Branchiobdellid annelids and their crayfish hosts: are they engaged in a cleaning symbiosis?

Branchiobdellid annelids and their freshwater crayfish hosts are generally thought to have a commensal relationship. Branchiobdellids of the genus Cambarincola exploit their hosts through a variety of mechanisms; however, an effect of branchiobdellids on crayfish has not been conclusively demonstrated. We investigated whether branchiobdellids positively affect the host crayfish Cambarus chasmodactylus in the New River, North Carolina. In a laboratory experiment, we placed 0, 3, or 6 branchiobdellids on C. chasmodactylus and observed a significant effect of branchiobdellid presence on both growth and mortality of host crayfish; crayfish with branchiobdellids exhibited faster growth and lower mortality with increasing branchiobdellid density. A tracer experiment demonstrated that branchiobdellids feed on items found in the branchial chamber of C. chasmodactylus. We hypothesize that such feeding activity by branchiobdellids reduces fouling of crayfish gills by epibionts and particulate matter and could lead to the reduced mortality and increased growth rates observed in the laboratory experiment. Specifically, Cambarincola may improve the ventilatory and excretory fitness of C. chasmodactylus by cleaning gill filaments. Field data support this hypothesis by demonstrating that branchiobdellids are found disproportionately at sites proximal to the branchial chamber in the New River. This study provides evidence that the relationship between C. chasmodactylus and Cambarincola may be a cleaning symbiosis, at least in environments where gill fouling is a problem for C. chasmodactylus.     

Feather mites on birds: costs of parasitism or conditional outcomes?

Feather mites (suborder Astigmata, superfamilies Analgoidea, Pterolichoidea and Freyaniidae) are among the commonest ectosymbionts of birds. Most researchers have assumed they are parasites, having negative effects on hosts. Here we present evidence that suggests that feather mites may not be parasites. We develop a framework for considering conditional outcomes in these interspecific associations, dealing with different kinds of relationships between symbionts. The non-parasitic status of feather mites is supported by a literature review as well as by preliminary data on mites' food. We illustrate symbiotic relationships with a graphical model showing different scenarios in which hosts' cost-benefit relations are determined by the interactions among their symbionts.     

Prey–predator mutualism in a tritrophic system on a camphor tree

We report the discovery of a mutualistic system encompassing prey–predator interactions. A domatium is a small space in a vein axil on the underside of leaves of woody angiosperms. Cinnamomum camphora Linn. has domatia that harbor a microphytophagous eriophyid mite (sp. 1). We previously reported that a predatory mite, Euseius sojaensis (Ehara), depends on this eriophyid mite as food. We revealed that E. sojaensis also preyed upon another eriophyid mite (sp. 2) that induces galls on leaves, and that the mean area of C. camphora leaves with galls was usually less than half that of leaves without galls. We experimentally tested the effect of E. sojaensis on galls, and confirmed that the presence of E. sojaensis reduced gall induction. Therefore, C. camphora, eriophyid mite sp. 1, and E. sojaensis comprise a mutualistic system, in spite of the prey–predator interactions among them. The conventional concept of mutualism does not apply to such prey–predator interactions, so we defined them as systematic mutualism. Here, the system consists of three trophic levels, and individuals that constitute this system benefit from the other species that constitute this system.     

Microalgae–bacteria symbiosis in microalgal growth and biofuel production: a review

Photosynthetic microalgae can capture solar energy and convert it to bioenergy and biochemical products. In nature or industrial processes, microalgae live together with bacterial communities and may maintain symbiotic relationships. In general interactions, microalgae exude dissolved organic carbon that becomes available to bacteria. In return, the bacteria remineralize sulphur, nitrogen and phosphorous to support the further growth of microalgae. In specific interactions, heterotrophic bacteria supply B vitamins as organic cofactors or produce siderophores to bind iron, which could be utilized by microalgae, while the algae supply fixed carbon to the bacteria in return. In this review, we focus on mutualistic relationship between microalgae and bacteria, summarizing recent studies on the mechanisms involved in microalgae–bacteria symbiosis. Symbiotic bacteria on promoting microalgal growth are described and the relevance of microalgae–bacteria interactions for biofuel production processes is discussed. Symbiotic microalgae–bacteria consortia could be utilized to improve microalgal biomass production and to enrich the biomass with valuable chemical and energy compounds. The suitable control of such biological interactions between microalgae and bacteria will help to improve the microalgae-based biomass and biofuel production in the future.     

