Swollen-thorn Acacias Research Articles

Scaling of indirect defences in Central American swollen-thorn acacias

AbstractMyrmecophytes may adjust the investment on ant rewards, depending on tree size and ant defence level. In swollen-thorn acacias (Vachellia collinsii), we tested whether the level of protection provided by the resident ants (defending vs. non-defending) influenced the relation between tree size and ant rewards, or between types of ant rewards (housing and food). We quantified ant rewards in trees occupied by defending and by non-defending ants. We predicted: (1) a positive relation between plant diameter and ant reward investment, with a steeper slope for defending than for non-defending ant species; and (2) that if there is any tradeoff between ant rewards, it should be aggravated (steeper slope) when inhabited by non-defending ants. We found that most structures for ants grew according to plant diameter, but contrary to our first prediction it was independent of the level of ant defence. Most ant rewards did not show a tradeoff between them, besides a weak negative relation between spine length and number of pinnules, which contrary to the prediction occurred when occupied by defending ants. The evidence shows that the interacting ants had a weaker influence on the scaling of defence structures in myrmecophytes than the habitat (location).

Short-term plasticity and variation in acacia ant-rewards under different conditions of ant occupancy and herbivory.

In ant-plant defense mutualisms, plants known as myrmecophytes provide food and shelter to ant partners in exchange for defense against herbivores and pathogens. To ensure interaction pay-off, myrmecophytes must regulate their investment in ant-rewards depending on local conditions and herbivore pressure. We investigated how myrmecophyte investment in multiple ant-rewards relates to herbivory, ant defense, and ant occupancy over time. Specifically, we examined the plasticity of ant-rewards produced by swollen-thorn acacias (Vachellia collinsii) under different ant occupancy and herbivory conditions. We compared food rewards (number of extrafloral nectaries and pinnules as a proxy for food bodies) and housing rewards (domatia dimensions) of V. collinsii for three conditions: (1) occupied (defended by the obligate mutualist Pseudomyrmex spinicola) versus unoccupied trees, (2) occupied trees subject to an experimental herbivory manipulation versus control trees, and (3) trees occupied by different ant species varying in their level of defense (P. spinicola, P. simulans, Crematogaster crinosa). We found that food rewards were more likely to vary in time depending on ant occupancy and resident species. Conversely, housing rewards varied with the condition (occupancy or species of partner) and less through time. A one-time herbivory manipulation did not cause any changes to the ant-rewards produced. Our results reveal short-term plasticity in V. collinsii ant-rewards and demonstrate that myrmecophytes with constitutive rewards can adjust their investment in ant-rewards depending on the presence and identity of ant partners.

Development and evolution of age-dependent defenses in ant-acacias

Age-dependent changes in plant defense against herbivores are widespread, but why these changes exist remains a mystery. We explored this question by examining a suite of traits required for the interaction between swollen thorn acacias (genus Vachellia) and ants of the genus Pseudomyrmex In this system, plants provide ants with refuge and food in the form of swollen stipular spines, protein-lipid-rich "Beltian" bodies, and sugar-secreting extrafloral nectaries-the "swollen thorn syndrome." We show that this syndrome develops at a predictable time in shoot development and is tightly associated with the temporal decline in the microRNAs miR156 and miR157 and a corresponding increase in their targets-the SPL transcription factors. Growth under reduced light intensity delays both the decline in miR156/157 and the development of the swollen thorn syndrome, supporting the conclusion that these traits are controlled by the miR156-SPL pathway. Production of extrafloral nectaries by Vachellia sp. that do not house ants is also correlated with a decline in miR156/157, suggesting that this syndrome evolved by co-opting a preexisting age-dependent program. Along with genetic evidence from other model systems, these findings support the hypothesis that the age-dependent development of the swollen thorn syndrome is a consequence of genetic regulation rather than a passive developmental pattern arising from developmental constraints on when these traits can develop.

