A carnivorous plant fed by its ant symbiont: a unique multi-faceted nutritional mutualism

Scarcity of essential nutrients has led plants to evolve alternative nutritional strategies, such as myrmecotrophy (ant-waste-derived nutrition) and carnivory (invertebrate predation). The carnivorous plant Nepenthes bicalcarata grows in the Bornean peatswamp forests and is believed to have a mutualistic relationship with its symbiotic ant Camponotus schmitzi. However, the benefits provided by the ant have not been quantified. We tested the hypothesis of a nutritional mutualism, using foliar isotopic and reflectance analyses and by comparing fitness-related traits between ant-inhabited and uninhabited plants. Plants inhabited by C. schmitzi produced more leaves of greater area and nitrogen content than unoccupied plants. The ants were estimated to provide a 200% increase in foliar nitrogen to adult plants. Inhabited plants also produced more and larger pitchers containing higher prey biomass. C. schmitzi-occupied pitchers differed qualitatively in containing C. schmitzi wastes and captured large ants and flying insects. Pitcher abortion rates were lower in inhabited plants partly because of herbivore deterrence as herbivory-aborted buds decreased with ant occupation rate. Lower abortion was also attributed to ant nutritional service. The ants had higher δ(15)N values than any tested prey, and foliar δ(15)N increased with ant occupation rate, confirming their predatory behaviour and demonstrating their direct contribution to the plant-recycled N. We estimated that N. bicalcarata derives on average 42% of its foliar N from C. schmitzi wastes, (76% in highly-occupied plants). According to the Structure Independent Pigment Index, plants without C. schmitzi were nutrient stressed compared to both occupied plants, and pitcher-lacking plants. This attests to the physiological cost of pitcher production and poor nutrient assimilation in the absence of the symbiont. Hence C. schmitzi contributes crucially to the nutrition of N. bicalcarata, via protection of assimilatory organs, enhancement of prey capture, and myrmecotrophy. This combination of carnivory and myrmecotrophy represents an outstanding strategy of nutrient sequestration.     

Evolution of a unique seed maturity pattern in Croton bonplandianum Baill strengthens ant-plant mutualism for seed dispersal

Summary The female flowers of Croton bonplandianum bear nectar glands which become active during fruit maturation and attain peak activity just prior to the splitting of fruits. This temporal specificity of nectar gland activity is shown to facilitate seed dispersal by ants, which are attracted to the plant only during the fruit maturation period. The nectar glands establish a nectar influence zone with a radius of 60 cm around the plant within which seed dispersal by ants is effective. Seed dispersal by ants is facilitated only if the seeds are placed within this nectar influence zone. This is accomplished by an intriguing evolutionary shift in the maturation pattern of the fruits. Unlike the usual acropetal development, fruit maturation in Croton is temporally asymmetrical, with the fruits nearer the parental axis maturing early. This unique pattern of fruit development together with the polychasial branching system leads to a concentration of seeds within the nectar influence zone and enhances seed dispersal by ants. The proximate factors responsible for this asynchronous fruit maturity were investigated.     

Effects of a belowground mutualism on an aboveground mutualism

Studies of multitrophic interactions between below‐ and aboveground communities have generally focused on soil organisms and antagonists of plant shoots and leaves (herbivores). Despite the widespread occurrence of plant mutualists below‐ and aboveground which can occur on the same host plant, the potential for interactions between them has not been considered. Here we demonstrate that aboveground plant mutualists, insect pollinators, are strongly influenced by belowground plant mutualists, arbuscular mycorrhizal fungi. The presence of arbuscular mycorrhizal fungi in the roots of Chamerion angustifolium increased pollinator visitation and per cent seed set of this plant in the field by up to two times compared with non‐mycorrhizal plants. We propose that interactions between belowground and aboveground mutualisms are widespread and may play important functional roles in populations and communities.     

Discovery of a unique strain-specific idiotypic antigenic determinant of mouse T-lymphocyte antigen-recognizing receptors

The cellular radioimmunoassay using rabbit anti-CBA-anti-C57BL/6 antiidiotypic serum was performed to detect a private strain-specific antigenic idiotypic determinant (s) on activated CBA-anti-C57BL/6 T cells. This private idiotype was not expressed on other activated T cells under study: CBA-anti-BALB/C; C3H-anti-C57BL/6; AKR-anti-C57BL/6; A/Sn-anti-C57BL/6; BALB/C-anti-C57BL/6; DBA/2-anti-C57BL/6. It is suggested that gene (s) coding the private strain-specific idiotypic antigenic determinant of the antigen-recognition receptor of T cells is not localized on the H-2 complex of mice.     