Context‐dependent outcomes in a reproductive mutualism between two freshwater fish species

1. The development of encompassing general models of ecology is precluded by underrepresentation of certain taxa and systems. Models predicting context‐dependent outcomes of biotic interactions have been tested using plants and bacteria, but their applicability to higher taxa is largely unknown.
2. We examined context dependency in a reproductive mutualism between two stream fish species: mound nest‐building bluehead chub Nocomis leptocephalus and mountain redbelly dace Chrosomus oreas, which often uses N. leptocephalus nests for spawning. We hypothesized that increased predator density and decreased substrate availability would increase the propensity of C. oreas to associate with N. leptocephalus and decrease reproductive success of both species.
3. In a large‐scale in situ experiment, we manipulated egg predator density and presence of both symbionts (biotic context), and replicated the experiment in habitats containing high‐ and low‐quality spawning substrate (abiotic context).
4. Contradictory to our first hypothesis, we observed that C. oreas did not spawn without its host. The interaction outcome switched from commensalistic to mutualistic with changing abiotic and biotic contexts, although the net outcome was mutualistic.
5. The results of this study yielded novel insight into how context dependency operates in vertebrate mutualisms. Although the dilution effect provided by C. oreas positively influenced reproductive success of N. leptocephalus, it was not enough to overcome both egg predation and poor spawning habitat quality. Outcomes of the interaction may be ultimately determined by associate density. Studies of context dependency in vertebrate systems require detailed knowledge of species life‐history traits.

     

Can forest fragmentation disrupt a conditional mutualism? A case from central Amazon

This is the first study to investigate whether scatter-hoarding behavior, a conditional mutualism, can be disrupted by forest fragmentation. We examined whether acouchies (Myoprocta acouchy, Rodentia) and agoutis (Dasyprocta leporina, Rodentia) changed scatter-hoarding behavior toward seeds of Astrocaryum aculeatum (Arecaceae) as a consequence of a decrease in forest-patch area. Our study was conducted at the 30-year-old Biological Dynamics of Forest Fragments Project, in central Amazon, Brazil. We tested whether forest size affected the number of Astrocaryum seeds removed and scatter-hoarded (and likely dispersed) by acouchies and agoutis, as well as the distance that the seeds were hoarded. The study extended over three seasons: the peak of the rainy season (March–April), the transition between the rainy and the dry season (May–June), and the peak of the dry season (August–September). Our results revealed that the number of seeds removed was larger in smaller fragments, but that the percentage of seeds hoarded was much lower, and seeds eaten much higher, in 1-ha fragments. Moreover, fewer seeds were taken longer distances in fragments than in the continuous forest. Site affected the number of seeds removed and season affected the percentage of seeds hoarded: more seeds were removed from stations in one site than in two others, and hoarding was more important in April and September than in June. Our study reveals that scatter-hoarding behavior is affected by forest fragmentation, with the most important disruption in very small fragments. Fragmentation converts a largely mutualistic relationship between the rodents and this palm in large forest patches into seed predation in small fragments.     

