Predators Exacerbate Competitive Interactions and Dominance Hierarchies between Two Coral Reef Fishes

Predation and competition are critical processes influencing the ecology of organisms, and can play an integral role in shaping coral reef fish communities. This study compared the relative and interacting effects of competition and predation on two competing species of coral reef fish, Pomacentrus amboinensis and P. moluccensis (Pomacentridae), using a multifactorial experiment. Fish were subjected to the sight and smell of a known predator (Pseudochromis fuscus), the presence of the heterospecific competitor (i.e., P. amboinensis vs. P. moluccensis), or a combination of the two for a period of 19 days. The sub-lethal effects of predator/competitor treatments were compared with controls; a combination of otolith microstructure analysis and observations were used to determine otolith growth patterns and behaviour. We predicted that the stress of competition and/or predation would result in strong sub-lethal impacts, and act synergistically on growth and behavioural patterns. We found strong evidence to support this prediction, but only for P. amboinensis, which suffered reductions in growth in both predator and competitor treatments, with the largest reductions occurring when subjected to both predation and competition concurrently. There was strong evidence of asymmetrical competition between the two damselfish species, with P. moluccensis as the dominant competitor, displaying strong aggressive behaviour towards P. amboinensis. Growth reductions for P. amboinensis in predator/competitor treatments appeared to come about primarily due to increases in shelter seeking behaviour, which significantly reduced the foraging rates of individuals compared with controls. These data highlight the importance of predator/competitor synergisms in influencing key behaviours and demographic parameters for juvenile coral reef fishes.     

Differences in Aggressive Behaviors between Two Ant Species Determine the Ecological Consequences of a Facultative Food-for-Protection Mutualism

Ant-hemipteran mutualisms are widespread interactions in terrestrial food webs with far-reaching consequences for arthropod communities. Several hypotheses address the behavioral mechanisms driving the impacts of this mutualism, but relatively few studies have considered multiple ant species simultaneously as well as interspecific and intraspecific variation in ant behavior. In a series of field experiments that manipulated ant diet, this work examines the role of induced behaviors of forest ant species actively engaged in mutualism with Hemiptera. Based on other work in ant mutualisms, we predicted a higher frequency of aggressive behaviors towards prey and competitors by ants in the presence of honeydew-producing Hemiptera. We specifically compared Camponotus chromaoides and Formica neogagates (Formicidae), two abundant species in temperate forests of the northeastern U.S.A. After manipulating ant diet and interactions with sap-feeders experimentally, we observed 494 one-on-one interactions between ants and competitors, ladybird beetles and caterpillar prey. We found that C. chromaoides, exhibited behavioral dominance over F. neogagates, and C. chromaoides was more likely to attack ladybird beetles, competing ants, and caterpillar prey. However, contrary to other work in ant-Hemipteran mutualisms, we observed no evidence that food rewards provided by sap-feeders induced changes in ant behavior for either ant species examined. These results reveal the importance of considering interspecific differences in behavior as a mechanism underlying the ecological impacts of ant-Hemipteran protection mutualisms.     

A Novel Filtering Mutualism between a Sponge Host and Its Endosymbiotic Bivalves

Sponges, porous filter-feeding organisms consisting of vast canal systems, provide unique substrates for diverse symbiotic organisms. The Spongia (Spongia) sp. massive sponge is obligately inhabited by the host-specific endosymbiotic bivalve Vulsella vulsella, which benefits from this symbiosis by receiving protection from predators. However, whether the host sponge gains any benefit from this association is unclear. Considering that the bivalves exhale filtered water into the sponge body rather than the ambient environment, the sponge is hypothesized to utilize water exhaled by the bivalves to circulate water around its body more efficiently. We tested this hypothesis by observing the sponge aquiferous structure and comparing the pumping rates of sponges and bivalves. Observations of water currents and the sponge aquiferous structure revealed that the sponge had a unique canal system enabling it to inhale water exhaled from bivalves, indicating that the host sponge adapted morphologically to receive water from the bivalves. In addition, the volume of water circulating in the sponge body was dramatically increased by the water exhaled from bivalves. Therefore, this sponge-bivalve association can be regarded as a novel mutualism in which two filter-feeding symbionts promote mutual filtering rates. This symbiotic association should be called a “filtering mutualism”.     