Reduced Responsiveness to Volatile Signals Creates a Modular Reward Provisioning in an Obligate Food-for-Protection Mutualism.

Plants in more than 100 families secrete extrafloral nectar (EFN) to establish food-for-protection mutualisms with ants. Facultative ant-plants secrete EFN as a jasmonic acid (JA)-dependent response to attract generalist ants. In contrast, obligate ant-plants like the Central American “Swollen-Thorn Acacias” are colonized by specialized ants, although an individual host can carry ant colonies from different species that differ in the degree of protection they provide. We hypothesized that hosts that associate simultaneously with various partners should produce rewards in a modular manner to preferentially reward high quality partners. To test this hypothesis, we applied JA to distinct leaves and quantified cell wall invertase activity (CWIN; a regulator of nectar secretion) and EFN secretion by these “local” (i.e., treated) and the “systemic” (i.e., non-treated) leaves of the same branch. Both CWIN activity and EFN secretion increased in local and systemic leaves of the facultative ant-plant Acacia cochliacantha, but only in the local leaves of the obligate ant-plant, A. cornigera. The systemic EFN secretion in A. cochliacantha was associated with an enhanced emission of volatile organic compounds (VOCs). Such VOCs function as “external signals” that control systemic defense responses in diverse plant species. Indeed, the headspace of JA-treated branches of A. cochliacantha induced EFN secretion in both plant species, whereas the headspace of A. cornigera caused no detectable induction effect. Analyses of the headspace using GC-MS identified six VOCs in the headspace of A. cochliacantha that were not emitted by A. cornigera. Among these VOCs, β-caryophyllene and (cis)-hexenyl isovalerate have already been reported in other plant species to induce defense traits, including EFN secretion. Our observations underline the importance of VOCs as systemic within-plant signals and show that the modular rewarding in A. cornigera is likely to result from a reduced emission of the systemic signal, rather than from a reduced responsiveness to the signal. We suggest that modular rewarding allows hosts to restrict the metabolic investment to specific partners and to efficiently sanction potential exploiters.

A review of the Pseudomyrmex ferrugineus and Pseudomyrmex goeldii species groups: acacia-ants and relatives (Hymenoptera: Formicidae).

The Pseudomyrmex ferrugineus group contains the Mesoamerican acacia-ants, an assemblage of species that inhabit and protect swollen-thorn acacias (Vachellia spp.). Recent phylogenetic studies have confirmed the existence of two generalist (dead twig-inhabiting) species that are embedded within the P. ferrugineus group. They are described here as P. evitus sp. nov. (occurring from Mexico to Costa Rica) and P. feralis sp. nov. (Guatemala). The morphological definition of the P. ferrugineus group is revised to incorporate additional variability in the worker and queen castes. The previous diagnosis of the males, based largely on features of the genitalia, requires little revision. Closely related to the P. ferrugineus group is a clade of five predominantly South American species, here designated and diagnosed as the P. goeldii group. The five species, P. goeldii (Forel), P. laevifrons Ward, P. micans sp. nov., P. obtusus sp. nov., and P. parvulus sp. nov., are characterized and illustrated. P. laevifrons and P. micans are closely related and difficult to distinguish, possibly reflecting incomplete isolation. Keys are provided for the identification of the species in both groups.

The role of birds in the acacia—ant interaction: New insights from nest predation

The association of the swollen-thorn acacia (Acacia cornigera) and ants is an example of defensive mutualism. It has been shown that some bird species prefer to nest in myrmecophyte acacias, suggesting that their nests are protected from predators by the associated ants. Based on previous knowledge regarding the existence of extended benefits for birds in the acacia-ant interaction, the role of the rufous-naped wren was analyzed within the ant-acacia system. Nest predation was assessed taking into account tree species with and without myrmecophytic interactions, tree cover and height, the presence and abundance of ants, predator type, and the distance between each nest and the closest myrmecophyte acacia. The probability of survivorship of artificial nests using a known fate analysis was calculated. The results showed non-significant differences in the probability of survivorship regardless of the presence and density of myrmecophyte acacias, tree cover and height, the presence and abundance of ants, or predator type. Interestingly, the highest degree of predation in the artificial nests was related to the rufous-naped wren. These results suggest that the acacia-ant-bird interaction is more complex than previously perceived.

