Benefits for Plants in Ant-Plant Protective Mutualisms: A Meta-Analysis

Costs and benefits for partners in mutualistic interactions can vary greatly, but surprisingly little is known about the factors that drive this variation across systems. We conducted a meta-analysis of ant-plant protective mutualisms to quantify the effects of ant defenders on plant reproductive output, to evaluate if reproductive effects were predicted from reductions in herbivory and to identify characteristics of the plants, ants and environment that explained variation in ant protection. We also compared our approach with two other recent meta-analyses on ant-plant mutualisms, emphasizing differences in our methodology (using a weighted linear mixed effects model) and our focus on plant reproduction rather than herbivore damage. Based on 59 ant and plant species pairs, ant presence increased plant reproductive output by 49% and reduced herbivory by 62%. The effects on herbivory and reproduction within systems were positively correlated, but the slope of this relationship (0.75) indicated that tolerance to foliar herbivory may be a common plant response to absence of ant guards. Furthermore, the relationship between foliar damage and reproduction varied substantially among systems, suggesting that herbivore damage is not a reliable surrogate for fitness consequences of ant protection. Studies that experimentally excluded ants reported a smaller effect of ant protection on plant reproduction than studies that relied upon natural variation in ant presence, suggesting that study methods can affect results in these systems. Of the ecological variables included in our analysis, only plant life history (i.e., annual or perennial) explained variation in the protective benefit of mutualistic ants: presence of ants benefitted reproduction of perennials significantly more than that of annuals. These results contrast with other quantitative reviews of these relationships that did not include plant life history as an explanatory factor and raise several questions to guide future research on ant-plant protection mutualisms.

[1]  E. Bruna,et al.  Effects of plant age, experimental nutrient addition and ant occupancy on herbivory in a neotropical myrmecophyte , 2006 .

[2]  David P Edwards.  The roles of tolerance in the evolution, maintenance and breakdown of mutualism , 2009, Naturwissenschaften.

[3]  E. A. Catchpole,et al.  Ants and extrafloral nectaries: no evidence for plant protection in Helichrysum spp. — ant interactions , 1983, Oecologia.

[4]  T. Palmer,et al.  Short-term dynamics of an acacia ant community in Laikipia, Kenya , 2000, Oecologia.

[5]  Benjamin M. Bolker,et al.  Ecological Models and Data in R , 2008 .

[6]  Douglas W. Yu,et al.  Experimental demonstration of species coexistence enabled by dispersal limitation , 2004 .

[7]  N. Pierce,et al.  A castration parasite of an ant–plant mutualism , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[8]  G. Arnqvist,et al.  MetaWin: Statistical Software for Meta-Analysis with Resampling Tests. Version 1.Michael S. Rosenberg , Dean C. Adams , Jessica Gurevitch , 1998 .

[9]  A. Evans,et al.  Sterilization and canopy modification of a swollen thorn acacia tree by a plant-ant , 1999, Nature.

[10]  H. Vasconcelos,et al.  Cheating the cheater: domatia loss minimizes the effects of ant castration in an Amazonian ant-plant , 2002, Oecologia.

[11]  R. Leimu,et al.  A Meta-Analysis of Local Adaptation in Plants , 2008, PloS one.

[12]  S. D. Cooper,et al.  The importance of data-selection criteria: meta-analyses of stream predation experiments , 1999 .

[13]  G. Stone,et al.  How aggressive ant-guards assist seed-set in Acacia flowers , 1997, Nature.

[14]  N. E. Raine,et al.  Guards and thieves: antagonistic interactions between two ant species coexisting on the same ant‐plant , 2004 .

[15]  C. Osenberg,et al.  CRYPTIC DENSITY DEPENDENCE: EFFECTS OF COVARIATION BETWEEN DENSITY AND SITE QUALITY IN REEF FISH , 2003 .

[16]  Douglas W. Yu.  Regular ArticleParasites of mutualisms , 2001 .

[17]  T. Itioka,et al.  Effects of food rewards offered by ant–plant Macaranga on the colony size of ants , 2001, Ecological Research.

[18]  A. Agrawal,et al.  Dynamic anti-herbivore defense in ant-plants : the role of induced responses , 1998 .

[19]  T. Miller.  Does having multiple partners weaken the benefits of facultative mutualism? A test with cacti and cactus‐tending ants , 2007 .

[20]  Robert D. Holt,et al.  RESOLVING ECOLOGICAL QUESTIONS THROUGH META‐ANALYSIS: GOALS, METRICS, AND MODELS , 1999 .

[21]  K. Linsenmair,et al.  Reduced chemical defence in ant‐plants? A critical re‐evaluation of a widely accepted hypothesis , 2002 .

[22]  T. Whitham,et al.  The Continuum of Plant Responses to Herbivory: The Influence of Plant Association, Nutrient Availability, and Timing , 1989, The American Naturalist.

[23]  Jessica Gurevitch,et al.  STATISTICAL ISSUES IN ECOLOGICAL META‐ANALYSES , 1999 .

[24]  D. Janzen.  COEVOLUTION OF MUTUALISM BETWEEN ANTS AND ACACIAS IN CENTRAL AMERICA , 1966, Evolution; international journal of organic evolution.

[25]  D. Davidson,et al.  Myrmecophytic Cecropia: antiherbivore defenses under different nutrient treatments , 1995, Oecologia.

[26]  D. McKey,et al.  Protective ant-plant interactions as model systems in ecological and evolutionary research. , 2003 .