Mutualism fails when climate response differs between interacting species

Successful species interactions require that both partners share a similar cue. For many species, spring warming acts as a shared signal to synchronize mutualist behaviors. Spring flowering plants and the ants that disperse their seeds respond to warming temperatures so that ants forage when plants drop seeds. However, where warm‐adapted ants replace cold‐adapted ants, changes in this timing might leave early seeds stranded without a disperser. We investigate plant seed dispersal south and north of a distinct boundary between warm‐ and cold‐adapted ants to determine if changes in the ant species influence local plant dispersal. The warm‐adapted ants forage much later than the cold‐adapted ants, and so we first assess natural populations of early and late blooming plants. We then transplant these plants south and north of the ant boundary to test whether distinct ant climate requirements disrupt the ant–plant mutualism. Whereas the early blooming plant's inability to synchronize with the warm‐adapted ant leaves its populations clumped and patchy and its seedlings clustered around the parents in natural populations, when transplanted into the range of the cold‐adapted ant, effective seed dispersal recovers. In contrast, the mutualism persists for the later blooming plant regardless of location because it sets seed later in spring when both warm‐ and cold‐adapted ant species forage, resulting in effective seed dispersal. These results indicate that the climate response of species interactions, not just the species themselves, is integral in understanding ecological responses to a changing climate. Data linking phenological synchrony and dispersal are rare, and these results suggest a viable mechanism by which a species' range is limited more by biotic than abiotic interactions – despite the general assumption that biotic influences are buried within larger climate drivers. These results show that biotic partner can be as fundamental a niche requirement as abiotic resources.     

Rex-Centric Mutualism

We asked whether Rex exclusion encoded by a lambda prophage confers a protective or a cell-killing phenotype. We found that the Rex system can channel lysogenic cells into an arrested growth phase that gives an overall protective ability to the host despite some associated killing.     

Symbiont Interactions in a Tripartite Mutualism: Exploring the Presence and Impact of Antagonism between Two Fungus-Growing Ant Mutualists

Mutualistic associations are shaped by the interplay of cooperation and conflict among the partners involved, and it is becoming increasingly clear that within many mutualisms multiple partners simultaneously engage in beneficial interactions. Consequently, a more complete understanding of the dynamics within multipartite mutualism communities is essential for understanding the origin, specificity, and stability of mutualisms. Fungus-growing ants cultivate fungi for food and maintain antibiotic-producing Pseudonocardia actinobacteria on their cuticle that help defend the cultivar fungus from specialized parasites. Within both ant-fungus and ant-bacterium mutualisms, mixing of genetically distinct strains can lead to antagonistic interactions (i.e., competitive conflict), which may prevent the ants from rearing multiple strains of either of the mutualistic symbionts within individual colonies. The success of different ant-cultivar-bacterium combinations could ultimately be governed by antagonistic interactions between the two mutualists, either as inhibition of the cultivar by Pseudonocardia or vice versa. Here we explore cultivar-Pseudonocardia antagonism by evaluating in vitro interactions between strains of the two mutualists, and find frequent antagonistic interactions both from cultivars towards Pseudonocardia and vice versa. To test whether such in vitro antagonistic interactions affect ant colonies in vivo, we performed sub-colony experiments using species of Acromyrmex leaf-cutting ants. We created novel ant-fungus-bacterium pairings in which there was antagonism from one, both, or neither of the ants'' microbial mutualists, and evaluated the effect of directional antagonism on cultivar biomass and Pseudonocardia abundance on the cuticle of workers within sub-colonies. Despite the presence of frequent in vitro growth suppression between cultivars and Pseudonocardia, antagonism from Pseudonocardia towards the cultivar did not reduce sub-colony fungus garden biomass, nor did cultivar antagonism towards Pseudonocardia reduce bacteria abundance on the cuticle of sub-colony workers. Our findings suggest that inter-mutualist antagonism does not limit what combinations of cultivar and Pseudonocardia strains Acromyrmex fungus-growing ants can maintain within nests.     

