heil et al., 1998). Taste seems to be much more important in FBs which are used by foraging insects from the vicinity, while a high nutritive value should be selected for in FBs which serve as the main food source for ant colonies living in myrmecophytic species. Finally, water contents of fresh FBs also differed between the two functional groups and were much higher in FBs from myrmecophilic species (Heil et al., 1998). Containing a high proportion of soluble sugars and amino acids dissolved in large quantities of water, FBs of myrmecophilic species seem to resemble some kind of ‘packed’ extrafloral nectar (EFN). Thus, these FBs mimic a widespread kind of plant-derived food resource which is used by many different ant species (Heil et al., 1998; Koptur, 1992).
|
Due to their high contents of lipids and proteins, production of FBs by the myrmecophyte, M. triloba, consumes a considerable amount of resources. Both FB production and overall above-ground biomass production were quantified for unbranched M. triloba saplings, and daily courses of photosynthetic rate (net rate of photosynthetic CO2 uptake) were measured for the same plants. To estimate the plants' total energy budget under field conditions, a CO2/H2O-porometer system (CQP 130; Walz, Effeltrich, Germany, see Heil et al., 1997
; Zotz et al., 1995 for details) was used. FB production amounted to about 5% of total above-ground biomass production. Based on the chemical composition of FBs and shoot and leaf material it could be calculated that about 30% of the total lipids, 7% of the proteins and amino acids and 2% of the carbohydrates invested into the overall above-ground growth were diverted to FB production (Heil et al., 1997). Based on the construction costs of the different types of tissue (see Penning de Vries et al., 1974 for the chosen method to calculate construction costs and Griffin, 1994, for a discussion of these methods), FB production consumed about 5% of the plants' total energy budget as estimated from photosynthetic net assimilation (Heil et al., 1997).
Parallel measurements and calculations were conducted for the FB and EFN production and photosynthesis of similar-sized saplings of the myrmecophilic M. tanarius. Due to the lower contents of lipids and proteins, construction costs of FBs are lower (Heil, 1998). FB and EFN production by M. tanarius consumed about 4% of the plants total energy budget (Heil, 1998).
|
Benefits of defence |
|---|
|
TopAbstractIntroductionCosts of food body...Benefits of defenceRegulation of FB productionRegulation of EFN productionConclusions and directions for...References |
|---|
Defence via housed or attracted insects is indirect (Price et al., 1980
) and thus might be expected to have only a low efficiency. Indeed, ant-exclusion experiments demonstrated that the defence resulting from facultative, myrmecophilic interactions is less efficient than defence provided by symbiotic Crematogaster plant ants living in myrmecophytic species (Fiala et al., 1994, 1989). Recent field experiments were based on the comparison of damage suffered by leaves situated on ant-defended twigs to the damage suffered by leaves on twigs of the same plants from which ants were kept off experimentally. Neighbouring twigs were selected and were treated as matched pairs with one twig per pair being randomly selected for ant removal. The results were therefore not biased by any site effects or genetic differences between experimental plants (Heil et al., 2001b). After 6 weeks, leaves on M. triloba twigs on which ants still were present had lost on average 1.2% of their total area (median, n=411), while leaf damage on ant-free twigs of the same plants amounted to 2.6% missing area (median, n=412). The highest efficacy of defence became apparent on young leaves that had newly developed during the experimental time span (1.4% missing leaf area on defended leaves compared to 4.2% for ant-free leaves, n=57 and 40, respectively). In M. tanarius, the effect of defence was less pronounced. On average, defended leaves lost 3.2% leaf area (n=294), while leaves to which ants had no access lost 4.2% (n=362). Values for newly developed leaves were 2.1% (n=95) and 3.9% (n=117), respectively (all data from Heil et al., 2001b). Based on Wilcoxon tests for matched pairs, all differences between damage levels of leaves on treated and control twigs were highly significant (P<0.001 in all four cases mentioned).
