Crematogaster Mimosae Research Articles

Symbiotic ant traits produce differential host-plant carbon and water dynamics in a multi-species mutualism.

Cooperative interactions may frequently be reinforced by "partner fidelity feedback," in which high- or low-quality partners drive positive feedbacks with high or low benefits for the host, respectively. Benefits of plant-animal mutualisms for plants have been quantified almost universally in terms of growth or reproduction, but these are only two of many sinks to which a host-plant allocates its resources. By investigating how partners to host-plants impact two fundamental plant resources, carbon and water, we can better characterize plant-partner fidelity and understand how plant-partner mutualisms may be modulated by resource dynamics. In Laikipia, Kenya, four ant species compete for Acacia drepanolobium host-plants. These ants differ in multiple traits, from nectar consumption to host-plant protection. Using a 5-year ant removal experiment, we compared carbon fixation, leaf water status, and stem non-structural carbohydrate concentrations for adult ant-plants with and without ant partners. Removal treatments showed that the ants differentially mediate tree carbon and/or water resources. All three ant species known to be aggressive against herbivores were linked to benefits for host-plant resources, but only the two species that defend but do not prune the host, Crematogaster mimosae and Tetraponera penzigi, increased tree carbon fixation. Of these two species, only the nectivore C. mimosae increased tree simple sugars. Crematogaster nigriceps, which defends the tree but also castrates flowers and prunes meristems, was linked only to lower tree water stress approximated by pre-dawn leaf water potential. In contrast to those defensive ants, Crematogaster sjostedti, a poor defender that displaces other ants, was linked to lower tree carbon fixation. Comparing the effects of the four ant species across control trees suggests that differential ant occupancy drives substantial differences in carbon and water supply among host trees. Our results highlight that ant partners can positively or negatively impact carbon and/or water relations for their host-plant, and we discuss the likelihood that carbon- and water-related partner fidelity feedback loops occur across ant-plant mutualisms.

Browsing impacts on Acacia drepanolobium Sjostedt and associated ant guilds in Ol Pejeta Conservancy, Kenya.

The numbers of Acacia drepanolobium trees are declining over much of Africa and large mammals particularly more prone and vulnerable to loss of habitat owing to human settlement encroachment. In Ol pejeta conservancy a sanctuary for the protection of the endangered black rhino, there is significant browse and vegetation pressure on the habitat particularly on the Acacia drepanolobium tree population. This study aimed to investigate the Acacia drepanolobium and ants’ interaction under different browsing intensities, determine effect of prescribed burnings on Crematogaster ants and Acacia drepanolobium interaction, investigate the tenancy dynamics of ants under varying morphological characteristics of Acacia drepanolobium trees, and finally to determine if Crematogaster ants’ communities/ colonization on Acacia drepanolobium change over time. Twelve (12) randomly chosen plots (keyed in a waypoint on the GPS) with fifty or more Acacia drepanolobium trees were studied for the study as follows, two (2) in a Chimpanzee Sanctuary where elephant, giraffe and rhino are excluded (control), six (6) in the reserve and four (4) in the Ranch. Two (2) plots treated with prescribed burning (fire) were compared with two un-burnt plots. All data collected was fed and entered into Excel spreadsheet and Statistical Package for the Social Science version 20 for analysis. The data were then processed into quantitative tables to give a comparative analysis for response obtained. Size class distributions of the reserve, Ranch and control were compared by means of Analysis of Variance (ANOVA) and other relevant parametric statistics. The result shows that in Ol pejeta conservancy browsing levels has statistically significant effect on Crematogaster ants and Acacia drepanolobium interaction. There was a strong and notable distinction between the four acacia ant species in the overall extends and levels of tenancy while responding to varied browsing pressures; Crematogaster mimosae and Tetraponera penzigi were found to be the most abundant/frequently observed ant species occupying trees in the reserve where there is intensive browsing (Reserve) and the ranch with medium browsing intensity. From this research experimental evidence explains the ability of trees to re-induce greater spine and gall numbers and that ant tenancy in A. drepanolobium is influenced by the tree’s morphological characteristics. The findings and results also indicated that prescribed burning significantly affected the type of ant inhabiting the A. drepanolobium tree. Going by the results of this paper, it was concluded that this mutualism is a key component of Ol pejeta biodiversity and ecosystem function. The study recommends that the results in this research should be used in determining ecological factors that influence conservation sustainability and predict the consequences of heavy browsing pressure, morphological characteristics and prescribed burning on the health of Acacia drepanolobium.

