Light environment influences the flood tolerance in Cordia americana (L.) Gottschling & J.S.Mill.

The subtropical riverine forests present a variation in soil water availability throughout the year, following precipitation seasonality. The objective of this work was to evaluate the responses of Cordia americana to different light intensities combined with soil flooding. Seedlings were acclimated to light treatments, with full sun and shade conditions. Sun and shade plants were subjected to soil flooding during periods of 10 (short) and 30 (longer) days. After 10 days, flooded plants had a higher root dry mass accumulation and soluble sugars content, regardless of the light condition. Shade plants presented higher shoot soluble sugars content in relation to the sun plants. After 30 days, a higher shoot soluble sugar content was observed in sun and shade flooded plants. In addition, a higher root soluble sugar content was also observed in sun plants under flood. Periods of short flooding, characterized in subtropical forests as from 5 to 15 days, favor the growth of shade plants and the roots sugar accumulation, fact that can explain the species distribution. However, long periods of flooding may be associated with light environment plasticity, suggesting that the sun plants present a higher flooding tolerance, directly associated with the ability to maintain the sugar content.

Ant-plant mutualism: a dietary by-product of a tropical ant's macronutrient requirements.

Many arboreal ants depend on myrmecophytic plants for both food and shelter; in return, these ants defend their host plants against herbivores, which are often insects. Ant-plant and other mutualisms do not necessarily involve the exchange of costly rewards or services; they may instead result from by-product benefits, or positive outcomes that do not entail a cost for one or both partners. Here, we examined whether the plant-ant Allomerus octoarticulatus pays a short-term cost to defend their host plants against herbivores, or whether plant defense is a by-product benefit of ant foraging for insect prey. Because the food offered by ant-plants is usually nitrogen-poor, arboreal ants may balance their diets by consuming insect prey or associating with microbial symbionts to acquire nitrogen, potentially shifting the costs and benefits of plant defense for the ant partner. To determine the effect of ant diet on an ant-plant mutualism, we compared the behavior, morphology, fitness, stable isotope signatures, and gaster microbiomes of A. octoarticulatus ants nesting in Cordia nodosa trees maintained for nearly a year with or without insect herbivores. At the end of the experiment, ants from herbivore exclosures preferred protein-rich baits more than ants in the control (i.e., herbivores present) treatment. Furthermore, workers in the control treatment were heavier than in the herbivore-exclusion treatment, and worker mass predicted reproductive output, suggesting that foraging for insect prey directly increased ant colony fitness. The gaster microbiome of ants was not significantly affected by the herbivore exclusion treatment. We conclude that the defensive behavior of some phytoecious ants is a by-product of their need for external protein sources; thus, the consumption of insect herbivores by ants benefits both the ant colony and the host plant.

Drowning out the protection racket: partner manipulation or drought can strengthen ant-plant mutualism.

Two recent reports discuss interactions between plants and ants that defend them from herbivores. Acacia trees provide their ant bodyguards with a diet that reduces their ability to benefit from alternate hosts. Provisioning of ants by Cordia trees during drought may buy insurance against extreme defoliation events, not just average-year benefits.

Water stress strengthens mutualism among ants, trees, and scale insects.

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.

The direct and ecological costs of an ant-plant symbiosis.

How strong is selection for cheating in mutualisms? The answer depends on the type and magnitude of the costs of the mutualism. Here we investigated the direct and ecological costs of plant defense by ants in the association between Cordia nodosa, a myrmecophytic plant, and Allomerus octoarticulatus, a phytoecious ant. Cordia nodosa trees produce food and housing to reward ants that protect them against herbivores. For nearly 1 year, we manipulated the presence of A. octoarticulatus ants and most insect herbivores on C. nodosa in a full-factorial experiment. Ants increased plant growth when herbivores were present but decreased plant growth when herbivores were absent, indicating that hosting ants can be costly to plants. However, we did not detect a cost to ant colonies of defending host plants against herbivores. Although this asymmetry in costs suggests that the plants may be under stronger selection than the ants to cheat by withholding investment in their partner, the costs to C. nodosa are probably at least partly ecological, arising because ants tend scale insects on their host plants. We argue that ecological costs should favor resistance or traits other than cheating and thus that neither partner may face much temptation to cheat.