Anoxic Conditions Promote Species-Specific Mutualism between Gut Microbes In Silico

The human gut is inhabited by thousands of microbial species, most of which are still uncharacterized. Gut microbes have adapted to each other''s presence as well as to the host and engage in complex cross feeding. Constraint-based modeling has been successfully applied to predicting microbe-microbe interactions, such as commensalism, mutualism, and competition. Here, we apply a constraint-based approach to model pairwise interactions between 11 representative gut microbes. Microbe-microbe interactions were computationally modeled in conjunction with human small intestinal enterocytes, and the microbe pairs were subjected to three diets with various levels of carbohydrate, fat, and protein in normoxic or anoxic environments. Each microbe engaged in species-specific commensal, parasitic, mutualistic, or competitive interactions. For instance, Streptococcus thermophilus efficiently outcompeted microbes with which it was paired, in agreement with the domination of streptococci in the small intestinal microbiota. Under anoxic conditions, the probiotic organism Lactobacillus plantarum displayed mutualistic behavior toward six other species, which, surprisingly, were almost entirely abolished under normoxic conditions. This finding suggests that the anoxic conditions in the large intestine drive mutualistic cross feeding, leading to the evolvement of an ecosystem more complex than that of the small intestinal microbiota. Moreover, we predict that the presence of the small intestinal enterocyte induces competition over host-derived nutrients. The presented framework can readily be expanded to a larger gut microbial community. This modeling approach will be of great value for subsequent studies aiming to predict conditions favoring desirable microbes or suppressing pathogens.     

Mutualism between co-introduced species facilitates invasion and alters plant community structure

Generalized mutualisms are often predicted to be resilient to changes in partner identity. Variation in mutualism-related traits between native and invasive species however, can exacerbate the spread of invasive species (‘invasional meltdown’) if invasive partners strongly interact. Here we show how invasion by a seed-dispersing ant (Myrmica rubra) promotes recruitment of a co-introduced invasive over native ant-dispersed (myrmecochorous) plants. We created experimental communities of invasive (M. rubra) or native ants (Aphaenogaster rudis) and invasive and native plants and measured seed dispersal and plant recruitment. In our mesocosms, and in laboratory and field trials, M. rubra acted as a superior seed disperser relative to the native ant. By contrast, previous studies have found that invasive ants are often poor seed dispersers compared with native ants. Despite belonging to the same behavioural guild, seed-dispersing ants were not functionally redundant. Instead, native and invasive ants had strongly divergent effects on plant communities: the invasive plant dominated in the presence of the invasive ant and the native plants dominated in the presence of the native ant. Community changes were not due to preferences for coevolved partners: variation in functional traits of linked partners drove differences. Here, we show that strongly interacting introduced mutualists can be major drivers of ecological change.     

The Benefits of Mutualism: A Conceptual Framework

There are three general mechanisms by which phenotypic benefits are transferred between unrelated organisms. First, one organism may purloin benefits from another by preying on or parasitizing the other organism. Second, one organism may enjoy benefits that are incidental to or a by-product of the self-serving traits of another organism. Third, an organism may invest in another organism if that investment produces return benefits which outweigh the cost of the investment. Interactions in which both parties gain a net benefit are mutualistic. The three mechanisms by which benefits are transferred between organisms can be combined in pairs to produce six possible kinds of original or 'basal' mutualisms that can arise from an amutualistic state. A review of the literature suggests that most or all interspecific mutualism have origins in three of the six possible kinds of basal mutualism. Each of these three basal mutualisms have byproduct benefits flowing in at least one direction. The transfer of by-product benefits and investment are common to both intra- and interspecific mutualisms, so that some interspecific mutualisms have intraspecific analogs. A basal mutualism may evolve to the point where each party invests in the other, sometimes obscuring the nature of the original interaction along the way. Two prominent models for the evolution of mutualism do not include by-product benefits: Roughgarden's model for the evolution of the damsel-fish anemone mutualism and the 'Tit-for-Tat' model of reciprocity. Using the conceptual framework presented here, including in particular by-product benefits, I have shown how it is possible to construct more parsimonious alternatives to both models.     

叶下珠头细蛾与小果叶下珠互利共生的研究--生物学及系统稳定性

【目的】为了确定小果叶下珠 Phyllanthus microcarpus 与叶下珠头细蛾 Epicephala sp.之间专性互利共生系统稳定性的增强是否主要通过彼此之间相互遏制对方对自身进行过度开采。【方法】通过对小果叶下珠上共生的叶下珠头细蛾形态及生物学的研究,记述了叶下珠头细蛾专性寄生寄主植物时的行为特性及共生双方利益得失。【结果】叶下珠头细蛾在广西一年两代,成虫的羽化数量与寄主植物雌雄花总数峰值变化同步;幼虫对小果叶下珠果实的寄生率为96%,单个果实内幼虫寄生数量＞1,但平均每个果实内被取食的种子为56.9%,叶下珠头细蛾低龄幼虫相对较高的死亡率限制了其对寄主种子的过度取食;果实内种子的适度保留和低龄幼虫的高死亡率是小果叶下珠-叶下珠头细蛾互利共生体系维持稳定的关键因素。【结论】小果叶下珠的表型性状出现了趋异性进化,叶下珠头细蛾与不同表型的小果叶下珠均有互利共生关系。因此,对叶下珠头细蛾形态及生物学进行详细研究有助于深入了解小果叶下珠与头细蛾共生体系物种组成多样性及进化生物学,并为探讨大戟科植物同头细蛾属昆虫协同互利共生多样性形成原因提供依据。     