Population Genomics and Demographic Sampling of the Ant-Plant Vachellia drepanolobium and Its Symbiotic Ants From Sites Across Its Range in East Africa

The association between the African ant plant, Vachellia drepanolobium, and the ants that inhabit it has provided insight into the boundaries between mutualism and parasitism, the response of symbioses to environmental perturbations, and the ecology of species coexistence. We use a landscape genomics approach at sites sampled throughout the range of this system in Kenya to investigate the demographics and genetic structure of the different partners in the association. We find that different species of ant associates of V. drepanolobium show striking differences in their spatial distribution throughout Kenya, and these differences are only partly correlated with abiotic factors. A comparison of the population structure of the host plant and its three obligately arboreal ant symbionts, Crematogaster mimosae, Crematogaster nigriceps, and Tetraponera penzigi, shows that the ants exhibit somewhat similar patterns of structure throughout each of their respective ranges, but that this does not correlate in any clear way with the respective genetic structure of the populations of their host plants. A lack of evidence for local coadaptation in this system suggests that all partners have evolved to cope with a wide variety of biotic and abiotic conditions.

Left out in the cold: temperature-dependence of defense in an African ant-plant mutualism.

Many tropical plants are defended by ants, and the costs and benefits of these mutualisms can vary across gradients of herbivory, soil fertility, latitude, and other environmental factors. Yet despite an abundant literature documenting thermal constraints on ant activity and behavior, we know little about whether temperature variation can influence the benefits conferred by ants to plants. We evaluated the effects of dawn-to-dusk fluctuations in temperature on patrolling and aggressive behavior in four arboreal ant mutualists of Acacia drepanolobium trees in central Kenya. We found that ant aggressive behavior significantly increased with branch surface temperature, primarily in the two most aggressive ant species: Crematogaster mimosae and C.nigriceps workers attacked a simulated herbivore at higher rates as surface temperature rose. In a browsing experiment, we found that goats browsed more frequently and for longer durations on C.mimosae-defended trees during cooler times of day, while goat browsing on plants from which ants had been removed was not affected by temperature. Our study demonstrates temperature-dependence in the efficacy of ant defense against herbivory and suggests that these ant-plants may be more vulnerable to herbivory during cooler hours of the day, when many native browsers are most active.

Acacia Ants Respond to Plant-Borne Vibrations Caused by Mammalian Browsers

Living in the African savanna is dangerous, especially for plants. Many plants therefore engage in mutualism with ants, in which plants provide food and shelter in exchange for protection against herbivores. Ants become alarmed when the plant takes on some sort of damage. They immediately emerge from their plant shelter and aggressively defend the plant. Mammalian herbivores can have devastating effects on trees by browsing, breaking tree branches, stripping bark, and pushing over entire trees. However, mutualistic ants substantially reduce the amount of damage. To efficiently protect the tree, ants need to rapidly react together when the tree is under attack. Here, we show that the acacia ant Crematogaster mimosae defends its host tree by exploiting plant-borne vibrations caused by browsers feeding on the tree. Experiments with controlled vibrations show that ants discriminate browser-induced vibrations from those induced by wind, become alarmed, and patrol on the branches. Browser-induced vibrations serve as a long-distance alarm cue. The vibrations propagate through the whole acacia tree and trigger ants' defensive behavior, even on the other side of the tree. Furthermore, the ants make use of tropotactic directional vibration sensing to orient to the attacked part of the tree and fight back the attacker.