Plant defense, herbivory, and the growth of Cordia alliodora trees and their symbiotic Azteca ant colonies.

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.

Indirect benefits of symbiotic coccoids for an ant-defended myrmecophytic tree.

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.

Contrasting bee pollination in two co-occurring distylic species of Cordia (Cordiaceae, Boraginales) in the Brazilian semi-arid Caatinga: generalist in C. globosa vs. specialist in C. leucocephala.

In this study we compare the reproductive biology of Cordia globosa and C. leucocephala (Cordiaceae, Boraginales; formerly referred to Boraginaceae) to understand the functioning of the floral morphs and the relations with their effective pollinators. The species are synchronopatric, distylic, and self-incompatible. Though they share melittophilous traits, the main visitor and pollinator of C. globosa was the generalist and exotic bee Apis mellifera, while the only one of C. leucocephala was the oligoletic bee Ceblurgus longipalpis. These two latter species are restricted to the Caatinga of NE Brazil, contrasting with the wide distribution of Cordia globosa. While the fruit-set for C. globosa was high, independently if the pollen donor/stigma receptor was a pin (long-styled) or thrum (short-styled) individual, in C. leucocephala the fruit-set was low and occurred only when a thrum individual was the pollen donor. This raises the possibility of this species moving towards dioecy. The high natural fruit-set of C. globosa confirms the generalist bee as its effective pollinator. The low fruit-set after manual crosses in C. leucocephala may be due to low pollen viability. Additionally, the low natural fruit-set (two times lower than after crosses) may be related with the foraging behavior of the specialist pollinator.

Contrasting bee pollination in two co-occurring distylic species of Cordia (Cordiaceae, Boraginales) in the Brazilian semi-arid Caatinga: generalist in C. globosa vs. specialist in C. leucocephala

In this study we compare the reproductive biology of Cordia globosa and C. leucocephala (Cordiaceae, Boraginales; formerly referred to Boraginaceae) to understand the functioning of the floral morphs and the relations with their effective pollinators. The species are synchronopatric, distylic, and self-incompatible. Though they share melittophilous traits, the main visitor and pollinator of C. globosa was the generalist and exotic bee Apis mellifera, while the only one of C. leucocephala was the oligoletic bee Ceblurgus longipalpis. These two latter species are restricted to the Caatinga of NE Brazil, contrasting with the wide distribution of Cordia globosa. While the fruit-set for C. globosa was high, independently if the pollen donor/stigma receptor was a pin (long-styled) or thrum (short-styled) individual, in C. leucocephala the fruit-set was low and occurred only when a thrum individual was the pollen donor. This raises the possibility of this species moving towards dioecy. The high natural fruit-set of C. globosa confirms the generalist bee as its effective pollinator. The low fruit-set after manual crosses in C. leucocephala may be due to low pollen viability. Additionally, the low natural fruit-set (two times lower than after crosses) may be related with the foraging behavior of the specialist pollinator.

Neste estudo comparamos a biologia reprodutiva de Cordia globosa e C. leucocephala para entender a função dos orfos florais e as relações com seus polinizadores efetivos. As espécies são sincronopátricas, distílicas e auto-incompatíveis. Embora elas compartilhem atributos melitófilos, o principal visitante e polinizador de C. globosa foi Apis mellifera, abelha generalista e exótica, enquanto o de C. leucocephala foi a abelha oligolética Ceblurgus longipalpis. Essas duas últimas espécies são restritas à Caatinga do Nordeste do Brasil, contrastando com a ampla distribuição de C. globosa. Enquanto a formação de frutos de C. globosa foi alta, independente se o doador ou receptor de pólen era um indivíduo brevi- ou longistilo, em C. leucocephala a formação de frutos foi baixa e ocorreu apenas quando o doador de pólen era brevistilo. Este fato levanta a possibilidade desta espécie estar se movendo em direção à dioicia. A alta formação natural de frutos de C. globosa confirma a abelha generalista como seu polinizador efetivo. A baixa formação de frutos após cruzamentos manuais e C. leucocephala pode ser devida à baixa viabilidade polínica. Adicionalmente, a baixa formação natural de frutos (duas vezes menor que a de cruzamentos) pode estar relacionada com o comportamento de forrageamento do polinizador especialista.