Long-term studies conducted over the time span of one year demonstrated that short-term experiments are not suitable to estimate the ‘real’ effect of a given defence (Heil et al., 2001b). A study comparing inhabited M. triloba trees to similar-sized ones which had been deprived from their ants experimentally for one year revealed that ant-free plants lost, on average, about 80% of their total leaf area (mean, n=16), while total leaf area of inhabited trees increased by about 40% (mean, n=16) within the same time span (Fig. 4).
|
Besides the defence against folivores, protection from shoot-boring insects and pathogenic fungi adds significantly to the overall effect of symbiotic Crematogaster ants associated with M. triloba (Heil et al., 1999
). Measurements of chitinase activity, a plant trait which has been shown to play an important role in the plants own, direct defence against pathogenic fungi (Iseli et al., 1996; Jackson and Taylor, 1996; Sahai and Manocha, 1993), revealed very low activities in myrmecophytic Macaranga species (Heil et al., 1999). This probably represents a general trait of ant plants, since Mexican Acacia myrmecophytes showed comparably low chitinase activities when compared to related species exhibiting no obligate mutualism with defending ants (Heil et al., 2000c). In M. triloba, the inhabiting ants can have a direct protective effect against pathogenic fungi (Heil et al., 1999), a result which is supported by similar findings on ant plants of the genus Piper (Letourneau, 1998).
The high efficacy of ant defence results from both the ants' mobility and low specificity. Ants can concentrate very quickly on those parts of the plant surface which actually require defence (Fig. 1d
), and they are effective against many types of insects, climbers, and pathogens. They fulfil several functions for which otherwise a variety of different chemical substances would be necessary. This may be the most important general benefit of indirect plant defence, which makes use of ‘animal-specific’ traits rather than of intrinsic plant properties (Price et al., 1980). Ants in the obligate myrmecophytic interactions are adapted much closer to their individual host and are much more dependent upon it. The higher efficacy of their interactions as compared to those in myrmecophilic relationships therefore seems to be an adaptive trait.
|
Regulation of FB production |
|---|
|
TopAbstractIntroductionCosts of food body...Benefits of defenceRegulation of FB productionRegulation of EFN productionConclusions and directions for...References |
|---|
FB production represents a comparably costly defence (see above, and Heil et al., 1997
). In general, so-called ‘allocation costs’ are assumed to occur whenever defence consumes limited resources which then cannot be used for other vitally important functions such as growth and reproduction (Simms and Fritz, 1990; Simms and Rausher, 1987; Herms and Mattson 1992). Therefore, every ‘costly’ defensive trait should reduce the plants' fitness when expressed under conditions not requiring defence. This model can be used to understand the evolution of inducible defences (Heil, 1999, 2000) and explains why the induction of defence can cause a reduction of reproductive success when occurring under enemy-free conditions (Agrawal et al., 1999; Baldwin, 1998; Heil et al., 2000b).
However, this also leads to the prediction that investments in indirect defences, such as the production of FBs or EFN, should be regulated by the plants in order to avoid superfluous costs. Fertilization studies conducted under field conditions revealed that FB production by M. triloba is limited by soil nutrient content (Heil et al., 2001a) and thus is likely to cause relevant allocation costs. On average, FB production by fertilized M. triloba plants was more than three times higher than by untreated controls (4-week field experiment). Significantly higher amounts of FBs were already present on fertilized M. triloba plants 2 d after the onset of fertilization (M Heil, unpublished data). In comparison to the untreated controls, M. triloba saplings which had been fertilized for 4 weeks to increase FB production contained higher numbers of eggs, larvae, pupae, and of adult ants, while colonies in plants from which FBs had been removed showed the reverse pattern (Fig. 5). These treatments had highly significant effects on ant colony structure and size. The effects of different treatments affected all developmental stages, but the small larvae significantly (Table 1). FB supply is obviously a main factor determining the size and structure of inhabiting ant colonies. Ant colony size is an important defensive trait, since the number of adult workers living in a plant is negatively correlated to the plant's leaf damage (Heil et al., 2001a).
|
|
According to these results, FB production consumes important and limited resources but is positively correlated to the plants' defensive ability. It was thus likely to be regulated ‘actively’ by the plant itself. Indeed, ant-free M. triloba plants, grown in nylon-mesh field cages to prevent them from herbivore damage, showed much lower rates of FB production than similar-sized inhabited plants that had been cultivated under otherwise identical conditions (Heil et al., 1997
). The same held true for plants grown in a greenhouse in Germany. Negative effects of missing defence on plant performance and FB production were thus not likely to bias these patterns (Heil, 1998; Heil et al., 1997). Obviously, FB production is upregulated in the presence of an inhabiting ant colony. It still remains to determine whether FB removal or the presence of a specific ant colony are triggering this response.
