Academic Appointments

Honors & Awards

  • Pew Scholar in Conservation, The Pew Charitable Trust (1992)
  • Outstanding Service Award: Teaching, Organization for Tropical Studies (2002)
  • Outstanding Researcher, Biology, National University of Mexico (2003)
  • Foreign Member, American Academy of Arts and Sciences (2004)
  • Foreign Associate, US National Academy of Science (2004)
  • Presidential Award in Ecology, Secretary of Environment, Mexico (2003)

Professional Education

  • B.Sc., University of Morelos, Mexico, Biology (1972)
  • M.Sc., University of Wales, Ecology (1977)
  • Ph.D., University of Wales, Ecology (1980)

Community and International Work

  • Plant-animal interactions, Mexico, Costa Rica, Amazonia


    ecology and evolutionary biology

    Partnering Organization(s)

    National University of Mexico, Organization for Tropical Studies, Amazonian Institute of Research

    Populations Served

    USA and LAtin American Students and policy makers



    Ongoing Project


    Opportunities for Student Involvement


Research & Scholarship

Current Research and Scholarly Interests

My interests are centered on the study of plant-animal interactions, trying to understand how the ecology and evolution of plants is affected by their biotic environment, particularly animals. My work is focused on tropical forest ecosystems, particulalry in Mexico and Amazonia, but I am also interested in developing similar studies in other ecosystems as well.
In the field of conservation biology, I am interested in studying the consequences of anthropogenic impact on the disruption of ecological processes, particularly biotic interactions.
Finally, I have a major interest in environmental education and sharing of my experiences in ecology and conservation, with the general public and students of all levels.


  • Effect of Herbivores on Plant Diversity, National University of Mexico (UNAM)

    This project examines via experimental manipulations and observations, the impact of herbivores on plant community, structure and diversity.




2014-15 Courses

Postdoctoral Advisees

Graduate and Fellowship Programs

  • Biology (School of Humanities and Sciences) (Phd Program)


Journal Articles

  • Integrating Stand and Soil Properties to Understand Foliar Nutrient Dynamics during Forest Succession Following Slash-and-Burn Agriculture in the Bolivian Amazon. PloS one Broadbent, E. N., Almeyda Zambrano, A. M., Asner, G. P., Soriano, M., Field, C. B., de Souza, H. R., Peña-Claros, M., Adams, R. I., Dirzo, R., Giles, L. 2014; 9 (2)


    Secondary forests cover large areas of the tropics and play an important role in the global carbon cycle. During secondary forest succession, simultaneous changes occur among stand structural attributes, soil properties, and species composition. Most studies classify tree species into categories based on their regeneration requirements. We use a high-resolution secondary forest chronosequence to assign trees to a continuous gradient in species successional status assigned according to their distribution across the chronosequence. Species successional status, not stand age or differences in stand structure or soil properties, was found to be the best predictor of leaf trait variation. Foliar δ(13)C had a significant positive relationship with species successional status, indicating changes in foliar physiology related to growth and competitive strategy, but was not correlated with stand age, whereas soil δ(13)C dynamics were largely constrained by plant species composition. Foliar δ(15)N had a significant negative correlation with both stand age and species successional status, - most likely resulting from a large initial biomass-burning enrichment in soil (15)N and (13)C and not closure of the nitrogen cycle. Foliar %C was neither correlated with stand age nor species successional status but was found to display significant phylogenetic signal. Results from this study are relevant to understanding the dynamics of tree species growth and competition during forest succession and highlight possibilities of, and potentially confounding signals affecting, the utility of leaf traits to understand community and species dynamics during secondary forest succession.

    View details for DOI 10.1371/journal.pone.0086042

    View details for PubMedID 24516525

  • Water stress strengthens mutualism among ants, trees, and scale insects. PLoS biology Pringle, E. G., Akçay, E., Raab, T. K., Dirzo, R., Gordon, D. M. 2013; 11 (11)


    Abiotic environmental variables strongly affect the outcomes of species interactions. For example, mutualistic interactions between species are often stronger when resources are limited. The effect might be indirect: water stress on plants can lead to carbon stress, which could alter carbon-mediated plant mutualisms. In mutualistic ant-plant symbioses, plants host ant colonies that defend them against herbivores. Here we show that the partners' investments in a widespread ant-plant symbiosis increase with water stress across 26 sites along a Mesoamerican precipitation gradient. At lower precipitation levels, Cordia alliodora trees invest more carbon in Azteca ants via phloem-feeding scale insects that provide the ants with sugars, and the ants provide better defense of the carbon-producing leaves. Under water stress, the trees have smaller carbon pools. A model of the carbon trade-offs for the mutualistic partners shows that the observed strategies can arise from the carbon costs of rare but extreme events of herbivory in the rainy season. Thus, water limitation, together with the risk of herbivory, increases the strength of a carbon-based mutualism.

    View details for DOI 10.1371/journal.pbio.1001705

    View details for PubMedID 24223521

  • Richness and Abundance of Ichneumonidae in a Fragmented Tropical Rain Forest NEOTROPICAL ENTOMOLOGY Ruiz-Guerra, B., Hanson, P., Guevara, R., Dirzo, R. 2013; 42 (5): 458-465
  • Consumer preference for seeds and seedlings of rare species impacts tree diversity at multiple scales OECOLOGIA Young, H. S., McCauley, D. J., Guevara, R., Dirzo, R. 2013; 172 (3): 857-867


    Positive density-dependent seed and seedling predation, where herbivores selectively eat seeds or seedlings of common species, is thought to play a major role in creating and maintaining plant community diversity. However, many herbivores and seed predators are known to exhibit preferences for rare foods, which could lead to negative density-dependent predation. In this study, we first demonstrate the occurrence of increased predation of locally rare tree species by a widespread group of insular seed and seedling predators, land crabs. We then build computer simulations based on these empirical data to examine the effects of such predation on diversity patterns. Simulations show that herbivore preferences for locally rare species are likely to drive scale-dependent effects on plant community diversity: at small scales these foraging patterns decrease plant community diversity via the selective consumption of rare plant species, while at the landscape level they should increase diversity, at least for short periods, by promoting clustered local dominance of a variety of species. Finally, we compared observed patterns of plant diversity at the site to those obtained via computer simulations, and found that diversity patterns generated under simulations were highly consistent with observed diversity patterns. We posit that preference for rare species by herbivores may be prevalent in low- or moderate-diversity systems, and that these effects may help explain diversity patterns across different spatial scales in such ecosystems.