Lake-front property: a unique germinal niche by the lateral ventricles of the adult brain

New neurons and glial cells are generated in an extensive germinal niche adjacent to the walls of the lateral ventricles in the adult brain. The primary progenitors (B1 cells) have astroglial characteristics but retain important neuroepithelial properties. Recent work shows how B1 cells contact all major compartments of this niche. They share the "shoreline" on the ventricles with ependymal cells, forming a unique adult ventricular zone (VZ). In the subventricular zone (SVZ), B1 cells contact transit amplifying (type C) cells, chains of young neurons (A cells), and blood vessels. How signals from these compartments influence the behavior of B1 or C cells remains largely unknown, but recent work highlights growth factors, neurotransmitters, morphogens, and the extracellular matrix as key regulators of this niche. The integration of emerging molecular and anatomical clues forecasts an exciting new understanding of how the germ of youth is actively maintained in the adult brain.     

Dynamics of a mutualism in a multi-species context

Despite recent findings that mutualistic interactions between two species may be greatly affected by species external to the mutualism, the implications of such multi-species interactions for the population dynamics of the mutualists are virtually unexplored. In this paper, we ask how the mutualism between the shoot-base boring weevil Apion onopordi and the rust fungus Puccinia punctiformis is influenced by the dynamics of their shared host plant Cirsium arvense, and vice versa. In particular, we hypothesized that the distribution of the weevil's egg load between healthy and rust-infected thistles may regulate the abundance of the mutualists and their host plant. In contrast to our expectations we found that the dynamics of the mutualists are largely determined by the dynamics of their host. This is, to our knowledge, the first demonstration that the dynamics of a mutualism are driven by a third, non-mutualistic species.     

Ant benefits in a seed dispersal mutualism

Myrmecochorous plant seeds have nutrient rich appendages, elaiosomes, which induce some ant species to carry the seeds back to their nest where the elaiosome is consumed and the seed is discarded unharmed. The benefits to plants of dispersal of their seeds in this way have been well documented, but the benefits to the ants from consuming the elaiosomes have rarely been measured and are less clear. Ant benefits from myrmecochory were investigated in a laboratory experiment using the ant Myrmica ruginodis and seeds of Ulex species. To separate the effects of elaiosome consumption on the development of newly produced larvae versus existing larvae, ten ‘Queenright’ colonies containing a queen were compared to ten ‘Queenless’ colonies. Six measures of colony fitness over a complete annual cycle were taken: sexual production, larval weight and number, pupal weight and number, and worker survival. Queenless colonies fed with elaiosomes produced 100.0±29.3 (mean ± SE) of larvae compared to non-elaiosome fed colonies which produced 49.6±19.0; an increase of 102%. Larval weight increased in both Queenright and Queenless colonies. In colonies fed with elaiosomes, larvae weighed 1.02±0.1 mg, but in non-elaiosome fed colonies larvae weighed 0.69±0.1 mg; an increase of 48%. The food supplement provided by Ulex elaiosomes was trivial in energetic terms, under the conditions of an ample diet, suggesting that these effects might be due to the presence of essential nutrients. Chemical analysis of Ulex elaiosomes showed the presence of four essential fatty acids and four essential sterols for ants.     

The cost of mutualism in a fly-fungus interaction

The movement ability of individuals has become increasingly important to a variety of ecological questions. In this study, I investigate how plant structure and changes in body size through development affect the movement ability of a predaceous stinkbug, Podisus maculiventris, on three species of goldenrod (Solidago spp.) representing a wide range of surface complexities. I adapt existing techniques for quantifying movement in two dimensions to the study of movement on natural plant structures in three dimensions. These experiments indicate that plant structure and insect size are significant factors affecting the movement ability of P. maculiventris. Changes in movement ability due to factors of ontogeny and different habitat structures suggest that the scale of an individual’s ambit or ecological sphere of influence may vary within its lifespan. Considering the influence of ontogeny and habitat structure on movement ability may be useful to investigations of population dynamics, foraging behavior, and pest management. Received: 14 July 1999 / Accepted: 23 March 2000     

A unique resource mutualism between the giant Bornean pitcher plant, Nepenthes rajah, and members of a small mammal community