Evolution of conditional dispersal: a reaction–diffusion–advection model

To study evolution of conditional dispersal, a Lotka-Volterra reaction-diffusion-advection model for two competing species in a heterogeneous environment is proposed and investigated. The two species are assumed to be identical except their dispersal strategies: both species disperse by random diffusion and advection along environmental gradients, but one species has stronger biased movement (i.e., advection along the environmental gradients) than the other one. It is shown that at least two scenarios can occur: if only one species has a strong tendency to move upward the environmental gradients, the two species can coexist since one species mainly pursues resources at places of locally most favorable environments while the other relies on resources from other parts of the habitat; if both species have such strong biased movements, it can lead to overcrowding of the whole population at places of locally most favorable environments, which causes the extinction of the species with stronger biased movement. These results provide a new mechanism for the coexistence of competing species, and they also imply that selection is against excessive advection along environmental gradients, and an intermediate biased movement rate may evolve.     

Is extrafloral nectar production induced by herbivores or ants in a tropical facultative ant–plant mutualism?

Many plants use induced defenses to reduce the costs of antiherbivore defense. These plants invest energy in growth when herbivores are absent but shunt energy to defense when herbivores are present. In contrast, constitutive defenses are expressed continuously regardless of herbivore presence. Induction has been widely documented in temperate plants but has not been reported from tropical plants. Most tropical plants have higher, more constant herbivore pressure than temperate plants. In this situation, it is hypothesized that constitutive defenses rather than induced defense would be favored. Using natural herbivores of four species of Inga saplings on Barro Colorado Island, Panama, herbivore presence was crossed with ant presence to determine their effects on extrafloral nectar production. Analysis of nectar samples revealed that Inga species do not induce nectar production in response to herbivores. This result is not due to an inability of the plants to respond, as the plants in this study increased nectar production in response to light and ant presence. Contrary to most induction experiments with temperate ecosystem plants, these results demonstrate that tropical plants do not induce one type of defense, and they suggest that the most adaptive defense strategies are different for the two ecosystems.     

Ungulate saliva inhibits a grass–endophyte mutualism

Fungal endophytes modify plant–herbivore interactions by producing toxic alkaloids that deter herbivory. However, studies have neglected the direct effects herbivores may have on endophytes. Antifungal properties and signalling effectors in herbivore saliva suggest that evolutionary pressures may select for animals that mitigate the effects of endophyte-produced alkaloids. Here, we tested whether saliva of moose (Alces alces) and European reindeer (Rangifer tarandus) reduced hyphal elongation and production of ergot alkaloids by the foliar endophyte Epichloë festucae associated with the globally distributed red fescue Festuca rubra. Both moose and reindeer saliva reduced the growth of isolated endophyte hyphae when compared with a treatment of distilled water. Induction of the highly toxic alkaloid ergovaline was also inhibited in plants from the core of F. rubra''s distribution when treated with moose saliva following simulated grazing. In genotypes from the southern limit of the species'' distribution, ergovaline was constitutively expressed, as predicted where growth is environmentally limited. Our results now present the first evidence, to our knowledge, that ungulate saliva can combat plant defences produced by a grass–endophyte mutualism.     

Trans-generational specificity within a cnidarian–algal symbiosis

Ocean warming and other anthropogenic stresses threaten the symbiosis between tropical reef cnidarians and their dinoflagellate endosymbionts (Symbiodinium). Offspring of many cnidarians acquire their algal symbionts from the environment, and such flexibility could allow corals to respond to environmental changes between generations. To investigate the effect of both habitat and host genotype on symbiont acquisition, we transplanted aposymbiotic offspring of the common Caribbean octocoral Briareum asbestinum to (1) an environmentally different habitat that lacked B. asbestinum and (2) an environmentally similar habitat where local adults harbored Symbiodinium phylotypes that differed from parental colonies. Symbiont acquisition and establishment of symbioses over time was followed using a within-clade DNA marker (23S chloroplast rDNA) and a within-phylotype marker (unique alleles at a single microsatellite locus). Early in the symbiosis, B. asbestinum juveniles harbored multiple symbiont phylotypes, regardless of source (parent or site). However, with time (~4 yr), offspring established symbioses with the symbiont phylotype dominant in the parental colonies, regardless of transplant location. Within-phylotype analyses of the symbionts revealed a similar pattern, with offspring acquiring the allelic variant common in symbionts in the parental population regardless of the environment in which the offspring was reared. These data suggest that in this host species, host–symbiont specificity is a genetically determined trait. If this level of specificity is widespread among other symbiotic cnidarians, many cnidarian–algal symbioses may not be able to respond to rapid, climate change-associated environmental changes by means of between-generation switching of symbionts.     

