Mutualistic Systems Research Articles

Spatial structure of ant-gardens: vertical distribution on host trees and succession/segregation of associated vascular epiphytes

Questions Ant-gardens (AGs) involve a close association between epiphytes and ants with concurrent mutualistic interactions including protection, dispersal and nutrition; however, little is known about the spatial structure patterns that determine their establishment and formation. Our main questions were: 1) Do the AGs have a particular pattern of vertical distribution on their host trees? 2) Does a process of succession of epiphytes occur during the development of AGs? 3) Are epiphytes segregated in AGs? Location An anthropic landscape in southeastern Mexico. Methods We studied AGs built by Azteca gnava ants. We examined their vertical distribution on host trees as well as the diversity, composition and reproductive status of vascular epiphytes associated with the lower, medium and upper zones of small, medium and large AGs. Results A total of 859 AGs and 10,871 epiphytes, belonging to 26 different species, were recorded. We found that AGs are primarily (75%) located within tree crowns, and that the diversity and composition of epiphytes vary among AG sizes and among AG zones. We infer that the epiphytes that first become established in AGs are the bromeliad Aechmea tillandsioides and the gesneriad Codonanthe uleana, followed by the orchid Epidendrum flexuosum and the cactus Epiphyllum phyllanthus; these species were recorded, either individually or in co-occurrence, in 74% of the AGs examined. The species Ae. tillandsioides, Coryanthes picturata and Epid. flexuosum were most frequent in the upper AG zone, while Epidendrum pachyrachis was most frequent in the medium AG zone. Conclusions Our results show that AGs have distinct vertical distribution patterns on their tree hosts and that the establishment of epiphytes in AGs is successive and segregated, suggesting a spatial and temporal optimization in the establishment and development of these complex mutualistic systems. This article is protected by copyright. All rights reserved.

Nutrient recycling facilitates long-term stability of marine microbial phototroph-heterotroph interactions.

Biological interactions underpin the functioning of marine ecosystems, be it via competition, predation, mutualism, or symbiosis processes. Microbial phototroph-heterotroph interactions propel the engine that results in the biogeochemical cycling of individual elements and are critical for understanding and modelling global ocean processes. Unfortunately, studies thus far have focused on exponentially-growing cultures in nutrient-rich media, meaning knowledge of such interactions under in situ conditions is rudimentary at best. Here, we performed long-term phototroph-heterotroph co-culture experiments under nutrient-amended and natural seawater conditions which showed that it is not the concentration of nutrients but rather their circulation that maintains a stable interaction and a dynamic system. Using the Synechococcus-Roseobacter interaction as a model phototroph-heterotroph case study we show that whilst Synechococcus is highly specialised for carrying out photosynthesis and carbon-fixation it relies on the heterotroph to re-mineralise the inevitably leaked organic matter making nutrients circulate in a mutualistic system. In this sense we challenge the general belief that marine phototrophs and heterotrophs compete for the same scarce nutrients and niche space, but instead suggest these organisms more likely benefit from each other because of their different levels of specialization and complementarity within long-term stable-state systems.

The potential indirect effects among plants via shared hummingbird pollinators are structured by phenotypic similarity.

Plant species within communities may overlap in pollinators' use and influence visitation patterns of shared pollinators, potentially engaging in indirect interactions (e.g., facilitation or competition). While several studies have explored the mechanisms regulating insect-pollination networks, there is a lack of studies on bird-pollination systems, particularly in species-rich tropical areas. Here, we evaluated if phenotypic similarity, resource availability (floral abundance), evolutionary relatedness and flowering phenology affect the potential for indirect effects via shared pollinators in hummingbird-pollinated plant species within four communities in the Brazilian Atlantic forest. Among the evaluated factors, phenotypic similarity (corolla length and anther height) was the most important variable, while resource availability (floral abundance) had a secondary importance. On the other hand, evolutionary relatedness and flowering phenology were less important, which altogether highlights the relevance of convergent evolution and that the contribution of a plant to the diet of the pollinators of another plant is independent of the level of temporal overlap in flowering in this tropical system. Interestingly, our findings contrast with results from multiple insect-pollinated plant communities, mostly from temperate regions, in which floral abundance was the most important driver, followed by evolutionary relatedness and phenotypic similarity. We propose that these contrasting results are due to high level of specialization inherent to tropical hummingbird-pollination systems. Moreover, our results demonstrated that factors defining linkage rules of plant-hummingbird networks also determinate plant-plant potential indirect effects. Future studies are needed to test if these findings can be generalized to other highly specialized systems. Overall, our results have important implications for the understanding of ecological processes due resource sharing in mutualistic systems.