Mutual reproductive dependence of distylic Cordia leucocephala (Cordiaceae) and oligolectic Ceblurgus longipalpis (Halictidae, Rophitinae) in the Caatinga.

BACKGROUND AND AIMS: The close relationship between distylic Cordia leucocephala and the bee Ceblurgus longipalpis, both endemic to the Caatinga, north-east Brazil, was investigated, emphasizing reproductive dependence, morphological adaptations of the partners, and pollen flow. METHODS: In the municipality of Pedra, in the Caatinga of Pernambuco, the breeding system and reproductive success of C. leucocephala, its interaction with flower visitors and inter- and intramorph pollen flow were determined. KEY RESULTS: The bee Ceblurgus longipalpis, the unique flower visitor and effective pollinator of self-incompatible Cordia leucocephala, presents morphological features adapted to exploit hidden pollen and nectar in the long and narrow corolla tubes. Pollen of low-level anthers is collected with hairs on prolonged mouthparts and pollen of high-level anthers with clypeus, mandibles, and labrum, showing pollen removal from both levels with the same effectiveness. In both morphs, this results in similar legitimate, i.e. intermorph cross-pollen flow. Illegitimate pollen flow to stigmas of pin flowers, however, was much higher than to stigmas of thrum flowers. Moreover, more illegitimate pollen was transported to stigmas of pin and less to those of thrum flowers when compared with legitimate pollen flow. CONCLUSIONS: The study reveals a one-to-one reproductive inter-dependence between both partners. Data indicate that this relationship between bee species and plant species is one of the rare cases of monolecty among bees. Monotypic Ceblurgus longipalpis, the only rophitine species of Brazil, evolved prolonged mouthparts rare among short-tongued bees that enable them to access pollen from flowers with short-level anthers hidden for bees of other species, and nectar at the base of the flower tube.

Formation and structure of food bodies in Cordia nodosa (Boraginaceae).

Cordia nodosa Lamark (Boraginaceae) is a myrmecophyte (i.e., plants housing ants in hollow structures) that provisions associated ants with food bodies (FBs) produced 24 h a day. Distributed over all the young parts of the plants, they induce ants to forage continually and so to protect the plants. Metabolites are stored in the inner cells of C. nodosa FBs as they form. In addition the peripheral cells have an extrafloral nectary-like function and secrete a substance that covers the FBs. The amalgam of these two functions, distinct in other known cases, is discussed taking into account the origin of FBs and extrafloral nectaries.

Ant species confer different partner benefits on two neotropical myrmecophytes.

The dynamics of mutualistic interactions involving more than a single pair of species depend on the relative costs and benefits of interaction among alternative partners. The neotropical myrmecophytes Cordia nodosa and Duroia hirsuta associate with several species of obligately symbiotic ants. I compared the ant partners of Cordia and Duroia with respect to two benefits known to be important in ant-myrmecophyte interactions: protection against herbivores provided by ants, and protection against encroaching vegetation provided by ants. Azteca spp., Myrmelachista schumanni, and Allomerus octoarticulatus demerarae ants all provide the leaves of Cordia and Duroia some protection against herbivores. However, Azteca and Allomerus provide more protection than does Myrmelachista to the leaves of their host plants. Although Allomerus protects the leaves of its hosts, plants occupied by Allomerus suffer more attacks by herbivores to their stems than do plants occupied by other ants. Relative to Azteca or Allomerus, Myrmelachista ants provide better protection against encroaching vegetation, increasing canopy openness over their host plants. These differences in benefits among the ant partners of Cordia and Duroia are reflected in the effect of each ant species on host plant size, growth rate, and reproduction. The results of this study show how mutualistic ant partners can differ with respect to both the magnitude and type of benefits they provide to the same species of myrmecophytic host.