Floral phenotypic plasticity as a buffering mechanism in the globeflower–fly mutualism

A buffering mechanism in co-evolutionary relationships could be to display phenotypic plasticity in response to environmental changes. In the nursery pollination mutualism between the European globeflower and its exclusive fly pollinators, adults feed and mate in flowers, and larvae develop feeding on seeds. Flower number and size influence fitness for both partners, and large flowers attract more flies. We tested floral plasticity in plants from two contrasting environments: a high-altitude heath and low- and intermediate-altitude meadow forests. High-altitude plants have single flowers, while meadow-forest plants sometimes have multiple flowers. Plants were grown for 3 years in a garden and supplied with eight times more nutrients than available in natural soils, given to controls. During the experiment, over 90% of all plants with excess nutrients flowered, while in controls, 40% (high-altitude) to 75–78% (meadow-forest) plants flowered. Excess nutrients stimulated 30% larger flowers, and in meadow-forest plants flower number increased 4.5–5 times. Flower number was only doubled in high-altitude plants. High-altitude plants displayed less plasticity, and possibly, a different genetic strategy involving meristem limitation.     

Endosymbiosis as a compact ecosystem with material cycling: parasitism or mutualism?

To discover the evolutionary logic of intracellular endosymbiosis, we investigated a theoretical model (simultaneous ordinary differential equations) of a material-cycling system inside a host cell. In the model, we introduced a recently developed cell biology concept called "autophagy", which is a decomposing-recycle process of self-compiled materials found universally among eukaryote cells. Our model is based on traditional simultaneous ODE for natural ecosystems that involve producing, grazing, and decomposing processes in material cycling. In the basic intracellular metabolic system, several enzymes regulate metabolism by synthesizing and converting metabolites into biomolecules that are precursors for enzymes involved in the producing process. Symbionts are involved in grazing processes and autophagosomes that degrade materials are involved in decomposing recycles. We compared and analyzed the local stability of ODE systems in three cases: (1) the independent, free-living cell (the basal state of a cell), (2) the case where symbionts invade and exploit macrobiomaterials as parasites inside a host cell, and (3) the combination where symbionts assist the host's metabolism. We conclude that: (i) as consumers, symbionts are required to have a growth rate that is higher than the rate of autophagosome decomposition, (ii) the host cell with a biomass larger than the threshold size would realize the mutualistic relationship with its symbiont, and (iii) this partnership accelerates the biomaterial turnover flow on the basis of biomaterials.     

Consumer–resource dynamics of indirect interactions in a mutualism–parasitism food web module

Food web dynamics are well known to vary with indirect interactions, classic examples including apparent competition, intraguild predation, exploitative competition, and trophic cascades of food chains. Such food web modules entailing predation and competition have been the focus of much theory, whereas modules involving mutualism have received far less attention. We examined an empirically common food web module involving mutualistic (N ₂) and parasitic (N ₃) consumers exploiting a resource of a basal mutualist (N ₁), as illustrated by plants, pollinators, and nectar robbers. This mutualism–parasitism food web module is structurally similar to exploitative competition, suggesting that the module of two consumers exploiting a resource is unstable. Rather than parasitic consumers destabilizing the module through (?,?) indirect interactions, two mechanisms associated with the mutualism can actually enhance the persistence of the module. First, the positive feedback of mutualism favors coexistence in stable limit cycles, whereby (+,?) indirect interactions emerge in which increases in N ₂ have positive effects on N ₃ and increases in N ₃ have negative effects on N ₂. This (+,?) indirect interaction arising from the saturating positive feedback of mutualism has broad feasibility across many types of food web modules entailing mutualism. Second, optimization of resource exploitation by the mutualistic consumer can lead to persistence of the food web module in a stable equilibrium. The mutualism–parasitism food web module is a basic unit of food webs in which mutualism favors its persistence simply through density-dependent population dynamics, rather than parasitism destabilizing the module.     