Mutualistic strategies minimize coextinction in plant-disperser networks.

The global decline of mutualists such as pollinators and seed dispersers may cause negative direct and indirect impacts on biodiversity. Mutualistic network models used to understand the stability of mutualistic systems indicate that species with low partner diversity are most vulnerable to coextinction following mutualism disruption. However, existing models have not considered how species vary in their dependence on mutualistic interactions for reproduction or survival, overlooking the potential influence of this variation on species' coextinction vulnerability and on network stability. Using global databases and field experiments focused on the seed dispersal mutualism, we found that plants and animals that depend heavily on mutualistic interactions have higher partner diversity. Under simulated network disruption, this empirical relationship strongly reduced coextinction because the species most likely to lose mutualists depend least on their mutualists. The pattern also reduced the importance of network structure for stability; nested network structure had little effect on coextinction after simulations incorporated the empirically derived relationship between partner diversity and mutualistic dependence. Our results highlight a previously unknown source of stability in mutualistic networks and suggest that differences among species in their mutualistic strategy, rather than network structure, primarily accounts for stability in mutualistic communities.

Feasibility and coexistence of large ecological communities

The role of species interactions in controlling the interplay between the stability of ecosystems and their biodiversity is still not well understood. The ability of ecological communities to recover after small perturbations of the species abundances (local asymptotic stability) has been well studied, whereas the likelihood of a community to persist when the conditions change (structural stability) has received much less attention. Our goal is to understand the effects of diversity, interaction strengths and ecological network structure on the volume of parameter space leading to feasible equilibria. We develop a geometrical framework to study the range of conditions necessary for feasible coexistence. We show that feasibility is determined by few quantities describing the interactions, yielding a nontrivial complexity–feasibility relationship. Analysing more than 100 empirical networks, we show that the range of coexistence conditions in mutualistic systems can be analytically predicted. Finally, we characterize the geometric shape of the feasibility domain, thereby identifying the direction of perturbations that are more likely to cause extinctions.

Mutualism supports biodiversity when the direct competition is weak

A key question of theoretical ecology is which properties of ecosystems favour their stability and help maintaining biodiversity. This question recently reconsidered mutualistic systems, generating intense controversy about the role of mutualistic interactions and their network architecture. Here we show analytically and verify with simulations that reducing the effective interspecific competition and the propagation of perturbations positively influences structural stability against environmental perturbations, enhancing persistence. Noteworthy, mutualism reduces the effective interspecific competition only when the direct interspecific competition is weaker than a critical value. This critical competition is in almost all cases larger in pollinator networks than in random networks with the same connectance. Highly connected mutualistic networks reduce the propagation of environmental perturbations, a mechanism reminiscent of MacArthur’s proposal that ecosystem complexity enhances stability. Our analytic framework rationalizes previous contradictory results, and it gives valuable insight on the complex relationship between mutualism and biodiversity.