The Costs of Mutualism

Mutualisms are of central importance in biological systems.Despite growing attention in recent years, however, few conceptualthemes have yet to be identified that span mutualisms differingin natural history. Here I examine the idea that the ecologyand evolution of mutualisms are shaped by diverse costs, notonly by the benefits they confer. This concept helps link mutualismto antagonisms such as herbivory, predation, and parasitism,interactions defined largely by the existence of costs. I firstbriefly review the range of costs associated with mutualisms,then describe how one cost, the consumption of seeds by pollinatoroffspring, was quantified for one fig/pollinator mutualism.I compare this cost to published values for other fig/pollinatormutualisms and for other kinds of pollinating seed parasitemutualisms, notably the yucca/yucca moth interaction. I thendiscuss four issues that fundamentally complicate comparativestudies of the cost of mutualism: problems of knowing how tomeasure the magnitude of any one cost accurately; problems associatedwith using average estimates in the absence of data on sourcesof variation; complications arising from the complex correlatesof costs, such as functional linkages between costs and benefits;and problems that arise from considering the cost of mutualismas a unilateral issue in what is fundamentally a reciprocalinteraction. The rich diversity of as-yet unaddressed questionssurrounding the costs of mutualism may best be investigatedvia detailed studies of individual interactions.     

A single spiral artefact in Arthropod cuticle

Spirals are often seen in sections transverse to the axes of bumped structures in arthropod cuticle. (Sections through arthropod cornea or exocones yield excellent examples.) As arthropod cuticle has a helicoidal architecture (Bouligand, 1965), it might be expected that the spirals are a simple consequence of that structure. According to a symmetry argument, the spirals thus predicted must be double spirals. In contrast, the observed spirals are usually single. We propose that the single spirals result from an interaction between the microtome knife and the cuticle architecture. The direction of knife travel defines an orientation within the cuticle, subverting the symmetry arguments that require double spirals. Bouligand (1972) presented a model for the interaction of the knife with the cuticle. However, we offer arguments and observations which show that Bouligand's model is incorrect. We argue from detailed observations of the single spiral that it is indeed a knifing artifact and that its explanation probably lies within a certain class of models. Two related models based on relative movements of cuticle components are examined via computer techniques.     

Mutualism breakdown in breadfruit domestication

During the process of plant domestication, below-ground communities are rarely considered. Some studies have attempted to understand the changes in root symbionts owing to domestication, but little is known about how it influences mycorrhizal response in domesticated crops. We hypothesized that selection for above-ground traits may also result in decreased mycorrhizal abundance in roots. Breadfruit (Artocarpus sp.) has a long domestication history, with a strong geographical movement of cultivars from west to east across the Melanesian and Polynesian islands. Our results clearly show a decrease in arbuscular mycorrhizas (AMs) along a domestication gradient from wild to recently derived cultivars. We showed that the vesicular and arbuscular colonization rate decreased significantly in more recently derived breadfruit cultivars. In addition, molecular analyses of breadfruit roots indicated that AM fungal species richness also responded along the domestication gradient. These results suggest that human-driven selection for plant cultivars can have unintended effects on below-ground mutualists, with potential impacts on the stress tolerance of crops and long-term food security.     

Mutualism Disruption Threatens Global Plant Biodiversity: A Systematic Review

Background

As global environmental change accelerates, biodiversity losses can disrupt interspecific interactions. Extinctions of mutualist partners can create “widow” species, which may face reduced ecological fitness. Hypothetically, such mutualism disruptions could have cascading effects on biodiversity by causing additional species coextinctions. However, the scope of this problem – the magnitude of biodiversity that may lose mutualist partners and the consequences of these losses – remains unknown.