The web of the acacia orb-spider Eustala illicita (Araneae: Araneidae) with notes on its natural history

A great number of spiders build orb-webs and although the overall structure is the result of fixed behavioral patterns, much small-scale inter- and intraspecific variation is nonetheless evident. Thus in order to fully understand the orb-web and web-building behavior in these spiders, we need to study substantial samples of many different species of orb- weavers. However, to date only a few species have been rigorously studied both in the field and in the laboratory. Here, we investigate the ecology, behavior and orb-web of the neotropical spider Eustala illicita (O. Pickard-Cambridge 1889) and suggest it as suitable for further studies based on 1) the ease at which it can be located in abundant numbers in the field, 2) its willingness to build webs in the laboratory, 3) the plasticity of its behavior, and 4) its interesting ecology in the form of interactions with the swollen-thorn acacias and their ant mutualists. Here, we introduce its natural history and then provide a detailed description of orb-webs built in the field and in the laboratory, which we compare to other orb-spiders.

The interaction of thorns and symbiotic ants as an effective defence mechanism of swollen-thorn acacias.

Evidence is provided for the interaction of ants (Crematogaster spp.) and thorns as a means of defence against browsing mammals for one species of African myrmecophyte, Acacia drepanolobium. Two experiments were conducted using goats as representative mammalian browsers. In the first experiment, the defences of individual branches were manipulated in order to assess the effectiveness of ants and thorns both on their own and together as anti-herbivore defences. It was shown that ants on their own are more effective defences for a single branch than having neither ants nor thorns, but ants from a single branch do not add significantly to the effectiveness of thorns as an anti-herbivore defence. The second experiment looked at the effect of a whole tree of ants and how they interacted with thorns in the defence of the tree. It was shown that ants from a whole tree do significantly add to the effectiveness of thorns as an anti-herbivore defence. In all cases, the goat refused to go back to and feed from a tree whose ants had just attacked it. Thorns on their own, however, do not act as total browsing deterrents. They slow down the rate of feeding but animals may compensate for this by feeding for longer periods of time. The interaction of a whole tree of ants and thorns is a very effective browsing deterrent which causes the animal to stop feeding almost immediately, therefore keeping the amount of foliage lost to a minimum. These results provide support for the hypothesis that the ant-acacia relationship (in the case of A. drepanolobium) evolved at least partly because of pressure from browsing mammals.

Ants on swollen-thorn acacias: species coexistence in a simple system.

On the black cotton soils of the Laikipia ecosystem in Kenya, two swollen-thorn acacia species support nine ant species, four of which are apparently obligate plant-ants. Among the ants, there are five species of Crematogaster, two species of Camponotus, and one each of Tetraponera and Lepisota. Acacia drepanolobium is host to four ant species that are both common and mutually exclusive. These four ant species, and an additional non-exclusive ant species, tend to occur on trees of different sizes, implying a succession of ant occupants. Nonetheless, all four exclusive species occur in substantial proportions on trees of intermediate size. There is direct evidence that an early successional ant species (Tetraponera penzigi) is actively evicted by two late successional ant species in the genus Crematogaster. There was also some evidence of height differentiation among ant species resident on A. seyal. Different acacia-ant species had different direct effects on A. drepanolobium. Extrafloral nectaries were eaten and destroyed only on trees inhabited by Tetraponera. Axillary shoots were eaten only on trees inhabited by C. nigriceps (potentially another early successional ant). This was associated with more new terminal shoots and healthier leaves than other trees, but also the virtual elimination of flowering and fruiting. Different resident acacia-ant species also had characteristic relationships with other insects. Among the four mutually exclusive ant species, only Crematogaster sjostedti was associated with two species of Camponotus, at least one of which (C. rufoglaucus) appears to be a foraging non-resident. A. drepanolobium trees occupied by C. sjostedti were also far more heavily infested with leaf galls than were trees occupied by other ant species. A. drepanolobium trees occupied by C. mimosae and C. sjostedti uniquely had tended adult scale insects. This diversity of ant inhabitants, and their strikingly different relationships with their hosts and other insect species, are examples of coexisting diversity on an apparently uniform resource.