Economy of scale: third partner strengthens a keystone ant-plant mutualism.

While foundation species can stabilize ecosystems at landscape scales, their ability to persist is often underlain by keystone interactions occurring at smaller scales. Acacia drepanolobium is a foundation tree, comprising >95% of woody cover in East African black-cotton savanna ecosystems. Its dominance is underlain by a keystone mutualistic interaction with several symbiotic ant species in which it provides housing (swollen thorns) and carbohydrate-rich nectar from extra-floral nectaries (EFN). In return, it gains protection from catastrophic damage from mega-herbivores. Crematogaster mimosae is the ecologically dominant symbiotic ant in this system, also providing the highest protection services. In addition to tending EFN, C.mimosae tend scale insects for carbohydrate-rich honeydew. We investigated the role of scale insects in this specialized ant-plant interaction. Specifically, does this putatively redundant third partner strengthen the ant-plant mutualism by making the ant a better protector of the tree? Or does it weaken the mutualism by being costly to the tree while providing no additional benefit to the ant-plant mutualism? We coupled observational surveys with two scale-manipulation experiments and found evidence that this third partner strengthens the ant-plant mutualism. Trees with scale insects experimentally removed experienced a 2.5X increase in elephant damage compared to trees with scale insects present over 10 months. Reduced protection was driven by scale removal causing a decrease in ant colony size and per capita baseline activity and defensive behavior. We also found that ants increased scale-tending and the density of scale insects on trees when EFN were experimentally reduced. Thus, in this system, scale insects and EFN are likely complementary, rather than redundant, resources with scale insects benefitting ants when EFN production is low (such as during annual dry periods in this semi-arid ecosystem). This study reveals that a third-partner strengthens an ant-plant mutualism that serves to stabilize a whole ecosystem.

Polygyny does not explain the superior competitive ability of dominant ant associates in the African ant-plant, Acacia (Vachellia) drepanolobium.

The Acacia drepanolobium (also known as Vachellia drepanolobium) ant‐plant symbiosis is considered a classic case of species coexistence, in which four species of tree‐defending ants compete for nesting space in a single host tree species. Coexistence in this system has been explained by trade‐offs in the ability of the ant associates to compete with each other for occupied trees versus the ability to colonize unoccupied trees. We seek to understand the proximal reasons for how and why the ant species vary in competitive or colonizing abilities, which are largely unknown. In this study, we use RADseq‐derived SNPs to identify relatedness of workers in colonies to test the hypothesis that competitively dominant ants reach large colony sizes due to polygyny, that is, the presence of multiple egg‐laying queens in a single colony. We find that variation in polygyny is not associated with competitive ability; in fact, the most dominant species, unexpectedly, showed little evidence of polygyny. We also use these markers to investigate variation in mating behavior among the ant species and find that different species vary in the number of males fathering the offspring of each colony. Finally, we show that the nature of polygyny varies between the two commonly polygynous species, Crematogaster mimosae and Tetraponera penzigi: in C. mimosae, queens in the same colony are often related, while this is not the case for T. penzigi. These results shed light on factors influencing the evolution of species coexistence in an ant‐plant mutualism, as well as demonstrating the effectiveness of RADseq‐derived SNPs for parentage analysis.

Influence of neighboring plants on the dynamics of an ant-acacia protection mutualism.