    View details for DOI 10.1007/s00442-012-2542-2

    View details for Web of Science ID 000320409100021

    View details for PubMedID 23229391

  • Genetic basis of pathogen community structure for foundation tree species in a common garden and in the wild JOURNAL OF ECOLOGY Busby, P. E., Newcombe, G., Dirzo, R., Whitham, T. G. 2013; 101 (4): 867-877
  • Effects of mammalian herbivore declines on plant communities: observations and experiments in an African savanna JOURNAL OF ECOLOGY Young, H. S., McCauley, D. J., Helgen, K. M., Goheen, J. R., Otarola-Castillo, E., Palmer, T. M., Pringle, R. M., Young, T. P., Dirzo, R. 2013; 101 (4): 1030-1041
  • Ecological and evolutionary consequences of living in a defaunated world BIOLOGICAL CONSERVATION Galetti, M., Dirzo, R. 2013; 163: 1-6
  • Effects of grasses on sapling establishment and the role of transplanted saplings on the light environment of pastures: implications for tropical forest restoration APPLIED VEGETATION SCIENCE Meli, P., Dirzo, R. 2013; 16 (2): 296-304
  • The roles of productivity and ecosystem size in determining food chain length in tropical terrestrial ecosystems ECOLOGY Young, H. S., McCauley, D. J., Dunbar, R. B., Hutson, M. S., Ter-Kuile, M., Dirzo, R. 2013; 94 (3): 692-701


    Many different drivers, including productivity, ecosystem size, and disturbance, have been considered to explain natural variation in the length of food chains. Much remains unknown about the role of these various drivers in determining food chain length, and particularly about the mechanisms by which they may operate in terrestrial ecosystems, which have quite different ecological constraints than aquatic environments, where most food chain length studies have been thus far conducted. In this study, we tested the relative importance of ecosystem size and productivity in influencing food chain length in a terrestrial setting. We determined that (1) there is no effect of ecosystem size or productive space on food chain length; (2) rather, food chain length increases strongly and linearly with productivity; and (3) the observed changes in food chain length are likely achieved through a combination of changes in predator size, predator behavior, and consumer diversity along gradients in productivity. These results lend new insight into the mechanisms by which productivity can drive changes in food chain length, point to potential for systematic differences in the drivers of food web structure between terrestrial and aquatic systems, and challenge us to consider how ecological context may control the drivers that shape food chain length.

    View details for Web of Science ID 000317044300016

    View details for PubMedID 23687895

  • Plant defense, herbivory, and the growth of Cordia alliodora trees and their symbiotic Azteca ant colonies OECOLOGIA Pringle, E. G., Dirzo, R., Gordon, D. M. 2012; 170 (3): 677-685


    The effects of herbivory on plant fitness are integrated over a plant's lifetime, mediated by ontogenetic changes in plant defense, tolerance, and herbivore pressure. In symbiotic ant-plant mutualisms, plants provide nesting space and food for ants, and ants defend plants against herbivores. The benefit to the plant of sustaining the growth of symbiotic ant colonies depends on whether defense by the growing ant colony outpaces the plant's growth in defendable area and associated herbivore pressure. These relationships were investigated in the symbiotic mutualism between Cordia alliodora trees and Azteca pittieri ants in a Mexican tropical dry forest. As ant colonies grew, worker production remained constant relative to ant-colony size. As trees grew, leaf production increased relative to tree size. Moreover, larger trees hosted lower densities of ants, suggesting that ant-colony growth did not keep pace with tree growth. On leaves with ants experimentally excluded, herbivory per unit leaf area increased exponentially with tree size, indicating that larger trees experienced higher herbivore pressure per leaf area than smaller trees. Even with ant defense, herbivory increased with tree size. Therefore, although larger trees had larger ant colonies, ant density was lower in larger trees, and the ant colonies did not provide sufficient defense to compensate for the higher herbivore pressure in larger trees. These results suggest that in this system the tree can decrease herbivory by promoting ant-colony growth, i.e., sustaining space and food investment in ants, as long as the tree continues to grow.