Methodology/Principal Findings

We conducted a systematic review and synthesis of data from a broad range of sources to estimate the threat posed by vertebrate extinctions to the global biodiversity of vertebrate-dispersed and -pollinated plants. Though enormous research gaps persist, our analysis identified Africa, Asia, the Caribbean, and global oceanic islands as geographic regions at particular risk of disruption of these mutualisms; within these regions, percentages of plant species likely affected range from 2.1–4.5%. Widowed plants are likely to experience reproductive declines of 40–58%, potentially threatening their persistence in the context of other global change stresses.

Conclusions

Our systematic approach demonstrates that thousands of species may be impacted by disruption in one class of mutualisms, but extinctions will likely disrupt other mutualisms, as well. Although uncertainty is high, there is evidence that mutualism disruption directly threatens significant biodiversity in some geographic regions. Conservation measures with explicit focus on mutualistic functions could be necessary to bolster populations of widowed species and maintain ecosystem functions.     

Mutualism and biodiversity in soils

Most soil invertebrates and roots have developed strong interactions with micro-organisms to exploit the organic and mineral resources of soil. Micro-fauna are mainly predators of microorganisms whereas larger organisms interact with micro-organisms through the external rumen or facultative endosymbiotic digestive systems. Mobilisation of nutrient and organic resources through mutualism with soil microflora seems to be all the more efficient as the organisms are large (like e.g., roots, termites or earthworms) and temperature is high. In the humid tropics, part of the existing species richness may have originated from an increased base of resources resulting from the development of mutualistic relationships. Evidence for this process is given for earthworm communities. Consequences for soil function and the species richness of plants and consumers are discussed.     

A Bifurcation Analysis of a Differential Equations Model for Mutualism

We develop from basic principles a two-species differential equations model which exhibits mutualistic population interactions. The model is similar in spirit to a commonly cited model [Dean, A.M., Am. Nat. 121(3), 409–417 (1983)], but corrects problems due to singularities in that model. In addition, we investigate our model in more depth by varying the intrinsic growth rate for each of the species and analyzing the resulting bifurcations in system behavior. We are especially interested in transitions between facultative and obligate mutualism. The model reduces to the familiar Lotka–Volterra model locally, but is more realistic for large populations in the case where mutualist interaction is strong. In particular, our model supports population thresholds necessary for survival in certain cases, but does this without allowing unbounded population growth. Experimental implications are discussed for a lichen population.     

蚂蚁与蚁运植物的互惠共生关系

蚁运植物（myrmecochore)即指种子靠蚂蚁携带散布的植物。在长期的协同进化中,蚂蚁与蚁运植物形成了互惠共生关系。由于蚁运植物种子上附生有蚂蚁喜食的油质体,蚂蚁取食油质体后,将种子丢弃在蚁巢附近,从而使植物得以扩散。蚁运植物广布全世界,但主要分布在澳大利亚和南非。蚂蚁主要搬运草本植物和部分灌木植物的种子。对蚂蚁与蚁运植物互惠共生关系的研究表明：蚂蚁的搬运有利于保护和传播植物种子;蚁巢有利于种子萌发,出苗和建群;蚂蚁的搬运是影响某些温带森林群落结构的重要因素之一;蚂蚁与蚁运植物互惠共生对自然群落的恢复有重要作用。     

Effects of Sublethal Concentrations of Insecticides on the Functional Response of Two Mirid Generalist Predators

The use of agrochemicals particularly pesticides, can hamper the effectiveness of natural enemies, causing disruption in the ecosystem service of biological control. In the current study, the effects of the insecticides thiacloprid and chlorantraniliprole on the functional response curves were assessed for two mirid predator nymphs, Macrolophus pygmaeus Rambur and Nesidiocoris tenuis Reuter. In the absence of insecticides, both predators exhibited a type II functional response when feeding on eggs of the moth Ephestia kuehniella. N. tenuis seems to be a more efficient predator than M. pygmaeus, as model estimated handling time was significantly lower for the former than for the latter. Residual exposure of M. pygmaeus to sublethal concentrations of either insecticide was associated with a change in the asymptote but not the type of the functional response curve. Thiacloprid seems to be the least compatible with M. pygmaeus, as it led to both a significant reduction of the attack rate and an increase in handling time. In contrast, chlorantraniliprole exposure significantly increased the handling time, but not the attack rate of the predator. Residual exposure of N. tenuis to sublethal concentrations of either insecticide did not have a significant effect on the type nor the parameters of the functional response model. The results show that pesticide residues that do not have lethal effects on beneficial arthropods can reduce prey consumption depending on predator species and on likely risks associated with toxicity.