|
Regulation of EFN production |
|---|
|
TopAbstractIntroductionCosts of food body...Benefits of defenceRegulation of FB productionRegulation of EFN productionConclusions and directions for...References |
|---|
Similar adaptive patterns were found in the EFN production by M. tanarius. Field experiments based on the experimental protection of nectaries from nectar-consuming insects revealed a decrease in EFN secretion when nectar accumulated on the nectaries, while EFN flow increased again when consumers had access to the plants for 1 d (Heil et al., 2000
a). When EFN was collected with microcapillaries from plants cultivated under greenhouse conditions, repeated EFN removals (8 EFN removals in 24 h conducted every 3 h) led to a higher average amount of nectar produced per day than one single nectar removal after 24 h (Heil et al., 2000a). While the influence of chemical signals produced by nectar-consuming insects cannot yet be excluded, the latter result shows that the frequency of EFN removal alone can have some regulatory effect on the amount of nectar produced. Similar patterns have been reported for the secretion of floral nectar (Pyke, 1991) and thus might represent a general trait preventing plants from spending resources for insect rewards which are not likely to be consumed.
Several studies have indicated that EFN secretion or amino acid concentrations in EFN may increase in response to herbivory (Koptur, 1989; Smith et al., 1990; Stephenson, 1982; Swift and Lanza, 1993), and that this response does not require herbivore-specific elicitors (Heil et al., 2000a; Wäckers and Wunderlin, 1999). It has therefore been discussed whether or not EFN can be considered as an induced defence (Agrawal and Rutter, 1998). However, most of these studies suffered from methodological problems (discussed in Heil et al., 2000a). Moreover, no information was available on the underlying signalling pathway, and no study had focused on the effects of induced EFN production on nectary-visiting insects and herbivores.
Recently, a first data set answering these questions has been obtained from field studies on M. tanarius. Secretion rates of treated experimental and untreated control plants were compared to reference values measured in advance of the experiments on the same individual plants (Heil et al., 2001c). EFN production was quantified as the amount of soluble solids produced per 24 h. Although the concentration of nectar can change quickly once it has been secreted (Corbet et al., 1979), the relative composition of EFN of M. tanarius remains relatively constant even under field conditions. Combined measurements of nectar volume and concentration thus allow a reliable quantification of the amounts of secreted substances (method described and discussed in Heil et al., 2000a). All nectaries present on four identically treated leaves of each of 10 plants per treatment were included in these experiments. Herbivory, artificially damaging leaves with a needle, and exogenous jasmonic acid (JA) application all increased nectar flow significantly, while controls by spraying of the solvent used to apply JA (water) and zero-controls (no treatment) elicited no response (Fig. 6; repeated measures ANOVA for the effect of treatments with leaf number as the within-subject variable: F(4,196)=9.849, P<0.001). The response of EFN flow to leaf damage could be suppressed by the application of phenidone, an inhibitor of endogenous JA synthesis (Heil et al., 2001c). Under laboratory conditions, artificial damage strongly enhanced endogenous JA concentrations which were quantified by GC-Trace-MS according to the methods described previously (Baldwin et al., 1997; Koch et al., 1999). Quantitative dose–response relationships were found between the increase in nectar production and both the intensity of leaf damage and the amounts of exogenously applied JA, and a similar relationship occurred between the amount of endogenously produced JA and the intensity of leaf damage (Heil et al., 2001c). The numbers of defending insects appearing on the leaves under field conditions increased very soon after inducing EFN flow by the exogenous application of JA, while the numbers of herbivores decreased in the same experimental design (Fig. 7). In a 6-week study, the repeated induction of EFN flow by JA application or artificially damaging leaves resulted in a 10-fold reduction in herbivory as compared to untreated controls (Fig. 7). These results demonstrate that EFN production represents a further mechanism for induced, indirect plant defences that are mediated via the octadecanoid signal transduction cascade.
|
|
|
Conclusions and directions for further research |
|---|
|
TopAbstractIntroductionCosts of food body...Benefits of defenceRegulation of FB productionRegulation of EFN productionConclusions and directions for...References |
|---|
Many regulatory processes are controlling the production of ant food (FBs) or liquid ant rewards (EFN) by myrmecophytic and myrmecophilic Macaranga species. For example, EFN flow increases in response to leaf damage. This response is mediated via the octadecanoid pathway and can be elicited by mechanical leaf damage. By contrast, the factors regulating EFN secretion by M. tanarius and FB production by M. triloba according to the presence or absence of the respective consumers still have to be identified. Although very successful with respect to their defensive efficacy under field conditions, the strategies to nourish or attract ants or other insects which then act as indirect defensive agents seem to be costly in terms of investment of limited resources. All the mechanisms described can be interpreted as adaptations ensuring that the respective investments occur only under conditions actually requiring defence (EFN) or in the presence of defensive animals which consume the provided food (FBs and EFN). Few comparable studies have been conducted so far. A dependency of FB production by myrmecophytic Cecropia species on light and nutrient availability has been reported (Folgarait and Davidson, 1994
, 1995), and a dependency of FB production on the presence of a symbiotic ant colony has been reported for Piper (Risch and Rickson, 1981). Comparative studies on different genera of ant plants would help to decide whether the regulatory mechanisms as described here are general traits of specialized ant plants or rather specific adaptations of the genus Macaranga.