    View details for DOI 10.1007/s00442-012-2340-x

    View details for Web of Science ID 000309866200009

    View details for PubMedID 22562422

  • Averting biodiversity collapse in tropical forest protected areas NATURE Laurance, W. F., Useche, D. C., Rendeiro, J., Kalka, M., Bradshaw, C. J., Sloan, S. P., Laurance, S. G., Campbell, M., Abernethy, K., Alvarez, P., Arroyo-Rodriguez, V., Ashton, P., Benitez-Malvido, J., Blom, A., Bobo, K. S., Cannon, C. H., Cao, M., Carroll, R., Chapman, C., Coates, R., Cords, M., Danielsen, F., De Dijn, B., Dinerstein, E., Donnelly, M. A., Edwards, D., Edwards, F., Farwig, N., Fashing, P., Forget, P., Foster, M., Gale, G., Harris, D., Harrison, R., Hart, J., Karpanty, S., Kress, W. J., Krishnaswamy, J., Logsdon, W., Lovett, J., Magnusson, W., Maisels, F., Marshall, A. R., McClearn, D., Mudappa, D., Nielsen, M. R., Pearson, R., Pitman, N., van der Ploeg, J., Plumptre, A., Poulsen, J., Quesada, M., Rainey, H., Robinson, D., Roetgers, C., Rovero, F., Scatena, F., Schulze, C., Sheil, D., Struhsaker, T., Terborgh, J., Thomas, D., Timm, R., Urbina-Cardona, J. N., Vasudevan, K., Wright, S. J., Arias-G, J. C., Arroyo, L., Ashton, M., Auzel, P., Babaasa, D., Babweteera, F., Baker, P., Banki, O., Bass, M., Bila-Isia, I., Blake, S., Brockelman, W., Brokaw, N., Bruehl, C. A., Bunyavejchewin, S., Chao, J., Chave, J., Chellam, R., Clark, C. J., Clavijo, J., Congdon, R., Corlett, R., Dattaraja, H. S., Dave, C., Davies, G., Beisiegel, B. d., da Silva, R. d., Di Fiore, A., Diesmos, A., Dirzo, R., Doran-Sheehy, D., Eaton, M., Emmons, L., Estrada, A., Ewango, C., Fedigan, L., Feer, F., Fruth, B., Willis, J. G., Goodale, U., Goodman, S., Guix, J. C., Guthiga, P., Haber, W., Hamer, K., Herbinger, I., Hill, J., Huang, Z., Sun, I. F., Ickes, K., Itoh, A., Ivanauskas, N., Jackes, B., Janovec, J., Janzen, D., Jiangming, M., Jin, C., Jones, T., Justiniano, H., Kalko, E., Kasangaki, A., Killeen, T., King, H., Klop, E., Knott, C., Kone, I., Kudavidanage, E., Ribeiro, J. L., Lattke, J., Laval, R., Lawton, R., Leal, M., Leighton, M., Lentino, M., Leonel, C., Lindsell, J., Ling-Ling, L., Linsenmair, K. E., Losos, E., Lugo, A., Lwanga, J., Mack, A. L., Martins, M., McGraw, W. S., McNab, R., Montag, L., Thompson, J. M., Nabe-Nielsen, J., Nakagawa, M., Nepal, S., Norconk, M., Novotny, V., O'Donnell, S., Opiang, M., Ouboter, P., Parker, K., Parthasarathy, N., Pisciotta, K., Prawiradilaga, D., Pringle, C., Rajathurai, S., Reichard, U., Reinartz, G., Renton, K., Reynolds, G., Reynolds, V., Riley, E., Roedel, M., Rothman, J., Round, P., Sakai, S., Sanaiotti, T., Savini, T., Schaab, G., Seidensticker, J., Siaka, A., Silman, M. R., Smith, T. B., de Almeida, S. S., Sodhi, N., Stanford, C., Stewart, K., Stokes, E., Stoner, K. E., Sukumar, R., Surbeck, M., Tobler, M., Tscharntke, T., Turkalo, A., Umapathy, G., Van Weerd, M., Rivera, J. V., Venkataraman, M., Venn, L., Verea, C., de Castilho, C. V., Waltert, M., Wang, B., Watts, D., Weber, W., West, P., Whitacre, D., Whitney, K., Wilkie, D., Williams, S., Wright, D. D., Wright, P., Xiankai, L., Yonzon, P., Zamzani, F. 2012; 489 (7415): 290-?


    The rapid disruption of tropical forests probably imperils global biodiversity more than any other contemporary phenomenon. With deforestation advancing quickly, protected areas are increasingly becoming final refuges for threatened species and natural ecosystem processes. However, many protected areas in the tropics are themselves vulnerable to human encroachment and other environmental stresses. As pressures mount, it is vital to know whether existing reserves can sustain their biodiversity. A critical constraint in addressing this question has been that data describing a broad array of biodiversity groups have been unavailable for a sufficiently large and representative sample of reserves. Here we present a uniquely comprehensive data set on changes over the past 20 to 30 years in 31 functional groups of species and 21 potential drivers of environmental change, for 60 protected areas stratified across the world’s major tropical regions. Our analysis reveals great variation in reserve ‘health’: about half of all reserves have been effective or performed passably, but the rest are experiencing an erosion of biodiversity that is often alarmingly widespread taxonomically and functionally. Habitat disruption, hunting and forest-product exploitation were the strongest predictors of declining reserve health. Crucially, environmental changes immediately outside reserves seemed nearly as important as those inside in determining their ecological fate, with changes inside reserves strongly mirroring those occurring around them. These findings suggest that tropical protected areas are often intimately linked ecologically to their surrounding habitats, and that a failure to stem broad-scale loss and degradation of such habitats could sharply increase the likelihood of serious biodiversity declines.