Evolutionary flexibility in five hummingbird/plant mutualistic systems: testing temporal and geographic matching

AbstractAimPartners in co‐evolutionary interactions must be ecologically interdependent and at least at some stage have matching traits and more or less overlapping ranges. As co‐evolution is a process, neither the mutual dependence nor the trait and range matching are expected to be static or perfect. Here we investigate the extent of evolutionary flexibility in tight pollination mutualisms between hummingbirds and plants, ranging from straight‐billed species to sicklebills.LocationThe Americas.MethodsThe five considered pollination mutualisms are between the following hummingbird and plant species: Calypte anna and Ribes speciosum (Grossulariaceae); Basilinna xantusii and Arbutus peninsularis (Ericaceae); two species of Sephanoides and Tristerix aphyllus/corymbosus (Loranthaceae); two species of Eutoxeres and 34 species of curved‐corolla Centropogon (Campanulaceae); and six species of Oreotrochilus and seven species of Chuquiraga (Asteraceae). While ecological interdependence and trait matching in these mutualisms are well established, geographic occurrence data and molecular clock‐based ages for the 10 clades were newly compiled.ResultsWe found matching bird and plant stem ages in two of the five systems and (much) older bird than plant ages in the other three. The implied adaptation of plant populations to already existing hummingbird species fits with the modelled distributions. In three of the systems, the ranges of the plants overlap those of their pollinators by > 90%; conversely, the range overlap between the bird species and the plant species they pollinate is much less than that. Surprisingly, the age mismatch was greatest in the Eutoxeres/Centropogon system, in spite of the perfect morphological fit among bills and corollas, illustrating the evolutionary flexibility of these mutualisms and the apparently rapid ‘addition’ of further plant species.Main conclusionsThese findings illuminate the macroevolutionary assembly of hummingbird/plant mutualisms, which has been highly dynamic, even in specialized systems with perfect morphological trait fitting.

“Savor the earth to save it!”—The pedagogy of sustainable pleasure and relational ecology in a place-based public culinary culture

ABSTRACTSustainability has become a keyword in popular discourses in the age of the celebrity chef. As such, chefs and other actors working in the visible spaces and venues of a shared US public culinary culture have become powerful spokespersons for sustainable food production, consumption, and localization. Unlike catastrophist discourses of environmentalisms' of the past, however, this new discourse is often framed in terms of a politics of pleasure that redefines deliberate and considered hedonism as a kind of transformative eco-culinary engagement. In self-assigned missionary roles, chefs and other prepared food producers are often engaging in a very deliberate pedagogical project that link sensuality and sustainability. Likewise, and equally important to these efforts, is the centrality of regard—that is, attempts among chefs to re-embed exchange relations between producers and consumers, often serving as the critical interlocutors in such reassertions. This article is an exploration of how such processes have played out in the public culinary context of Knoxville, Tennessee and vicinity. As a mid-size city in the heart of southern Appalachia's Ridge and Valley sub-region, Knoxville is undergoing a familiar process of urban revitalization that includes a robust food service sector. Amid shifting demographics and media flows bringing more cosmopolitan influences to the region, a range of actors have grounded these in a regionally specific food and farming heritage in order to reconnect consumers and producers and cultivate a more sustainable and mutualistic local food system.

On stochastic multi-group Lotka-Volterra ecosystems with regime switching

Focusing on stochastic dynamics involving continuous states as well as discrete events, this paper investigates dynamical behaviors of stochastic multi-group Lotka-Volterra model with regime switching. The contributions of the paper lie on: (a) giving the sufficient conditions of stochastic permanence for generic stochastic multi-group Lotka-Volterra model, which are much weaker than the existing results in the literature; (b) obtaining the stochastic strong permanence and ergodic property for the mutualistic systems; (c) establishing the almost surely asymptotic estimate of solutions. These can specify some realistic recurring phenomena and reveal the fact that regime switching can suppress the impermanence. A couple of examples and numerical simulations are given to illustrate our results.

Reproduction Expanded: Multigenerational and Multilineal Units of Evolution

Reproduction is central to biology and evolution. Standard concepts of reproduction are drawn from animals. Nonstandard examples of reproduction can be found in unicellular eukaryotes that distribute their reproductive strategies across multiple generations, and in mutualistic systems that combine different modes of reproduction across multiple lineages. Examining multigenerational and multilineal reproducers and how they align fitness has implications for conceptualizing units of evolution.