A New Genus and Species of Mealybug (Homoptera: Coccoidea: Pseudococcidae) Associated with Ants in Swollen Thorn Acacias in Tanzania

A New Genus and Species of Mealybug (Homoptera: Coccoidea: Pseudococcidae) Associated with Ants in Swollen Thorn Acacias in Tanzania

Mutualism between Three Species of Tropical Piper (Piperaceae) and Their Ant Inhabitants

Three species of the genus Piper (P. cenocladum G.DG., P. fimbriulatum G.DG., P. sagittifolium G.DG.) from the wet evergreen forest of Costa Rica are associated with ants of the genus Pheidole in what appears to be a coevolved mutualistic relationship. The ants live in petiolar cavities and in the stems which they hollow out; the plant produces lipid-rich food bodies inside the petiolar cavities on which the ants feed. The ants appear to increase the competitive fitness of the plants by removing encroaching vines. More importantly, it seems that the plant may receive a nutritional benefit from the ants' presence by absorbing nutrients released from decaying nest material inside the stem. Ant-plant mutualisms involving several plant families have been described in the Old and New World tropics (Hocking, 1970; Janzen, 1967, 1969a, 1972, 1973a, 1975; Rehr et al., 1973; Whiffin, 1972). The swollen-thorn acacia and its obligate ant inhabitant, Pseudomyrmex, is the most thoroughly studied ant plant, or myrmecophyte (Janzen, 1967, 1969a, b). However, most of the ant-plant associations described in the New World tropics are facultative. It is often the case that the plant produces extrafloral nectaries and is associated with aggressive ants that feed on the nectar source and in turn presumably protect the plant from herbivory (Bequaert, 1922; Carroll, 1974; Whiffin, 1972). We describe a situation involving three species of plants of the genus Piper (P. cenocladum C. DC, P. fimbriulatum C. DC, P. sagittifolium C. DC) that are always associated with ants of the genus Pheidole in what appears to be a coevolved mutualistic relationship. The occurrence of ants in these Piper species has been previously noted (Burger, 1972), but there are no* descriptions of the benefits that both ants and plant derive from the relationship. Piper cenocladum and P. fimbriulatum are slender shrublike plants that grow commonly to a height of 4 m, although P. fimbriulatum sometimes reaches a height of 7-8 m. Both species live in the understory of the wet evergreen forest of Costa Rica between sea level and approximately 1100 m altitude. Piper cenocladum is endemic to Costa Rica and is found only on the Caribbean coast, while P. fimbriulatum is found only on the Pacific coast of Costa Rica and in western Panama (Burger, 1971). Piper sagittifolium is a smaller herbaceous plant seldom exceeding 1.5 m in height and has only been recorded from the 1 Present address : Department of Zoology, University of Michigan, Ann