    View details for DOI 10.1038/nature11318

    View details for Web of Science ID 000308635900041

    View details for PubMedID 22832582

  • Effects of Spatial Subsidies and Habitat Structure on the Foraging Ecology and Size of Geckos PLOS ONE Briggs, A. A., Young, H. S., McCauley, D. J., Hathaway, S. A., Dirzo, R., Fisher, R. N. 2012; 7 (8)


    While it is well established that ecosystem subsidies--the addition of energy, nutrients, or materials across ecosystem boundaries--can affect consumer abundance, there is less information available on how subsidy levels may affect consumer diet, body condition, trophic position, and resource partitioning among consumer species. There is also little information on whether changes in vegetation structure commonly associated with spatial variation in subsidies may play an important role in driving consumer responses to subsidies. To address these knowledge gaps, we studied changes in abundance, diet, trophic position, size, and body condition of two congeneric gecko species (Lepidodactylus spp.) that coexist in palm dominated and native (hereafter dicot dominated) forests across the Central Pacific. These forests differ strongly both in the amount of marine subsidies that they receive from seabird guano and carcasses, and in the physical structure of the habitat. Contrary to other studies, we found that subsidy level had no impact on the abundance of either gecko species; it also did not have any apparent effects on resource partitioning between species. However, it did affect body size, dietary composition, and trophic position of both species. Geckos in subsidized, dicot forests were larger, had higher body condition and more diverse diets, and occupied a much higher trophic position than geckos found in palm dominated, low subsidy level forests. Both direct variation in subsidy levels and associated changes in habitat structure appear to play a role in driving these responses. These results suggest that variation in subsidy levels may drive important behavioral responses in predators, even when their numerical response is limited. Strong changes in trophic position of consumers also suggest that subsidies may drive increasingly complex food webs, with longer overall food chain length.

    View details for DOI 10.1371/journal.pone.0041364

    View details for Web of Science ID 000307380900010

    View details for PubMedID 22899995

  • Diversification and phylogeographic structure in widespread Azteca plant-ants from the northern Neotropics MOLECULAR ECOLOGY Pringle, E. G., Ramirez, S. R., Bonebrake, T. C., Gordon, D. M., Dirzo, R. 2012; 21 (14): 3576-3592


    The Neotropical myrmecophytic tree Cordia alliodora hosts symbiotic Azteca ants in most of its widespread range. The taxonomy of the genus Azteca is notoriously difficult, which has frequently obscured species identity in ecological studies. We used sequence data from one mitochondrial and four nuclear loci to infer phylogenetic relationships, patterns of geographic distribution, and timing of diversification for 182 colonies of five C. alliodora-dwelling Azteca species from Mexico to Colombia. All morphological species were recovered as monophyletic, but we identified at least five distinct genetic lineages within the most abundant and specialized species, Azteca pittieri. Mitochondrial and nuclear data were concordant at the species level, but not within species. Divergence time analyses estimated that C. alliodora-dwelling Azteca shared a common ancestor approximately 10-22million years ago, prior to the proposed arrival of the host tree in Middle America. Diversification in A. pittieri occurred in the Pleistocene and was not correlated with geographic distance, which suggests limited historical gene flow among geographically restricted populations. This contrasts with the previously reported lack of phylogeographic structure at this spatial scale in the host tree. Climatic niches, and particularly precipitation-related variables, did not overlap between the sites occupied by northern and southern lineages of A. pittieri. Together, these results suggest that restricted gene flow among ant populations may facilitate local adaptation to environmental heterogeneity. Differences in population structure between the ants and their host trees may profoundly affect the evolutionary dynamics of this widespread ant-plant mutualism.

    View details for DOI 10.1111/j.1365-294X.2012.05618.x

    View details for Web of Science ID 000306087100017

    View details for PubMedID 22646059

  • From wing to wing: the persistence of long ecological interaction chains in less-disturbed ecosystems SCIENTIFIC REPORTS McCauley, D. J., DeSalles, P. A., Young, H. S., Dunbar, R. B., Dirzo, R., Mills, M. M., Micheli, F. 2012; 2


    Human impact on biodiversity usually is measured by reduction in species abundance or richness. Just as important, but much more difficult to discern, is the anthropogenic elimination of ecological interactions. Here we report on the persistence of a long ecological interaction chain linking diverse food webs and habitats in the near-pristine portions of a remote Pacific atoll. Using biogeochemical assays, animal tracking, and field surveys we show that seabirds roosting on native trees fertilize soils, increasing coastal nutrients and the abundance of plankton, thus attracting manta rays to native forest coastlines. Partnered observations conducted in regions of this atoll where native trees have been replaced by human propagated palms reveal that this complex interaction chain linking trees to mantas readily breaks down. Taken together these findings provide a compelling example of how anthropogenic disturbance may be contributing to widespread reductions in ecological interaction chain length, thereby isolating and simplifying ecosystems.

    View details for DOI 10.1038/srep00409

    View details for Web of Science ID 000304393800001

    View details for PubMedID 22624091

  • The effect of land use change and ecotourism on biodiversity: a case study of Manuel Antonio, Costa Rica, from 1985 to 2008 LANDSCAPE ECOLOGY Broadbent, E. N., Zambrano, A. M., Dirzo, R., Durham, W. H., Driscoll, L., Gallagher, P., Salters, R., Schultz, J., Colmenares, A., Randolph, S. G. 2012; 27 (5): 731-744
  • Consequences of Fragmentation of Tropical Moist Forest for Birds and Their Role in Predation of Herbivorous Insects BIOTROPICA Ruiz-Guerra, B., Renton, K., Dirzo, R. 2012; 44 (2): 228-236
  • Intersexual comparison of DNA content by flow cytometry, and chromosome number in four dioecious Chamaedorea palms from Mexico CARYOLOGIA Cepeda-Cornejo, V., Palomino, G., Mendez, I., Dirzo, R. 2012; 65 (4): 263-270


    Elucidating the factors that determine the abundance and distribution of species remains a central goal of ecology. It is well recognized that genetic differences among individual species can affect the distribution and species interactions of dependent taxa, but the ecological effects of genetic differences on taxa of the same trophic level remain much less understood. Our goal was to test the hypothesis that differences between related overstory tree species and their hybrids can influence the understory plant community in wild settings.We conducted vegetation surveys in a riparian community with the overstory dominated by Populus fremontii, P. angustifolia, and their natural hybrids (referred to as cross types) along the Weber River in north central Utah, USA. Understory diversity and community composition, as well as edaphic properties, were compared under individual trees.Diversity metrics differ under the three different tree cross types such that a greater species richness, diversity, and cover of understory plants exist under the hybrids compared with either of the parental taxa (30-54%, 40-48%, and 35-74% greater, respectively). The community composition of the understory also varied by cross type, whereby additional understory plant species cluster with hybrids, not with parental species.Genetic composition dictated by hybridization in the overstory can play a role in structuring the associated understory plants in natural communities-where a hybridized overstory correlates with a species-rich understory-and thus can have cascading effects on community members of the same trophic level. The underlying mechanism requires further investigation.