Effective competition determines the global stability of model ecosystems

We investigate the stability of Lotka-Volterra (LV) models constituted by two groups of species such as plants and animals in terms of the intragroup effective competition matrix, which allows separating the equilibrium equations of the two groups. In matrix analysis, the effective competition matrix represents the Schur complement of the species interaction matrix. It has been previously shown that the main eigenvalue of this effective competition matrix strongly influences the structural stability of the model ecosystem. Here, we show that the spectral properties of the effective competition matrix also strongly influence the dynamical stability of the model ecosystem. In particular, a necessary condition for diagonal stability of the full system, which guarantees global stability, is that the effective competition matrix is diagonally stable, which means that intergroup interactions must be weaker than intra-group competition in appropriate units. For mutualistic or competitive interactions, diagonal stability of the effective competition is a sufficient condition for global stability if the inter-group interactions are suitably correlated, in the sense that the biomass that each species provides to (removes from) the other group must be proportional to the biomass that it receives from (is removed by) it. For a non-LV mutualistic system with saturating interactions, we show that the diagonal stability of the corresponding LV system close to the fixed point is a sufficient condition for global stability.

Host sanctions in Panamanian Ficus are likely based on selective resource allocation.

Fig trees and their pollinators, fig wasps, present a powerful model system for studying mutualism stability: both partners depend on each other for reproduction, cooperation levels can be manipulated, and the resulting field-based fitness quantified. Previous work has shown that fig trees can severely reduce the fitness of wasps that do not pollinate by aborting unpollinated figs or reducing the number and size of wasp offspring. Here we evaluated four hypotheses regarding the mechanism of sanctions in four Panamanian fig species. We examined wasp and fig samples from field experiments with manipulated levels of pollination. In unpollinated figs, the fig wall and the wasp offspring had a lower dry mass. Unpollinated figs had as many initiated wasp galls as pollinated figs but fewer galls that successfully produced live wasp offspring. Across three experimentally increasing levels of pollination, we found nonlinear increases in fig wall mass, the proportion of wasp galls that develop, and wasp mass. Our data did not support the hypotheses that lack of pollination prevents gall formation or that fertilized endosperm is required for wasp development. While our data are potentially consistent with the hypothesis that trees produce a wasp-specific toxin in response to lack of pollination, we found the hypothesis that sanctions are a consequence of trees allocating more resources to better-pollinated figs more parsimonious with the aggregate data. Our findings are completely analogous to the selective resource allocation to more beneficial tissues documented in other mutualistic systems.

The Metronome of Symbiosis: Interactions Between Microbes and the Host Circadian Clock.

The entrainment of circadian rhythms, physiological cycles with a period of about 24 h, is regulated by a variety of mechanisms, including nonvisual photoreception. While circadian rhythms have been shown to be integral to many processes in multicellular organisms, including immune regulation, the effect of circadian rhythms on symbiosis, or host-microbe interactions, has only recently begun to be studied. This review summarizes recent work in the interactions of both pathogenic and mutualistic associations with host and symbiont circadian rhythms, focusing specifically on three mutualistic systems in which this phenomenon has been best studied. One important theme taken from these studies is the fact that mutualisms are profoundly affected by the circadian rhythms of the host, but that the microbial symbionts in these associations can, in turn, manipulate host rhythms. The interplay between circadian rhythms and symbiosis is a promising new field with effects that should be kept in mind when designing future studies across biology.

Asymptotic Behavior of Solution of a Periodic Mutualistic System

Asymptotic Behavior of Solution of a Periodic Mutualistic System

Competition for foundation patronage and the differential effects of prestige on the grant market success of social movement organisations