Predation on Swollen-Thorn Acacia Ants by White-faced Monkeys, Cebus capucinus

White-faced monkeys, Cebus capucinus, intensively preyed on the ant Pseudomyrrmex belti, that obligatorily occupies and protects swollen-thorn acacias, primarily Acacia collinsii, at the study site. The Cebus obtained ants and probably ant larvae from acacias by ripping off branches and opening thorns with their teeth. This action often resulted in extensive physical destruction of the acacia, loss of the ant colony, and subsequent death of the plant. Implications of this predation and other interactions between monkeys and myrmecophytes are discussed. IN THE MUTUALISTIC ASSOCIATION between obligate acacia ants (several species of the genus Pseudomyrmex) and swollen-thorn acacias (several species of the genus Acacia) of Central America, the plant provides the ants with food and domicile, while the ant protects the plant from herbivores (primarily insects) by stinging and from invading vegetation by biting it off (Janzen 1966, 1967, 1974). Although some arthropods, lizards, birds, and mammals are known to eat swollen-thorn acacia plant parts, extensive damage of ant-occupied swollen-thorn acacias from these animals is very infrequent. Evidence strongly suggests that large browsing mammals avoid occupied acacias because of the aggressive ants. Similarly, acacia ants and their larvae are seldom eaten from the swollen-thorn acacia by birds and arthropods. No mammal has been reported to intentionally eat acacia ants (Janzen 1969b). During a study of the ecology and behavior of the white-faced monkey, Cebus capucinus, in the tropical dry forest of northwest Costa Rica, Cebus interactions with ant-occupied swollen-thorn acacias provided an apparent exception to the effectiveness of this mutualistic association. These interactions and other observations of interactions between monkeys (Cebus and Ate/es geoffroyi) and myrmecophytes during the study are described in this paper. METHODS AND STUDY AREA From October 1971 to August 1973 observations were made intermittently on the three monkey species, Cebus capucinus, Ateles geoffroyi, and Alouatta palliata, of Santa Rosa National Park in Guanacaste Province, northwest Costa Rica. A more intensive study of Cebus ecology, using the focal animal technique (Altmann 1974), was conducted one week each month from January to August 1973 on a troop of 18 to 21 animals. Focal animals were under observation for about 25-35 hours each study week (except for only 13 hours in the study week in June) with observations generally spanning all hours of the day for a given week. Santa Rosa National Park is located approximately 50 km north-northwest off Liberia, Guanacaste Province. Most of the park is on a plateau of about 280 m, where a mosaic of forests and man-created savannahs occurs. The Cebus study area was located in deciduous, secondary forest averaging 10-15 m tall, the predominant forest type in the plateau area. Annual rainfall averages approximately 1750 mm, and almost all of it falls between mid-May and midDecember. Deciduous trees lose their leaves during the severe dry season. Swollen-thorn acacias (primarily Acacia collinsii) are common in these deciduous

Pseudomyrmex nigropilosa : A Parasite of a Mutualism

Pseudomyrmex nigropilosa is a parasite ofthe ant-acacia mutualism in Central America in that it harvests the resources of swollen-thorn acacias but does not protect the acacias. In the process, it also lowers the rate of occupation by the obligate acacia-ants, species of ants that do protect swollen-thorn acacias. Tenancy ofan acacia by P. nigropilosa must be temporary, since the unoccupied plant is shortly killed by herbivores or competing plants, or is taken over by obligate acacia-ants. As expected of a species of short-lived ant, a P. nigropilosa colony produces reproductives earlier in the life of the colony and maintains fewer grams of workers per gram of brood than does a colony of the long-lived obligate acacia-ants.

Nesting Association Between Two Neotropical Polybiine Wasps (Hymenoptera, Vespidae)

Nidification by the docile wasp, Mischocyttarus immarginatus, is highly selective for the immediate surroundings of Polybia occidentalis nests during the dry season in Costa Rica. INTERSPECIFIC NESTING RELATIONSHIPS may reflect the attempts of susceptible species to nest in proximity to more numerous or more aggressive species thereby lessening the effects of predation. The social Hymenoptera are commonly involved in nesting associations in the tropics. The nest-building activities of many birds are concentrated within a zone of safety surrounding the nests of aggressive vespid wasps such as Polistes in the Neotropics (Richards and Richards 1951) and Ropalidia in Africa (Moreau 1936). The nesting of oropendolas and caciques (Icteridae) near large nests of the polybiine wasps, Polybia (Myers 1929), Stelopolybia, Protopolybia, and the stingless bee Trigona, is thought by Smith (1968) to lessen predation by other vertebrates. The attraction of bird nesting to trees containing nests of the vicious African ant, Oecophylla, has been documented by MacLaren (1950). Janzen (1969) has shown that various lowland Central American birds nest preferentially in swollen thorn acacias (myrmecophytes) normally occupied by obligate acacia ants of the genus Pseu