Limiting the cost of mutualism: the defensive role of elongated gynophore in the leafflower–moth mutualism

Mutualisms are interactions from which both partners benefit but may collapse if mutualists’ costs and benefits are not aligned. Host sanctions are one mechanism whereby hosts selectively allocate resources to the more cooperative partners and thereby reduce the fitness of overexploiters; however, many mutualisms lack apparent means of host sanctions. In mutualisms between plants and pollinating seed parasites, such as those between leafflowers and leafflower moths, pollinators consume subsets of the seeds as larval food in return for their pollination service. Plants may select against overexploiters by selectively aborting flowers with a heavy egg load, but in many leafflower species, seeds are fully eaten in some fruits, suggesting that such a mechanism is not present in all species. Instead, the fruits of Breynia vitis-idaea have stalk-like structures (gynophore) through which early-instar moth larvae must bore to reach seeds. Examination of moth mortality in fruits with different gynophore lengths suggested that fruits with longer gynophore had higher moth mortality and, therefore, less seed damage. Most moth mortality occurred at the egg stage or as early larval instar before moths reached the seeds, consistent with the view that gynophore functions to prevent moth access to seeds. Gynophore length was unaffected by plant size, extent of moth oviposition, or geography; thus, it is most likely genetically controlled. Because gynophores do not elongate in related species whose pollinators oviposit directly into the ovary, the gynophore in B. vitis-idaea may have evolved as a defense to limit the cost of the mutualism.     

Mutualism in a community context: the positive feedback between an ant–aphid mutualism and a gall-making midge

Although mutualisms are widespread and often described in natural history accounts, their ecological influences on other community members remain largely unexplored. Many of these influences are likely a result of indirect effects. In this field study, we investigated the indirect effects of an ant–aphid mutualism on the abundance, survival rates and parasitism rates of a co-occurring herbivore. Rabdophaga salicisbrassicoides (Diptera: Cecidomyiidae) induces rosette galls on the developing shoots of Salix exigua trees, and populations can reach outbreak densities (up to 1,000 galls/stem) in central Washington State (USA). Ant-tended aphids feed on these same stems and often feed on gall tissue. In this study we used a combination of manipulative experiments and observational surveys to test the hypothesis that the abundances of aphids, ants, and galls have positive and reciprocal effects on one another, in a manner that would create a positive feedback loop in population growth. In addition, we examined whether the combined presence of ants and aphids reduces parasitism rates for the gallers. In support of the positive feedback loop hypothesis, aphids enjoyed higher population growth rates in the presence of ants and galls, the presence of ants and aphids resulted in increased abundance of galls, and the abundances of ants, aphids and galls were all positively correlated with one another. However, the mechanism underlying the positive effect of ants and aphids on galler density remains unknown, as the mutualism did not affect parasitism rates. More broadly, this study demonstrates that mutualisms can have significant and complex indirect effects on community and population ecology.     

Partner choice in Medicago Truncatula–Sinorhizobium symbiosis

In nitrogen-fixing symbiosis, plant sanctions against ineffective bacteria have been demonstrated in previous studies performed on soybean and yellow bush lupin, both developing determinate nodules with Bradyrhizobium sp. strains. In this study, we focused on the widely studied symbiotic association Medicago truncatula–Sinorhizobium meliloti, which forms indeterminate nodules. Using two strains isolated from the same soil and displaying different nitrogen fixation phenotypes on the same fixed plant line, we analysed the existence of both partner choice and plant sanctions by performing split-root experiments. By measuring different parameters such as the nodule number, the nodule biomass per nodule and the number of viable rhizobia per nodule, we showed that M. truncatula is able to select rhizobia based on recognition signals, both before and after the nitrogen fixation step. However, no sanction mechanism, described as a decrease in rhizobia fitness inside the nodules, was detected. Consequently, even if partner choice seems to be widespread among legumes, sanction of non-effective rhizobia might not be universal.     