In general, it is still under discussion whether the costs of defensive traits occur at all, and whether they play an important role in the evolution of defence. The present results indicate that these costs do indeed occur in the investigated system, and that several mechanisms have evolved to control and thereby reduce these costs whenever possible. Studies on other forms of defence support these findings (Fagerström, 1989; Gershenzon, 1994; Niemann et al., 1992; Sagers and Coley, 1995; Simms and Rausher, 1989). Further studies on different plant species and different forms of defence should be conducted to determine whether defence in general causes allocation costs, whether and under which conditions these translate into fitness costs, and how these costs influence the plants' life histories and ecological properties.
|
Acknowledgments |
|---|
We thank Andrea Hilpert, Frieda Reisberg, Eva Wirth, Astrid Boots, Karin Heil, and Ralf Krüger for much practical help with both analytical and field work, Fritz Thiele and Andreas Kreiner for cultivating the greenhouse plants, and Professor Dr Doyle McKey for critically reading the manuscript. Dr Rosli Hashim, Dr Hj Azarae Idris and the Economic Planning Unit (EPU) kindly gave permission to conduct field studies at the Ulu Gombak Field Studies Centre in West Malaysia. Financial support by the German Research Foundation (DFG: TP C8 in SFB 251, grants Li150/13-1/3 and He3169/1-1) and logistical help by the Malaysian Airlines System (MAS) is gratefully acknowledged.
|
Notes |
|---|
4 Present address: Centre d'Ecologie Fonctionelle et Evolutive (CEFE, CNRS) 1919 Route de Mende, F-34293 Montpellier Cedex 5, France.
5 To whom correspondence should be addressed. Fax: +49 931 888 4352. E-mail: ke\|[uscr ]\|lins{at}biozentrum.uni\|[hyphen]\|wuerzburg.de
|
References |
|---|
|
TopAbstractIntroductionCosts of food body...Benefits of defenceRegulation of FB productionRegulation of EFN productionConclusions and directions for...References |
|---|
Agrawal AA, Rutter MT. 1998. Dynamic anti-herbivore defense in ant–plants: the role of induced responses. Oikos 83, 227–236.
Agrawal AA, Strauss SY, Stout MJ. 1999. Costs of induced responses and tolerance to herbivory in male and female fitness components of wild radish. Evolution 53, 1093–1104.
Baldwin IT. 1998. Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proceedings of the National Academy of Sciences, USA 95, 8113–8118.
Baldwin IT, Zhang Z-P, Diab N, Ohnmeiss TE, McCloud ES, Lynds GY, Schmelz EA. 1997. Quantification, correlations and manipulation of wound-induced changes in jasmonic acid and nicotine in Nicotiana sylvestris. Planta 201, 397–404.
Beattie AJ. 1985. The evolutionary ecology of ant–plant mutualisms. Cambridge, UK: Cambridge University Press.
Buckley RC. 1982. Ant–plant interactions: a world review. In: RC Buckley, ed. Ant–plant interactions in Australia. The Hague, Boston, London: W Junk, 111–162.
Corbet SA, Willmer PG, Beament JWL, Unwin DM, Prys-Jones OE. 1979. Post-secretory determinants of sugar concentration in nectar. Plant, Cell and Environment 2, 293–308.
Fagerström T. 1989. Anti-herbivory chemical defense in plants: a note on the concept of cost. The American Naturalist 133, 281–287.
Fiala B, Grunsky H, Maschwitz U, Linsenmair KE. 1994. Diversity of ant–plant interactions: protective efficacy in Macaranga species with different degrees of ant association. Oecologia 97, 186–192.