Ant-plant protection symbioses, in which plants provide food and/or shelter for ants in exchange for protection from herbivory, are model systems for understanding the ecology of mutualism. While interactions between ants, host plants, and herbivores have been intensively studied, we know little about how plant-plant interactions influence the dynamics of these mutualisms, despite strong evidence that plants compete for resources, that hosting ants can be costly, and that host-plant provisioning to ants can therefore be constrained by resource availability. We used field experiments in a semiarid Kenyan savanna to examine interactions between the ant-plant Acacia drepanolobium, neighboring grasses, and two species of symbiotic acacia-ants with divergent behaviors: Crematogaster mimosae, an aggressive symbiont that imposes high costs to host trees via consumption of extrafloral nectar, and Tetraponera penzigi, a less-protective symbiont that imposes lower costs because it does not consume nectar. We hypothesized that by competing with acacias for resources, neighboring grasses (1) reduce hosts' ability to support costly C.mimosae, while having little or no effect on the ability of hosts to support low-cost T.penzigi, and (2) reduce sapling growth rates irrespective of ant occupant. We factorially manipulated the presence/absence of grasses and the identity of ant occupants on saplings and evaluated effects on colony survivorship and sapling growth rates over 40weeks. Contrary to prediction, the high-cost/high-reward nectar-dependent mutualist C.mimosae had higher colony-survival rates on saplings with grass neighbors present. Grasses appear to have indirectly facilitated the survival of C.mimosae by reducing water stress on host plants; soils under saplings shaded by grasses had higher moisture content, and these saplings produced more active nectaries than grass-removal saplings. Consistent with prediction, survival of low-cost/low-reward T.penzigi did not differ significantly between grass-removal treatments. Saplings occupied by low-cost/low-reward T.penzigi grew 100% more on average than saplings occupied by high-cost/high-reward C.mimosae, demonstrating that mutualist-partner identity strongly and differentially influences demographic rates of young plants. In contrast, contrary to prediction, grass neighbors had no significant net impact on sapling growth rates. Our results suggest that neighboring plants can exert strong and counterintuitive effects on ant-plant protection symbioses, highlighting the need to integrate plant-plant interactions into our understanding of these mutualisms.

Impacts of worker density in colony‐level aggression, expansion, and survival of the acacia‐ant Crematogaster mimosae

AbstractExperimental studies assessing the impact of demographic changes on aggression and inter‐group competitive outcomes in communities of social species are rare. This gap in our knowledge is important, not only because social species are foundational elements of many terrestrial ecosystems, but because interference competition among social groups often involves decision‐like processes influenced by demographic and environmental contexts. In East Africa, the symbiotic ant Crematogaster mimosae is a co‐dominant competitor that engages in high‐mortality, intra‐ and interspecific battles for sole possession of host trees. We manipulated worker density on C. mimosae Acacia host trees, and the colony's opportunity to expand onto neighboring trees to identify how these factors influenced colony‐level aggression, expansion success, and longer‐term survivorship. Worker density on focal trees was increased through translocation of domatia‐bearing branches, and was decreased using partial tree fumigations. We examined impacts of density manipulations on aggression and immediate expansion success under two different risk scenarios. We tied focal trees to either an experimentally emptied‐tree (low‐risk treatment), or to a C. nigriceps‐occupied tree (high‐risk treatment). Expansion success onto emptied neighbor trees was 100% for controls and increased‐density colonies, but only 50% for decreased‐density colonies, despite the fact that host trees are a limiting resource in this system. Success expanding onto trees occupied by a heterospecific competitor reached 36%, 40%, and 79% in decreased, control, and increased‐density trees, respectively. Our results show that changes in worker density due to disturbances or inter‐group battles have the potential to disrupt competitive hierarchies. Worker density manipulations also affected longer‐term colony persistence. Behavioral and genetic data revealed that 12 months after expansions 100% of the decreased‐density colonies, and 25% of control and increased‐density colonies, had been supplanted by neighboring opportunistic conspecifics. Intraspecific aggression may have lower costs in C. mimosae because aggressive colonies can incorporate workers or queens from defeated competitors. The unexpectedly high frequency of conflicts between conspecific C. mimosae, in combination with behaviors decreasing the cost of intraspecific competition relative to interspecific conflict, may create opportunities for the survival of subordinate competitors in this ant–plant system.