    View details for DOI 10.3732/ajb.1100137

    View details for Web of Science ID 000295888800018

    View details for PubMedID 21960550

  • Analysis of a hyper-diverse seed dispersal network: modularity and underlying mechanisms ECOLOGY LETTERS Donatti, C. I., Guimaraes, P. R., Galetti, M., Pizo, M. A., Marquitti, F. M., Dirzo, R. 2011; 14 (8): 773-781


    Mutualistic interactions involving pollination and ant-plant mutualistic networks typically feature tightly linked species grouped in modules. However, such modularity is infrequent in seed dispersal networks, presumably because research on those networks predominantly includes a single taxonomic animal group (e.g. birds). Herein, for the first time, we examine the pattern of interaction in a network that includes multiple taxonomic groups of seed dispersers, and the mechanisms underlying modularity. We found that the network was nested and modular, with five distinguishable modules. Our examination of the mechanisms underlying such modularity showed that plant and animal trait values were associated with specific modules but phylogenetic effect was limited. Thus, the pattern of interaction in this network is only partially explained by shared evolutionary history. We conclude that the observed modularity emerged by a combination of phylogenetic history and trait convergence of phylogenetically unrelated species, shaped by interactions with particular types of dispersal agents.

    View details for DOI 10.1111/j.1461-0248.2011.01639.x

    View details for Web of Science ID 000292864400007

    View details for PubMedID 21699640

  • Differential diameter-size effects of forest management on tree species richness and community structure: implications for conservation BIODIVERSITY AND CONSERVATION Gutierrez-Granados, G., Perez-Salicrup, D. R., Dirzo, R. 2011; 20 (7): 1571-1585
  • Distinct Leaf-trait Syndromes of Evergreen and Deciduous Trees in a Seasonally Dry Tropical Forest BIOTROPICA Pringle, E. G., Adams, R. I., Broadbent, E., Busby, P. E., Donatti, C. I., Kurten, E. L., Renton, K., Dirzo, R. 2011; 43 (3): 299-308
  • A Novel Method to Improve Individual Animal Identification Based on Camera-Trapping Data JOURNAL OF WILDLIFE MANAGEMENT Mendoza, E., Martineau, P. R., Brenner, E., Dirzo, R. 2011; 75 (4): 973-979

    View details for DOI 10.1002/jwmg.120

    View details for Web of Science ID 000291818100025



    Seabirds often cause significant changes to soil properties, and seabird-dominated systems often host unique plant communities. This study experimentally (1) examined species-specific responses to seabird guano gradients, (2) considered the role that differential functional traits among species play in altering plant response to guano, and (3) investigated the implications of seabird guano on range-expanding species.Using a greenhouse fertilization experiment, we examined how guano fertilization affects the growth and functional traits of four tree species dominant in the Pacific Islands: Cocos nucifera, Pisonia grandis, Scaevola sericea, and Tournefortia argentea. In these systems, seabirds are frequently found in association with three of these four species; the remaining species, C. nucifera, is a recently proliferating species commonly found in the region but rarely associated with seabirds.We determined that responses to guano addition differed significantly between species in ways that were consistent with predictions based on differing functional traits among species. Notably, we demonstrated that C. nucifera showed no growth responses to guano additions, whereas all seabird-associated plants showed strong responses.These results provide experimental evidence of differential species response to guano additions, suggesting that differences in species functional traits may contribute to changes in plant communities in seabird-dominated areas, with seabird-associated species garnering performance advantages in these high-nutrient environments. Among these species, results also suggest that C. nucifera may have a competitive advantage in low-nutrient environments, providing an unusual example of how a range-expanding plant species can profit from low-nutrient environments.

    View details for DOI 10.3732/ajb.1000159

    View details for Web of Science ID 000286884500015

    View details for PubMedID 21613110

  • Indirect benefits of symbiotic coccoids for an ant-defended myrmecophytic tree ECOLOGY Pringle, E. G., Dirzo, R., Gordon, D. M. 2011; 92 (1): 37-46


    The net benefits of mutualism depend directly on the costs and effectiveness of mutualistic services and indirectly on the interactions that affect those services. We examined interactions among Cordia alliodora myrmecophytic trees, their symbiotic ants Azteca pittieri, coccoid hemipterans, and foliar herbivores in two Neotropical dry forests. The tree makes two investments in symbiotic ants: it supplies nesting space, as domatia, and it provides phloem to coccoids, which then produce honeydew that is consumed by ants. Although higher densities of coccoids should have higher direct costs for trees, we asked whether higher densities of coccoids can also have higher indirect benefits for trees by increasing the effectiveness of ant defense against foliar herbivores. We found that trees benefited from ant defense against herbivores. Ants defended trees effectively only when colonies reached high densities within trees, and ant and coccoid densities within trees were strongly positively correlated. The benefits of reduced foliar herbivory by larger ant colonies were therefore indirectly controlled by the number of coccoids. Coccoid honeydew supply also affected per capita ant aggression against tree herbivores. Ants experimentally fed a carbohydrate-rich diet, analogous to sugar obtained from coccoids, were more aggressive against caterpillars per capita than ants fed a carbohydrate-poor diet. Ant defense was more effective on more valuable and vulnerable young leaves than on older leaves. Young domatia, associated with young leaves, contained higher coccoid densities than older domatia, which suggests that coccoids may also drive spatially favorable ant defense of the tree. If higher investments by one mutualistic partner are tied to higher benefits received from the other, there may be positive feedback between partners that will stabilize the mutualism. These results suggest that higher investment by trees in coccoids leads to more effective defense by ants against the tree's foliar herbivores.