Abiotic factors,competition or predation: what determines the distribution of young crayfish in a watershed?

In the headwaters of the New River in western North Carolina, the dominant crayfish species changes with increasing stream size. One transition occurs between third- and fourth-order streams. Cambarus chasmodactylus is the dominant species in third-order tributaries. Orconectes cristavarius is the dominant species in the fourth-order South Fork of the New River. While adult C. chasmodactylus are present in the South Fork, the young-of-the-year (YOY) of this species are absent despite evidence of reproduction. In this study we evaluated the factors that may be responsible for the absence of C. chasmodactylus YOY from the South Fork. A field experiment was used to evaluate the role of abiotic factors and competition with YOY O. cristavarius. There was no significant effect of either of these factors on mortality or growth of C. chasmodactylus YOY. The growth rate of O. cristavarius was 3× faster than that of C. chasmodactylus in this experiment. Since neither abiotic factors nor competition appeared responsible for the exclusion of C. chasmodactylus YOY from the South Fork we evaluated the potential importance of selective predation by rock bass (Ambloplites rupestris), a fish species that is common in the South Fork but virtually absent in the tributaries. In a laboratory experiment, C. chasmodactylus YOY experienced significantly higher mortality than O. cristavarius YOY in the presence of rock bass. Field observations and a laboratory experiment suggest that the two crayfish species differ in their anti-predator behaviors. Cambarus chasmodactylus was less likely to swim when initially disturbed and swam shorter distances than O. cristavarius. The differences in escape behavior and growth rate may contribute to the differences in the vulnerability of the two species to rock bass predation. Our results suggest that intense predation pressure exerted by the rock bass may contribute to the virtual exclusion of C. chasmodactylus YOY from the fourth-order South Fork. Handling editor: J. Trexler     

Patterns in benthic food webs: a role for omnivorous crayfish?

1. The biomass and species richness of macrophytes and invertebrates in artificial ponds at two sites in southern Sweden (twenty-one ponds at each site) were investigated. Alkalinity was high at one site (H ponds) and low at the other site (L ponds). The ponds chosen had different densities of signal crayfish (Pacifastacus leniusculus), with mean crayfish abundance (estimated by trapping and expressed as catch per unit effort) significantly higher in the L ponds (10.7) than in the H ponds (4.9). Macrophytes, invertebrates, the amount of periphyton on stones and the organic content of the sediment were determined in each pond. 2. Macrophyte biomass, cover and species richness declined with increasing crayfish density. Macrophyte species composition differed between ponds and was related to crayfish abundance. 3. The total biomass of invertebrates and the biomass of herbivorous/detritivorous invertebrates declined with increasing crayfish abundance, but the biomass of predatory invertebrates declined only in the L ponds. The relative biomass of Gastropoda and Odonata declined in ponds where crayfish were abundant. In ponds where crayfish were abundant the invertebrate fauna was dominated by sediment-dwelling taxa (Sialis (H and L ponds) and Chironomidae (H ponds)). 4. The number of invertebrate taxa in macrophytes declined with increasing crayfish abundance. The percentage of macrophyte-associated invertebrate taxa differed between ponds, but also between sites. The relative biomass of Gastropoda declined in H ponds where crayfish were abundant. In H ponds Trichoptera or Gammarus sp. and Heteroptera dominated where crayfish were abundant, whereas Odonata dominated in L ponds with abundant crayfish. 5. The organic content of the sediment decreased in ponds with high crayfish densities, while the amount of periphyton on stones was not related to crayfish density. 6. We conclude that the signal crayfish may play an important role as a keystone consumer in pond ecosystems, but lower trophic levels did not respond to changes in the abundance of the crayfish according to the trophic cascade model. Omnivorous crayfish may decouple the cascading effect.