Association between the African lycaenid,Anthene usamba, and an obligate acacia ant,Crematogaster mimosae

The African lycaenid butterfly, Anthene usamba, is an obligate myrmecophile of the acacia ant, Crematogaster mimosae. Female butterflies use the presence of C. mimosae as an oviposition cue. The eggs are laid on the foliage and young branches of the host plant, Acacia drepanolobium. Larvae shelter in the swollen thorns (domatia) of the host tree, where they live in close association with the acacia ants, and each larva occupies a domatium singly. Anthene usamba are tended by ants that feed from the dorsal nectary organ at regular intervals. Larvae also possess tentacle organs flanking the dorsal nectary organ and appear to signal to ants by everting these structures. Larvae were observed to spend most of their time within the domatia. Stable isotope analysis of matched host plant‐ant‐butterfly samples revealed that Anthene usamba are d 15 N enriched relative to the ants with which they associate. These data, based on the increase in d 15 N through trophic levels, indicate that the caterpillars of these butterflies are aphytophagous and either exploit the ant brood of C. mimosae within the domatia, or are fed mouth to mouth by adult workers via trophallaxis. This is the first documented case of aphytophagy in African Anthene. Pupation occurs inside the domatium and the imago emerges and departs via the hole chewed by the larva. The adult females remain closely associated with their natal patch of trees, whereas males disperse more widely across the acacia savannah. Females prefer to oviposit on trees with the specific host ant, C. mimosae, an aggressive obligate mutualist, and avoid neighbouring trees with other ant species. Adult butterflies are active during most months of the year, and there are at least two to three generations each year. Observations made over a 5-year period indicate that a number of different lycaenid species utilize ant-acacias in East Africa, and these observations are summarized, together with comparisons from the literature. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109, 302‐312. ADDITIONAL KEYWORDS: Acacia drepanolobium ‐ mutualism ‐ Myrmicinae ‐ parasitism ‐ Polyommatinae ‐ Kenya.

Enough is enough: the effects of symbiotic ant abundance on herbivory, growth, and reproduction in an African acacia

Understanding how cooperative interactions evolve and persist remains a central challenge in biology. Many mutualisms are thought to be maintained by "partner fidelity feedback," in which each partner bases their investment on the benefits they receive. Yet, we know little about how benefits change as mutualists vary their investment, which is critical to understanding the balance between mutualism and antagonism in any given partnership. Using an obligate ant-plant mutualism, we manipulated the density of symbiotic acacia ants (Crematogaster mimosae) and examined how the costs and benefits to Acacia drepanolobium trees scaled with ant abundance. Benefits of ants to plants saturated with increasing ant abundance for protection from branch browsing by elephants and attack by branch galling midges, while varying linearly for protection from cerambycid beetles. In addition, the risk of catastrophic whole-tree herbivory by elephants was highest for trees with very low ant abundance. However, there was no relationship between ant abundance and herbivory by leaf-feeding invertebrates, nor by vertebrate browsers such as giraffe, steinbuck, and Grant's gazelle. Ant abundance did not significantly influence rates of branch growth on acacias, but there was a significant negative relationship between ant abundance and the number of fruits produced by host plants, suggesting that maintaining high-density ant colonies is costly. Because benefits to plants largely saturated with increasing colony size, while costs to plant reproduction increased, we suggest that ant colonies may achieve abundances that are higher than optimal for host plants. Our results highlight the conflicts of interest inherent in many mutualisms, and demonstrate the value of examining the shape of curves relating costs and benefits within these globally important interactions.

Polygyny in the nest-site limited acacia-ant Crematogaster mimosae

Polygyny is common in social insects despite inevitable decreases in nestmate relatedness and reductions to the inclusive fitness returns for cooperating non-reproductive individuals. We studied the prevalence and mode of polygyny in the African acacia-ant Crematogaster mimosae. These ants compete intensively with neighboring colonies of conspecifics and with three sympatric ant species for resources associated with the whistling-thorn acacias in which they all obligately nest. We used the genotypes of alate males at ten microsatellite loci to reconstruct queen genotypes and found that C. mimosae colonies are frequently secondarily polygynous, in that they include multiple closely related (and sometimes full-sib) queens, and (more rarely) unrelated queens. We also found that individual queens in both monogynous and polygynous colonies had mated with multiple males, making C. mimosae an interesting example of simultaneous polygyny and polyandry. The presence of polygyny in C. mimosae and the intense competition for nest-sites between C. mimosae and its conspecifics support the association between nest-site limitation and polygyny. Polygyny may allow for increased worker populations and a competitive advantage, as inter-colony conflicts are typically won by the colony with the larger number of workers.