    View details for Web of Science ID 000289552200006

    View details for PubMedID 21560674

  • Effects of forest fragmentation on assemblages of pollinators and floral visitors to male- and female-phase inflorescences of Astrocaryum mexicanum (Arecaceae) in a Mexican rain forest JOURNAL OF TROPICAL ECOLOGY Aguirre, A., Guevara, R., Dirzo, R. 2011; 27: 25-33
  • The coconut palm, Cocos nucifera, impacts forest composition and soil characteristics at Palmyra Atoll, Central Pacific JOURNAL OF VEGETATION SCIENCE Young, H. S., Raab, T. K., McCauley, D. J., Briggs, A. A., Dirzo, R. 2010; 21 (6): 1058-1068
  • Plant stages with biotic, indirect defences are more palatable and suffer less herbivory than their undefended counterparts BIOLOGICAL JOURNAL OF THE LINNEAN SOCIETY Llandres, A. L., Rodriguez-Girones, M. A., Dirzo, R. 2010; 101 (3): 536-543
  • Delineation of biogeomorphic land units across a tropical natural and humanized terrain in Los Tuxtlas, Veracruz, Mexico GEOMORPHOLOGY Concepcion Garcia-Aguirre, M., Alvarez, R., Dirzo, R., Ortiz, M. A., Eng, M. M. 2010; 121 (3-4): 245-256
  • Experimental defoliation affects male but not female reproductive performance of the tropical monoecious plant Croton suberosus (Euphorbiaceae) ANNALS OF BOTANY Narbona, E., Dirzo, R. 2010; 106 (2): 359-369


    Monoecious plants have the capacity to allocate resources separately to male and female functions more easily than hermaphrodites. This can be advantageous against environmental stresses such as leaf herbivory. However, studies showing effects of herbivory on male and female functions and on the interaction with the plant's pollinators are limited, particularly in tropical plants. Here, the effects of experimental defoliation were examined in the monoecious shrub Croton suberosus (Euphorbiaceae), a wasp-pollinated species from a Mexican tropical dry forest.Three defoliation treatments were applied: 0 % (control), 25 % (low) or 75 % (high) of plant leaf area removed. Vegetative (production of new leaves) and reproductive (pistillate and staminate flower production, pollen viability, nectar production, fruit set, and seed set) performance variables, and the abundance and activity of floral visitors were examined.Defoliated plants overcompensated for tissue loss by producing more new leaves than control plants. Production of staminate flowers gradually decreased with increasing defoliation and the floral sex ratio (staminate : pistillate flowers) was drastically reduced in high-defoliation plants. In contrast, female reproductive performance (pistillate flower production, fruit set and seed set) and pollinator visitation and abundance were not impacted by defoliation.The asymmetrical effects of defoliation on male and female traits of C. suberosus may be due to the temporal and spatial flexibility in the allocation of resources deployed by monoecious plants. We posit that this helps to maintain the plant's pollination success in the face of leaf herbivory stress.

    View details for DOI 10.1093/aob/mcq117

    View details for Web of Science ID 000280264400012

    View details for PubMedID 20519239



    Typically, plant-pollinator interactions are recognized as mutualistic relationships. Flower visitors, however, can potentially play multiple roles. The floral nectar in Croton suberosus has been proposed to operate as a reward for predators, especially the wasp Polistes instabilis (Vespidae), which kills herbivorous insects, while the plant has been thought to be mainly wind-pollinated. In this study, we reassessed the pollination mode of C. suberosus and the possible role of its flower visitors. Pollinator exclusion experiments demonstrated that C. suberosus should be considered a strictly entomophilous species. Inflorescences of C. suberosus were visited by a diverse entomofauna involving 28 taxa belonging to six orders; however, wasps and bees were the only visitors that carried C. suberosus pollen. The visitation rate of wasps was approximately four times that of bees. This observation, combined with the fact that the small size of bees makes effective contact of their bodies with the stigma difficult, strongly suggests that large wasps are responsible for most of the effective pollination of C. suberosus. Among the wasp visitors, P. instabilis seems to be one of the most important. These findings expose an unusual plant-insect interaction, in which the plant provides nectar and wasps pollinate and defend the plant.

    View details for DOI 10.3732/ajb.0900259

    View details for Web of Science ID 000276045500014

    View details for PubMedID 21622429

  • Sex-Related Differences in Reproductive Allocation, Growth, Defense and Herbivory in Three Dioecious Neotropical Palms PLOS ONE Cepeda-Cornejo, V., Dirzo, R. 2010; 5 (3)


    Frequently, in dioecious plants, female plants allocate more resources to reproduction than male plants. Therefore it is expected that asymmetrical allocation to reproduction may lead to a reproduction-growth tradeoff, whereby female plants grow less than male plants, but invest more in defenses and thus experience lower herbivory than male plants.We tested these expectations by comparing resource allocation to reproduction, growth and defense and its consequences on herbivory in three sympatric dioecious Chamaedorea palms (C. alternans, C. pinnatifrons and C. ernesti-augusti) using a pair-wise design (replicated male/female neighboring plants) in a Mexican tropical rain forest. Our findings support the predictions. Biomass allocation to reproduction in C. pinnatifrons was 3-times higher in female than male plants, consistent with what is known in C. alternans and C. ernesti-augusti. Growth (height and leaf production rate and biomass production) was higher in male plants of all three species. Female plants of the three species had traits that suggest greater investment in defense, as they had 4-16% tougher leaves, and 8-18% higher total phenolic compounds concentration. Accordingly, female plants sustained 53-78% lower standing herbivory and 49-87% lower herbivory rates than male plants.Our results suggests that resource allocation to reproduction in the studied palms is more costly to female plants and this leads to predictable intersexual differences in growth, defense and herbivory. We conclude that resource allocation to reproduction in plants can have important consequences that influence their interaction with herbivores. Since herbivory is recognized as an important selective force in plants, these results are of significance to our understanding of plant defense evolution.