Extant models of the financial patronage of Social Movement Organisations (SMOs) by private foundations exclusively use population density to account for competition. However, density fails to reveal how SMOs win grants whilst neglecting the strategic decision-making of foundation-investors. Here I recast patronage as a mutualistic network represented by a dynamic bipartite graph wherein SMOs and foundations cooperate across class whilst SMOs compete within class for financial support. A SMO's competitiveness rests with its position in a network-based prestige hierarchy and a foundation's propensity to invest is mediated by its structural position within the grant market. While previous research has predicted a positive monotonic relationship between status and patronage, using Stochastic Actor-Oriented Models I find a tendency for status-based disassortativity in the mutualistic system such that high-status foundations prefer to invest in low-status SMOs. I attribute this counterintuitive finding to foundations’ preferences for grantees that can innovate around social problems. Relative to their peripheral counterparts, well-funded SMOs may suffer a rigidity of goals due to the risk of alienating an existing support-base through organisational change. Data consist of 3261 grants given from 2003 to 2007 by 136 private foundations to 66 professional SMOs with nonprofit status loosely mobilised against the notion of anthropogenic climate change.

Coevolutionary dynamics in one-to-many mutualistic systems

“One-to-many” mutualisms are often observed in nature. In this type of mutualism, each host individual can interact with many symbionts, whereas each individual symbiont can interact with only one host individual. Partner choice by the host is a potentially critical mechanism for maintaining such systems; however, its long-term effects on the coevolution between the hosts and symbionts have not been completely explored. In this study, I developed a simple mathematical model to describe the coevolutionary dynamics between hosts and symbionts in a one-to-many mutualism. I assumed that each host chooses a constant number of symbionts from a potential symbiont population, a fraction of which are chosen through preferential choice on the basis of the cooperativeness of the symbionts and the rest are chosen randomly. Using numerical calculations, I found that mutualism is maintained when the preferential choice is not very costly and the mutation rate of symbionts is large. I also found that symbionts that receive benefits from hosts without a return (cheater symbionts) and hosts that do not engage in preferential partner choice (indiscriminator hosts) can coexist with mutualist symbionts and discriminator hosts, respectively. The parameter domain of pure mutualism, i.e., free from cheater symbionts and indiscriminator hosts, can be narrower than the whole domain where the mutualism persists.

Lack of genetic isolation by distance, similar genetic structuring but different demographic histories in a fig-pollinating wasp mutualism.

Historical abiotic factors such as climatic oscillations and extreme climatic events as well as biotic factors have shaped the structuring of species' genetic diversity. In obligate species-specific mutualisms, the biogeographic histories of the interacting species are tightly linked. This could be particularly true for nuclear genes in the Ficus-pollinating wasp mutualistic association as the insects disperse pollen from their natal tree. In this study, we compare spatial genetic structure of plant and pollinator for the Ficus hirta-Valisia javana association throughout southeast China including Hainan Island, for both nuclear and cytoplasmic markers. We show that dispersal of the insect leads to plant and insect presenting similar signatures of lack of genetic isolation by distance for nuclear genes on the continent over a distance of 1000 km. But we also show that the demographic histories of plant and insect are strikingly different. This is in agreement with extreme climatic events leading to transient regional extinctions of the insects, associated with local survival of the plants. We also observe evidence of genetic differentiation for both wasps and fig-tree between the continent and Hainan Island, although the Qiongzhou Strait is only on average 30 km wide, suggesting that geographic isolation by itself has not been sufficient to generate this differentiation. Hence, our results suggest that in highly dispersive mutualistic systems, isolation-by-dispersal limitation across a geographic barrier could be supplemented by isolation by adaptation, and maybe by coevolution, allowing further genetic divergence. In such systems, species may frequently be composed of a single population.

Macroevolutionary assembly of ant/plant symbioses: Pseudomyrmex ants and their ant-housing plants in the Neotropics.