Nutritional benefits ofcrematogaster mimosaeants andacacia drepanolobiumgum for patas monkeys and vervets in laikipia, Kenya

Patas monkeys (Erythrocebus patas) are midsized primates that feed extensively on the gum of Acacia drepanolobium and the ants are housed in swollen thorns of this Acacia. Their diet resembles that expected more of smaller bodied primates. Patas monkeys are also more like smaller bodied primates in reproducing at high rates. We sought to better understand the convergence of patas monkeys with smaller bodied primates by comparing their feeding behavior on ants and gum with that of closely related, sympatric vervets (Chlorocebus pygerythrus), and analyzing the nutrient content of the gum of A. drepanolobium and of Crematogaster mimosae, the most common ant species eaten by patas monkeys in Laikipia, Kenya. All occurrences of feeding and moving during focal animal sampling revealed that 1) patas monkeys seek A. drepanolobium gum but vervets avoid it; 2) both species open swollen thorns most often in the morning when antsare less active; 3) patas monkeys continually feed onswollen thorns and gum while moving quickly throughout the day, whereas vervets reduce their consumption of these items and their travel rate at mid-day, and; 4) vervets eat young swollen thorns at a higher rate than patas monkeys. Patas monkeys are able to spend little time acquiring substantial amounts of energy, protein, and minerals from A. drepanolobium gum and C. mimosae ants each day. These findings, when coupled with evidence of causes of infant and adult female mortality, suggest that reproductive success of female patas monkeys is more immediately affected by illness, disease, interactions between adults and infants, and access to water than by food.

Not all ants are equal: obligate acacia ants provide different levels of protection against mega-herbivores

AbstractIn obligate ant–plant mutualisms, the asymmetric engagement of a single plant species with multiple ant species provides the opportunity for partners to vary in their behaviour. Variation in behaviour has implications for the interactions with third‐party species such as herbivores. This study assessed the effect of obligate ant‐mutualists (Crematogaster mimosae, Crematogaster nigriceps and Tetraponera penzigi) inhabiting the African ant‐acacia (Acacia drepanolobium) on three mega‐herbivore browsers: the Maasai giraffe (Giraffa camelopardalis tippelskirchi), the reticulated giraffe (Giraffa c. reticulata) and the black rhino (Diceros bicornis). Giraffes are abundant and wide‐ranging herbivores of the acacias, whereas black rhinos are localized and perennial herbivores of the acacias. Multiyear field studies comparing the ants’ aggressive behaviour and browsing by mega‐herbivores suggested differences between the tending abilities of the primary ant species inhabiting A. drepanolobium. Trees occupied by the aggressive ant species C. mimosae had significantly less browsing by giraffes and black rhino than trees occupied by other ant species. The results of this study provide evidence that ant‐mutualists on African acacias can serve as deterrents to mega‐herbivores and that different ant species vary in their tending abilities.

Isolation and characterization of microsatellite markers from the acacia‐ant Crematogaster mimosae

We describe 10 microsatellite loci developed from Crematogaster mimosae, an ant species that nests mutualistically in Acacia drepanolobium trees in east Africa. Polymorphism ranged from 4 to 16 alleles per locus (mean=7.3). Observed and expected heterozygosities ranged from 0.485 to 0.813 (mean 0.626), and from 0.502 to 0.894 (mean 0.674), respectively. These markers will foster studies of the population structure, colony structure, and reproductive strategies of these ants.