    View details for DOI 10.1371/journal.pone.0009824

    View details for Web of Science ID 000275894400024

    View details for PubMedID 20352113

  • Importance of the lilac-crowned parrot in pre-dispersal seed predation of Astronium graveolens in a Mexican tropical dry forest JOURNAL OF TROPICAL ECOLOGY Ines Villasenor-Sanchez, E., Dirzo, R., Renton, K. 2010; 26: 227-236
  • Plants cause ecosystem nutrient depletion via the interruption of bird-derived spatial subsidies PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA Young, H. S., McCauley, D. J., Dunbar, R. B., Dirzo, R. 2010; 107 (5): 2072-2077


    Plant introductions and subsequent community shifts are known to affect nutrient cycling, but most such studies have focused on nutrient enrichment effects. The nature of plant-driven nutrient depletions and the mechanisms by which these might occur are relatively poorly understood. In this study we demonstrate that the proliferation of the commonly introduced coconut palm, Cocos nucifera, interrupts the flow of allochthonous marine subsidies to terrestrial ecosystems via an indirect effect: impact on birds. Birds avoid nesting or roosting in C. nucifera, thus reducing the critical nutrient inputs they bring from the marine environment. These decreases in marine subsidies then lead to reductions in available soil nutrients, decreases in leaf nutrient quality, diminished leaf palatability, and reduced herbivory. This nutrient depletion pathway contrasts the more typical patterns of nutrient enrichment that follow plant species introductions. Research on the effects of spatial subsidy disruptions on ecosystems has not yet examined interruptions driven by changes within the recipient community, such as plant community shifts. The ubiquity of coconut palm introductions across the tropics and subtropics makes these observations particularly noteworthy. Equally important, the case of C. nucifera provides a strong demonstration of how plant community changes can dramatically impact the supply of allochthonous nutrients and thereby reshape energy flow in ecosystems.

    View details for DOI 10.1073/pnas.0914169107

    View details for Web of Science ID 000274296300049

    View details for PubMedID 20133852

  • Insect herbivory declines with forest fragmentation and covaries with plant regeneration mode: evidence from a Mexican tropical rain forest OIKOS Ruiz-Guerra, B., Guevara, R., Mariano, N. A., Dirzo, R. 2010; 119 (2): 317-325
  • Niche partitioning among and within sympatric tropical seabirds revealed by stable isotope analysis MARINE ECOLOGY PROGRESS SERIES Young, H. S., McCauley, D. J., Dirzo, R., Dunbar, R. B., Shaffer, S. A. 2010; 416: 285-294

    View details for DOI 10.3354/meps08756

    View details for Web of Science ID 000283446400023

  • Resource partitioning by species but not sex in sympatric boobies in the central Pacific Ocean MARINE ECOLOGY PROGRESS SERIES Young, H. S., Shaffer, S. A., McCauley, D. J., Foley, D. G., Dirzo, R., Block, B. A. 2010; 403: 291-301

    View details for DOI 10.3354/meps08478

    View details for Web of Science ID 000276799000024

  • Prevalence of Tree Regeneration by Sprouting and Seeding Along a Rainfall Gradient in Hawai'i BIOTROPICA Busby, P. E., Vitousek, P., Dirzo, R. 2010; 42 (1): 80-86
  • Indirect effects of timber extraction on plant recruitment and diversity via reductions in abundance of frugivorous spider monkeys JOURNAL OF TROPICAL ECOLOGY Gutierrez-Granados, G., Dirzo, R. 2010; 26: 45-52


    Tolerance, the capacity of plants to withstand attack by animals, as opposed to resistance, has been poorly examined in the context of seed predation. We investigated the role that the seed mass of the large-seeded endemic tree Aesculus californica plays as a tolerance trait to rodent attack by comparing, under greenhouse conditions, patterns of germination, and subsequent seedling growth, of seeds with a wide range of natural damage. Germination percentage was reduced by 50% and time to germination by 64% in attacked compared to intact seeds, and germination probability was negatively correlated with damage. Seedlings that emerged from intact seeds were taller and bore more leaves than those from damaged seeds. This species' large seed mass favors tolerance to damage because heavily damaged seeds are able to germinate and produce seedlings. This finding is significant given that seeds of this species are known to contain chemical compounds toxic to vertebrates, a resistance trait. We posit that this combination of tolerance and resistance traits might be a particularly effective antipredation strategy when seeds are exposed to a variety of vertebrate predators.