Fiala B, Jakob A, Maschwitz U, Linsenmair KE. 1999. Diversity, evolutionary specialization and geographic distribution of a mutualistic ant–plant complex: Macaranga and Crematogaster in South East Asia. Biological Journal of the Linnean Society 66, 305–331.
Fiala B, Maschwitz U. 1990. Studies on the South East Asian ant–plant association Crematogaster borneensis/Macaranga: adaptations of the ant partner. Insectes Sociaux 37, 212–231.
Fiala B, Maschwitz U. 1991. Extrafloral nectaries in the genus Macaranga (Euphorbiaceae) in Malaysia: comparative studies of their possible significance as predispositions for myrmecophytism. Biological Journal of the Linnean Society 44, 287–305.
Fiala B, Maschwitz U. 1992a. Domatia as most important adaptions in the evolution of myrmecophytes in the paleotropical tree genus Macaranga (Euphorbiaceae). Plant Systematics and Evolution 180, 53–64.[Web of Science]
Fiala B, Maschwitz U. 1992b. Food bodies and their significance for obligate ant-association in the tree genus Macaranga (Euphorbiaceae). Botanical Journal of the Linnean Society 110, 61–75.
Fiala B, Maschwitz U, Tho YP, Helbig AJ. 1989. Studies of a South East Asian ant–plant association: protection of Macaranga trees by Crematogaster borneensis. Oecologia 79, 463–470.
Folgarait PJ, Davidson DW. 1994. Antherbivore defenses of myrmecophytic Cecropia under different light regimes. Oikos 71, 305–320.
Folgarait PJ, Davidson DW. 1995. Myrmecophytic Cecropia: antiherbivore defenses under different nutrient treatments. Oecologia 104, 189–206.
Gershenzon J. 1994. The cost of plant chemical defense against herbivores: a biochemical perspective. In: EA Bernays, ed. Insect–plant interactions, Vol. 5. Boca Raton: CRC Press, 105–173.
Griffin KL. 1994. Calorimetric estimates of construction cost and their use in ecological studies. Functional Ecology 8, 551–562.
Heil M. 1998. Quantitative Kosten-Nutzen-Analyse verschiedener Ameisen-Pflanzen-Assoziationen innerhalb der Gattung Macaranga. Berlin: Wissenschaft & Technik Verlag.
Heil M. 1999. Systemic acquired resistance—available information and open ecological questions. Journal of Ecology 87, 341–346.
Heil M. 2000. Different strategies for studying ecological aspects of systemic acquired resistance (SAR). Journal of Ecology 88, 707–708.
Heil M. 2001. The ecological concept of costs of induced systemic resistance (ISR). European Journal of Plant Pathology 107, 137–146.
Heil M, Fiala B, Baumann B, Linsenmair KE. 2000a. Temporal, spatial and biotic variations in extrafloral nectar secretion by Macaranga tanarius. Functional Ecology 14, 749–757.
Heil M, Fiala B, Boller T, Linsenmair KE. 1999. Reduced chitinase activities in ant plants of the genus Macaranga. Naturwissenschaften 86, 146–149.
Heil M, Fiala B, Kaiser W, Linsenmair KE. 1998. Chemical contents of Macaranga food bodies: adaptations to their role in ant attraction and nutrition. Functional Ecology 12, 118–122.
Heil M, Fiala B, Linsenmair KE. 2001a. Nutrient availability and indirect (biotic) defence in a Malaysian ant–plant. Oecologia 126, 404–408.
Heil M, Fiala B, Linsenmair KE, Zotz G, Menke P, Maschwitz U. 1997. Food body production in Macaranga triloba (Euphorbiaceae): a plant investment in anti-herbivore defence via mutualistic ant partners. Journal of Ecology 85, 847–861.
Heil M, Fiala B, Maschwitz U, Linsenmair KE. 2001b. On the benefits of indirect defence: short- and long-term studies in antiherbivore protection via mutualistic ants. Oecologia 126, 395–403.
Heil M, Hilpert A, Kaiser W, Linsenmair KE. 2000b. Reduced growth and seed set following chemical induction of pathogen defence: does systemic acquired resistance (SAR) incur allocation costs? Journal of Ecology 88, 645–654.
Heil M, Koch T, Hilpert A, Fiala B, Boland W, Linsenmair KE. 2001c. Extrafloral nectar production of the ant-associated plant, Macaranga tanarius, is an induced indirect defensive response elicited by jasmonic acid. Proceedings of the National Academy of Sciences, USA 98, 1083–1088.