[27]  R. Borges,et al.  Ant–plant conflicts and a novel case of castration parasitism in a myrmecophyte , 2005 .

[28]  D. Bates,et al.  Mixed-Effects Models in S and S-PLUS , 2001 .

[29]  C. Horvitz,et al.  EFFECTS OF ANTS AND AN ANT-TENDED HERBIVORE ON SEED PRODUCTION OF A NEOTROPICAL HERB , 1984 .

[30]  M. Anstett,et al.  Benefits conferred by “timid” ants: active anti-herbivore protection of the rainforest tree Leonardoxa africana by the minute ant Petalomyrmex phylax , 1997, Oecologia.

[31]  L. B. Thien,et al.  Ant-mealybug interaction decreases reproductive fitness of Schomburgkia tibicinis (Orchidaceae) in Mexico , 1989, Journal of Tropical Ecology.

[32]  S. Chamberlain,et al.  Quantitative synthesis of context dependency in ant-plant protection mutualisms. , 2009, Ecology.

[33]  Douglas W. Yu.  Parasites of mutualisms , 2001 .

[34]  P. Coley,et al.  Effects of leaf age and plant life history patterns on herbivory , 1980, Nature.

[35]  B. Fisher.  Facultative ant association benefits a Neotropical orchid , 1992, Journal of Tropical Ecology.

[36]  S. D. Cooper,et al.  Effect Size in Ecological Experiments: The Application of Biological Models in Meta‐Analysis , 1997, The American Naturalist.

[37]  S. Rinaldi,et al.  Cheating and the evolutionary stability of mutualisms , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[38]  L. Dyer,et al.  Trophic cascades in a complex terrestrial community. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[39]  A. Agrawal,et al.  The ecology and evolution of plant tolerance to herbivory. , 1999, Trends in ecology & evolution.

[40]  M. Stanton.  Interacting Guilds: Moving beyond the Pairwise Perspective on Mutualisms , 2003, The American Naturalist.

[41]  Judith L. Bronstein,et al.  The Contribution of Ant‐Plant Protection Studies to Our Understanding of Mutualism 1 , 1998 .

[42]  J. A. Barone,et al.  HERBIVORY AND PLANT DEFENSES IN TROPICAL FORESTS , 1996 .

[43]  R. Borges,et al.  The fitness consequences of bearing domatia and having the right ant partner: experiments with protective and non-protective ants in a semi-myrmecophyte , 2005, Oecologia.

[44]  R. Karban,et al.  RELAXATION OF INDUCED INDIRECT DEFENSES OF ACACIAS FOLLOWING EXCLUSION OF MAMMALIAN HERBIVORES , 2004 .

[45]  N. E. Raine,et al.  Floral volatiles controlling ant behaviour , 2009 .

[46]  N. E. Raine,et al.  SPATIAL STRUCTURING AND FLORAL AVOIDANCE BEHAVIOR PREVENT ANT–POLLINATOR CONFLICT IN A MEXICAN ANT‐ACACIA , 2002 .

[47]  K. Linsenmair,et al.  Spatiotemporal patterns in indirect defence of a South-East Asian ant-plant support the optimal defence hypothesis , 2004, Journal of Tropical Ecology.

[48]  Jessica Gurevitch,et al.  THE META‐ANALYSIS OF RESPONSE RATIOS IN EXPERIMENTAL ECOLOGY , 1999 .

[49]  O. Schmitz,et al.  Trophic Cascades in Terrestrial Systems: A Review of the Effects of Carnivore Removals on Plants , 2000, The American Naturalist.

[50]  C. Tillberg.  Friend or foe? A behavioral and stable isotopic investigation of an ant–plant symbiosis , 2004, Oecologia.

[51]  L. Freitas,et al.  Nectaries and reproductive biology of Croton sarcopetalus (Euphorbiaceae) , 2001 .

[52]  J. Longino.  Geographic variation and community structure in an ant-plant mutualism: Azteca and Cecropia in Costa Rica , 1989 .

[53]  D. Davidson,et al.  Antiherbivore defenses of myrmecophytic Cecropia under different light regimes , 1994 .

[54]  R. Primack,et al.  Measuring Fitness and Natural Selection in Wild Plant Populations , 1989 .

[55]  M. Conroy,et al.  Analysis and Management of Animal Populations , 2002 .

[56]  D. Herms,et al.  The Dilemma of Plants: To Grow or Defend , 1992, The Quarterly Review of Biology.

[57]  L. Isbell,et al.  Ants on swollen-thorn acacias: species coexistence in a simple system , 1997, Oecologia.

[58]  T. Oliver,et al.  Tolerance traits and the stability of mutualism , 2009 .

[59]  C. Fonseca,et al.  ABIOTIC FACTORS AND THE CONDITIONAL OUTCOME OF AN ANT–PLANT MUTUALISM , 2005 .

[60]  Richard Karban,et al.  Breakdown of an Ant-Plant Mutualism Follows the Loss of Large Herbivores from an African Savanna , 2008, Science.

[61]  L. Prior,et al.  Ecological Models and Data in R , 2011 .

[62]  Fernando A. O. Silveira,et al.  Ants on plants: a meta-analysis of the role of ants as plant biotic defenses , 2009, Oecologia.

[63]  J. Six,et al.  Assessing the effect of elevated carbon dioxide on soil carbon: a comparison of four meta‐analyses , 2009 .

[64]  T. Palmer,et al.  Mutualism as reciprocal exploitation: African plant-ants defend foliar but not reproductive structures. , 2007, Ecology.