Convergence in defense syndromes of young leaves in tropical rainforests

In tropical forests, the majority of damage by herbivores or pathogens occurs on young leaves, yet the patterns of damage and the factors that influence them are poorly known. By measuring damage throughout leaf development and maturation for five species in a Panamanian forest, we showed that leaf toughening, which only occurs over a few days once the leaf is fully expanded, is the main factor decreasing damage in mature leaves. Although rates of damage to young leaves are, on average, orders of magnitude greater than on mature leaves, there is significant interspecific variation in young leaf defenses and in damage rates. In a survey of 55 species of shade-tolerant plants, we found that each species only invested in a subset of the potential defensive mechanisms for young leaves. We measured rates of young leaf expansion, nitrogen content, delayed chloroplast development, synchrony of leaf production and rates of damage in the field. On a subset of 24 species, we also measured phenolic compounds, checked for the presence of saponins and alkaloids, and conducted bioassays using lepidopteran, coleopteran and orthopteran herbivores and four fungal pathogens to test for toxicity of young leaf extracts. Certain combinations of traits repeatedly co-occurred across unrelated species suggesting convergent evolution. We argue that selection has repeatedly led to tradeoffs among defenses such that species fall along an escape/defense continuum. At one extreme are species with a ‘defense’ strategy, which includes effective chemical defense, slow leaf expansion, normal greening and low rates of damage (less than 20% of the leaf area lost). At the other extreme are ‘escape’ species which have ineffective chemical defenses and, as a consequence, have high rates of leaf damage, 60% of leaf area lost during expansion. In partial compensation for ineffective chemical defense, these species have very rapid leaf expansion (doubling in area every day) which minimizes the window of vulnerability, delayed chlor∗ Corresponding author. Tel. : +1-801-581-8369; fax: +1-801-581-4668. E-mail address: kursar@biology.utah. edu (T.A. Kursar). 0305-1978/03/$ see front matter  2003 Elsevier Science Ltd. All rights reserved. doi:10.1016/S0305-1978(03)00087-5 930 T.A. Kursar, P.D. Coley / Biochemical Systematics and Ecology 31 (2003) 929–949 oplast development (white young leaves) which contain fewer resources, and synchronous leaf production to satiate herbivores. Thus, interspecific variation in young leaf damage rates is explained by differences in defense combinations along this escape/defense continuum. Because apparently beneficial traits such as effective chemical defense and rapid leaf expansion do not occur in the same species, we suggest that physiological constraints limit the defense combinations of any one species to a restricted subset of those observed. However, the defense and escape strategies do not represent different tradeoffs that have equal fitness, as species with the escape syndrome suffer much higher rates of damage. We hypothesize that the escape syndrome arose over evolutionary time among plants that failed to evolve effective secondary metabolites while herbivores succeeded in evolving adaptations to the chemistry of their host plant. Hence the defense syndrome should provide the greatest fitness, whereas the escape syndrome minimizes damage given the failure of the plant’s secondary metabolites to provide protection.  2003 Elsevier Science Ltd. All rights reserved.