    View details for DOI 10.3732/ajb.0800297

    View details for Web of Science ID 000267870800005

    View details for PubMedID 21628274

  • Morphological variation in the flowers of Jacaratia mexicana A. DC. (Caricaceae), a subdioecious tree PLANT BIOLOGY Aguirre, A., Vallejo-Marin, M., Piedra-Malagon, E. M., Cruz-Ortega, R., Dirzo, R. 2009; 11 (3): 417-424


    The Caricaceae is a small family of tropical trees and herbs in which most species are dioecious. In the present study, we extend our previous work on dioecy in the Caricaceae, characterising the morphological variation in sexual expression in flowers of the dioecious tree Jacaratia mexicana. We found that, in J. mexicana, female plants produce only pistillate flowers, while male plants are sexually variable and can bear three different types of flowers: staminate, pistillate and perfect. To characterise the distinct types of flowers, we measured 26 morphological variables. Our results indicate that: (i) pistillate flowers from male trees carry healthy-looking ovules and are morphologically similar, although smaller than, pistillate flowers on female plants; (ii) staminate flowers have a rudimentary, non-functional pistil and are the only flowers capable of producing nectar; and (iii) perfect flowers produce healthy-looking ovules and pollen, but have smaller ovaries than pistillate flowers and fewer anthers than staminate flowers, and do not produce nectar. The restriction of sexual variation to male trees is consistent with the evolutionary path of dioecy from hermaphrodite ancestors through the initial invasion of male-sterile plants and a subsequent gradual reduction in female fertility in cosexual individuals (gynodioecy pathway), but further work is needed to confirm this hypothesis.

    View details for DOI 10.1111/j.1438-8677.2008.00154.x

    View details for Web of Science ID 000265015300015

    View details for PubMedID 19470112

  • Effects of fragmentation on pollinator abundance and fruit set of an abundant understory palm in a Mexican tropical forest BIOLOGICAL CONSERVATION Aguirre, A., Dirzo, R. 2008; 141 (2): 375-384
  • Effects of Amazonian forest fragmentation on the interaction between plants, insect herbivores, and their natural enemies JOURNAL OF TROPICAL ECOLOGY Faveri, S. B., Vasconcelos, H. L., Dirzo, R. 2008; 24: 57-64
  • Seed-size variation determines interspecific differential predation by mammals in a neotropical rain forest OIKOS Mendoza, E., Dirzo, R. 2007; 116 (11): 1841-1852
  • The plight of large animals in tropical forests and the consequences for plant regeneration BIOTROPICA Wright, S. J., Stoner, K. E., Beckman, N., Corlett, R. T., Dirzo, R., Muller-Landau, H. C., Nunez-Iturri, G., Peres, C. A., Wang, B. C. 2007; 39 (3): 289-291
  • Size-related differential seed predation in a heavily defaunated neotropical rain forest BIOTROPICA Dirzo, R., Mendoza, E., Ortiz, P. 2007; 39 (3): 355-362
  • Ontogenetic switches from plant resistance to tolerance: minimizing costs with age? ECOLOGY LETTERS Boege, K., Dirzo, R., Siemens, D., Brown, P. 2007; 10 (3): 177-187


    Changes in herbivory and resource availability during a plant's development should promote ontogenetic shifts in resistance and tolerance, if the costs and benefits of these basic strategies also change as plants develop. We proposed and tested a general model to detect the expression of ontogenetic tradeoffs for these two alternative anti-herbivory strategies in Raphanus sativus. We found that ontogenetic trajectories occur in both resistance and tolerance but in opposite directions. The juvenile stage was more resistant but less tolerant than the reproductive stage. The ontogenetic switch from resistance to tolerance was consistent with the greater vulnerability of young plants to leaf damage and with the costs of resistance and tolerance found at each stage. We posit that the ontogenetic perspective presented here will be helpful in resolving the current debate on the existence and detection of a general resistance-tolerance tradeoff.

    View details for DOI 10.1111/j.1461-0248.2006.01012.x

    View details for Web of Science ID 000244227800003

    View details for PubMedID 17305801

  • Floristic diversity of sabal palmetto woodland: an endemic and endangered vegetation type from Mexico BIODIVERSITY AND CONSERVATION Lopez, J. C., Dirzo, R. 2007; 16 (3): 807-825
  • Variation in sexual expression in Jacaratia mexicana (Caricaceae) in southern Mexico: Frequency and relative seed performance of fruit-producing males BIOTROPICA Aguirre, A., Vallejo-Marin, M., Salazar-Goroztieta, L., Arias, D. M., Dirzo, R. 2007; 39 (1): 79-86
  • Biased seed rain in forest edges: Evidence from the Brazilian Atlantic forest BIOLOGICAL CONSERVATION de Melo, F. P., Dirzo, R., Tabarelli, M. 2006; 132 (1): 50-60
  • A quantitative analysis of forest fragmentation in Los Tuxtlas, southeast Mexico: patterns and implications for conservation REVISTA CHILENA DE HISTORIA NATURAL Mendoza, E., Fay, J., Dirzo, R. 2005; 78 (3): 451-467
  • Myrmecophily: Plants with their own army INTERCIENCIA Del Val, E., Dirzo, R. 2004; 29 (12): 673-?
  • Intraspecific variation in growth, defense and herbivory in Dialium guianense (Caesalpiniaceae) mediated by edaphic heterogeneity PLANT ECOLOGY Boege, K., Dirzo, R. 2004; 175 (1): 59-69
  • Global state of biodiversity and loss Annual Review of Environment and Natural Resources Rodolfo Dirzo, Peter Raven 2003; 28: 137-167
  • Biodiversity - Global biodiversity scenarios for the year 2100 SCIENCE Sala, O. E., Chapin, F. S., Armesto, J. J., Berlow, E., Bloomfield, J., Dirzo, R., Huber-Sanwald, E., Huenneke, L. F., Jackson, R. B., Kinzig, A., Leemans, R., Lodge, D. M., Mooney, H. A., Oesterheld, M., Poff, N. L., Sykes, M. T., Walker, B. H., Walker, M., Wall, D. H. 2000; 287 (5459): 1770-1774

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