Symbioses include some of the clearest cases of coevolution, but their origin, loss or reassembly with different partners can rarely be inferred. Here we use ant/plant symbioses involving three plant clades to investigate the evolution of symbioses. We generated phylogenies for the big-eyed arboreal ants (Pseudomyrmecinae), including 72% of their 286 species, as well as for five of their plant host groups, in each case sampling more than 61% of the species. We show that the ant-housing Vachellia (Mimosoideae) clade and its ants co-diversified for the past 5 Ma, with some species additionally colonized by younger plant-nesting ant species, some parasitic. An apparent co-radiation of ants and Tachigali (Caesalpinioideae) was followed by waves of colonization by the same ant clade, and subsequent occupation by a younger ant group. Wide crown and stem age differences between the ant-housing genus Triplaris (Polygonaceae) and its obligate ant inhabitants, and stochastic trait mapping, indicate that its domatium evolved earlier than the ants now occupying it, suggesting previous symbioses that dissolved. Parasitic ant species evolved from generalists, not from mutualists, and are younger than the mutualistic systems they parasitize. Our study illuminates the macroevolutionary assembly of ant/plant symbioses, which has been highly dynamic, even in very specialized systems.

The macroecology of phylogenetically structured hummingbird–plant networks

AbstractAimTo investigate the association between hummingbird–plant network structure and species richness, phylogenetic signal on species' interaction pattern, insularity and historical and current climate.LocationFifty‐four communities along a c. 10,000 km latitudinal gradient across the Americas (39° N–32° S), ranging from sea level to c. 3700 m a.s.l., located on the mainland and on islands and covering a wide range of climate regimes.MethodsWe measured the level of specialization and modularity in mutualistic plant–hummingbird interaction networks. Using an ordinary least squares multimodel approach, we examined the influence of species richness, phylogenetic signal, insularity and current and historical climate conditions on network structure (null‐model‐corrected specialization and modularity).ResultsPhylogenetically related species, especially plants, showed a tendency to interact with a similar array of mutualistic partners. The spatial variation in network structure exhibited a constant association with species phylogeny (R2 = 0.18–0.19); however, network structure showed the strongest association with species richness and environmental factors (R2 = 0.20–0.44 and R2 = 0.32–0.45, respectively). Specifically, higher levels of specialization and modularity were associated with species‐rich communities and communities in which closely related hummingbirds visited distinct sets of flowering species. On the mainland, specialization was also associated with warmer temperatures and greater historical temperature stability.Main conclusionsOur results confirm the results of previous macroecological studies of interaction networks which have highlighted the importance of species richness and the environment in determining network structure. Additionally, for the first time, we report an association between network structure and species phylogenetic signal at a macroecological scale, indicating that high specialization and modularity are associated with high interspecific competition among closely related hummingbirds, subdividing the floral niche. This suggests a tighter co‐evolutionary association between hummingbirds and their plants than in previously studied plant–bird mutualistic systems.

Scale‐dependent responses of pollination and seed dispersal mutualisms in a habitat transformation scenario

Summary Transformed habitats are the result of deliberate replacement of native species by an exotic monoculture, involving changes in biotic and abiotic conditions. Despite the fact that transformed habitats are becoming more common and constitute a major biodiversity change driver, little is known about the scale‐dependent responses of plant–animal mutualisms. Aiming to test the multiscale responses of pollination and seed dispersal in a habitat transformation scenario, we examined a gradient of native and transformed habitats at three spatial scales (0–50, 50–100 and 100–250 m) and focused on a highly specialized mutualistic system composed of a hemiparasitic mistletoe (Tristerix corymbosus) that is almost exclusively pollinated by a hummingbird (Sephanoides sephaniodes) and dispersed by an arboreal marsupial (Dromiciops gliroides). Even though mistletoes were found along the gradient, they were more abundant and more densely aggregated when the transformed habitat was dominant. Disperser and pollinator activity also increased as the transformed habitat becomes dominant, at the scale of 0–50 and 50–100 m, respectively. Furthermore, crop size and disperser activity covaried at broad and intermediate scales, whereas recruitment covaried at intermediate and fine scales. Moreover, disperser activity and the number of seedlings were spatially associated, stressing D. gliroides’ role in the recruitment of the mistletoe. Synthesis. This highly specialized mutualistic system seems to be responding positively to the habitat structure modifications associated with Eucalyptus plantations. However, the actual costs (e.g. reduced gene flow, increased herbivory) in these transformed habitats are yet to be assessed.