Birds and the Ant × Acacia Interaction in Central America, with Notes on Birds and Other Myrmecophytes

This paper discusses the trophic and nesting relationships between birds, and swollenthorn acacias and their ant occupants. It is part of a study of the ecological position of myrmecophytes (plants that have a mutualistic interaction with the ants that live in them) in lowland Central American plant communities (Janzen 1966, 1967a, 1967b) and refers primarily to the ant-occupied acacias of the New World, which are found only in the lowlands of Central America and northern Colombia. The very meager information available on other myrmecophytes and their interactions with birds is included in context. There are fewer than 10 references to birds and

Fire, Vegetation Structure, and the Ant X Acacia Interaction in Central America

The effect of fire on swollen—thorn acacias and their tenant obligate acacia—ants in the Central American dry lowlands is discussed. Fires may either consume the entire acacia shoot and ant colony, scorch and kill the acacia but not the ants, or kill neither acacia nor ant colony. Which alternative occurs depends on the structure of the immediately surrounding vegetation which in turn depends on how much of it has been killed by the ant colony and how fast the acacia has grown. The survival of the acacia population in frequently burned areas is almost entirely dependent upon some ant colonies surviving the fire to occupy the new sucker shoots from acacia stumps. The effect of these fires on the evolution of the interaction between the ant and the acacia is discussed.

COEVOLUTION OF MUTUALISM BETWEEN ANTS AND ACACIAS IN CENTRAL AMERICA.

The purpose of this paper is to discuss the coevolution of one of the more thoroughly studied mutualistic systems in the New World tropics: the interdependency between the and their ant inhabitants. This system has recently been described in detail in respect to one species of plant, Acacia cornigera L. (Mimosoideae; Leguminosae), and one species of ant, Pseudomyrmex ferruginea F. Smith (Pseudomyrmecinae; Formicidae), and shown experimentally to be a case of mutualism (Janzen, 1966a). In this species pair, the ant is dependent upon the acacia for food and domicile, and the acacia is dependent upon the ant for protection from phytophagous insects and neighboring plants. The literature dealing only with the New World tropical (Acacia spp.) and their ants (Pseudomyrmex spp.) has been re-evaluated by Janzen (1966a) and will not be discussed further in a review sense. The higher plants that commonly have ant colonies living in them have long been termed myrmecophytes. Ants living in plants range in habit from fortuitous usage of a plant cavity to highly complex interaction systems between the ant and the higher plant. The ant-acacia system represents this latter extreme, and the acacia is by any definition a myrmecophyte. A review paper on the subject of myrmecophytes is in preparation. In the present paper, plants with ants living in them will be called ant-plants; the ants will be called plant-ants. The swollen-thorn acacias are those with 1) enlarged stipular thorns normally tenanted by ants, 2) enlarged foliar nectaries, 3) modified leaflet tips called Beltian bodies (eaten by the ants), and 4) nearly year-round leaf production and maintenance even in areas with a distinct dry season (Fig. 1). Swollen-thorn have been shown experimentally to have a virtually obligate dependency on 1 Contribution No. 1308 from the Department of Entomology, The University of Kansas, Lawrence. This study was supported by National Science Foundation Grant GB-1428 to the University of California, Berkeley (Dr. R. F. Smith), University of California Associates in Tropical Biogeography Research Grants 66 and 81, and The University of Kansas General Research Grant 3173-5038, and also is a by-product of National Science Foundation Grant GB-91 (Dr. C. D. Michener).