Heil M, Staehelin C, McKey D. 2000c. Low chitinase activity in Acacia myrmecophytes: a potential trade-off between biotic and chemical defences? Naturwissenschaften 87, 555–558.[Web of Science][Medline]
Herms DA, Mattson WJ. 1992. The dilemma of plants: to grow or to defend. The Quarterly Review of Biology 67, 283–335.
Hölldobler B, Wilson EO. 1990. The ants. Berlin, Heidelberg, New York: Springer.
Iseli B, Armand S, Boller T, Neuhaus J-M, Henrissat B. 1996. Plant chitinases use two different hydrolytic mechanisms. FEBS Letters 382, 186–188.[Web of Science][Medline]
Jackson AO, Taylor CB. 1996. Plant–microbe interactions: life and death at the interface. The Plant Cell 8, 1651–1668.[Web of Science][Medline]
Koch T, Krumm T, Jung V, Engelberth J, Boland W. 1999. Differential induction of plant volatile biosynthesis in the lima bean by early and late intermediates of the octadecanoid-signaling pathway. Plant Physiology 121, 153–162.
Koptur S. 1989. Is extrafloral nectar an inducible defense? In: JH Bock, YB Linhart, ed. The evolutionary ecology of plants. Boulder, Colorado: Westview Press, 323–339.
Koptur S. 1992. Extrafloral nectary-mediated interactions between insects and plants. In: EA Bernays, ed. Insect–plant interactions, Vol. IV. Boca Raton: CRC Press, 81–129.
Letourneau DK. 1998. Ants, stem-borers, and fungal pathogens: experimental tests of a fitness advantage in Piper ant–plants. Ecology 79, 593–603.[Web of Science]
McKey D, Davidson DW. 1993. Ant–plant symbioses in Africa and the neotropics: history, biogeography and diversity. In: Goldblatt P, ed. Biological relationships between Africa and South America: Yale University Press, 568–606.
Niemann GJ, Pureveen JBM, Eijkel GB, Poorter H, Boon JJ. 1992. Differences in relative growth rate in 11 grasses correlate with differences in chemical composition as determined by pyrolysis mass spectrometry. Oecologia 89, 567–573.
Penning de Vries FWT, Brunsting AHM, van Laar HH. 1974. Products, requirements and efficiency of biosynthesis: a quantitative approach. Journal of Theoretical Biology 45, 339–377.[Web of Science][Medline]
Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN, Weis AE. 1980. Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annual Review of Ecology and Systematics 11, 41–65.[Web of Science]
Pyke GH. 1991. What does it cost a plant to produce floral nectar? Nature 350, 58–59.
Risch SJ, Rickson F. 1981. Mutualism in which ants must be present before plants produce food bodies. Nature 291, 149–150.
Sagers CL, Coley PD. 1995. Benefits and costs of defense in a neotropical shrub. Ecology 76, 1835–1843.
Sahai AS, Manocha MS. 1993. Chitinases of fungi and plants: their involvement in morphogenesis and host–parasite interaction. FEMS Microbiology Reviews 11, 317–338.
Simms EL, Fritz RS. 1990. The ecology and evolution of host–plant resistance to insects. Trends in Ecology and Evolution 5, 356–360.
Simms EL, Rausher MD. 1987. Costs and benefits of plant resistance to herbivory. The American Naturalist 130, 570–581.
Simms EL, Rausher MD. 1989. The evolution of resistance to herbivory in Ipomoea purpurea. II. Natural selection by insects and costs of resistance. Evolution 43, 573–585.
Smith LL, Lanza J, Smith GS. 1990. Amino acid concentrations in extrafloral nectar of Impatiens sultani increase after simulated herbivory. Ecology 71, 107–115.
Stephenson AG. 1982. The role of the extrafloral nectaries of Catalpa speciosa in limiting herbivory and increasing fruit production. Ecology 63, 663–669.
Swift S, Lanza J. 1993. How do Passiflora vines produce more extrafloral nectar after simulated herbivory? Bulletin of the Ecological Society of America 74, 451.
Wäckers FL, Wunderlin R. 1999. Induction of cotton extrafloral nectar production in response to herbivory does not require a herbivore-specific elicitor. Entomologia Experimentalis et Applicata 91, 149–154.
Zotz G, Harris G, Königer M, Winter K. 1995. High rates of photosynthesis in the tropical pioneer tree, Ficus insipida Willd. Flora 190, 265–272.
CiteULike 
Connotea 
Del.icio.us What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||