The carnivorous pitcher plant genus Nepenthes grows in nutrient-deficient substrates and produce jug-shaped leaf organs (pitchers) that trap arthropods as a source of N and P. A number of Bornean Nepenthes demonstrate novel nutrient acquisition strategies. Notably, three giant montane species are engaged in a mutualistic association with the mountain treeshrew, Tupaia montana, in which the treeshrew defecates into the pitchers while visiting them to feed on nectar secretions on the pitchers' lids.Although the basis of this resource mutualism has been elucidated, many aspects are yet to be investigated. We sought to provide insights into the value of the mutualism to each participant. During initial observations we discovered that the summit rat, R. baluensis, also feeds on sugary exudates of N. rajah pitchers and defecates into them, and that this behavior appears to be habitual. The scope of the study was therefore expanded to assess to what degree N. rajah interacts with the small mammal community.We found that both T. montana and R. baluensis are engaged in a mutualistic interaction with N. rajah. T .montana visit pitchers more frequently than R. baluensis, but daily scat deposition rates within pitchers do not differ, suggesting that the mutualistic relationships are of a similar strength. This study is the first to demonstrate that a mutualism exists between a carnivorous plant species and multiple members of a small mammal community. Further, the newly discovered mutualism between R. baluensis and N. rajah represents only the second ever example of a multidirectional resource-based mutualism between a mammal and a carnivorous plant.     

Histochemical and myosin composition of vampire bat (Desmodus rotundus) pectoralis muscle targets a unique locomotory niche

The vampire bat pectoralis muscle contains at least four fiber types distributed in a nonhomogeneous pattern. One of these fiber types, here termed IIe, can be elucidated only by adenosine triphosphatase (ATPase) histochemistry combined with reactions against antifast and antislow myosin antibodies. The histochemical and immunohistochemical observations indicate a well-developed specialization of function within specific regions of the muscle. In parallel, analyses of native myosin isoforms and myosin heavy chain isoforms indicate two points. First, the histochemical “type IIe” fiber is predominant in cranial portions of the muscle, and myosin extracted from these regions exhibits a unique electrophoretic mobility not observed in the myosin isoforms of more traditional laboratory mammals. Second, the type I fibers are confined to the pectoralis abdominalis muscle and a small adjacent region of the caudal part of the pectoralis. This pattern of type I fiber distribution is considered a derived character state compared to muscle histochemical phenotype and isoform composition in the pectoralis muscles of other phyllostomids we have studied (Artibeus jamaicensis, Artibeus lituratus, Carollia perspicillata). We relate this to the unique locomotory needs of the common vampire bat, Desmodus rotundus. © 1993 Wiley-Liss, Inc.     

Costs and benefits of a cleaning mutualism

Juvenile Atlantic salmon or parr ( Salmo salar L.) maintain station at certain locations in flowing stream water. This position choice is assumed to involve the maximization of energy intake, based upon food availability which is usually directly related to water flow rate. Conversely energy expenditure, including station holding behaviour, foraging and defending preferred sites, is inversely related to water flow rate. Adaptations of parr to life in fast flows implies that station holding is energetically inexpensive at water speeds up to the maximum sustained holding speed, which is fish specific, thus the most important energetic consideration for parr is the ability to maximize food intake. Ten groups of three parr were each observed for 60 min within an artificial stream tank over a heterogeneous substratum. Individual position choice and behaviour were recorded continuously. For each location chosen by the parr the potential upstream line‐of‐sight (LOS), defined as the maximum distance upstream that the water surface would be visible, was calculated. At those sites where foraging behaviour was observed, the mean upstream potential LOS was significantly greater than at sites where other behaviours were observed and at 400 randomly generated sites within the tank. When foraging, parr usually take food from the stream drift and there is a significant time expenditure on food location, identification and catching. Results presented here would seem to confirm that to maximize time available to make these decisions, a fish would be expected to maximize the distance over which it can observe potential food particles.     

Isotopic niche mirrors trophic niche in a vertebrate island invader

Caution for the indiscriminate conversion of the isotopic niche into ecologic niche was recently advised. We tested the utility of the isotopic niche to answer ecological questions on oceanic islands. We compared the isotopic niches of black rats (Rattus rattus) on two islands in the Gulf of California, Mexico: Farrallón de San Ignacio (FSI) and San Pedro Mártir (SPM). Both islands maintained several species of marine birds, but FSI is devoid of terrestrial vegetation and SPM has several species of terrestrial plants. We tested the hypothesis that rats on FSI have a narrower trophic niche due to its lower diversity of food items. We predicted a smaller variance in δ¹³C and δ¹⁵N values of rat muscle on FSI, and a lower use of marine birds as food on SPM. We also examined stomach contents of rats on both islands to validate the isotopic information. Variances in δ¹³C and δ¹⁵N values of black rats were lower on FSI, and the contribution of marine birds to the diet of rats was smaller on SPM. Stomachs in most rats collected on FSI contained only one or two types of food items, mostly marine birds and terrestrial invertebrates. In contrast, stomachs with only one type of food item were rare on SPM, and in most cases they contained three or more food types. Our findings showed that isotopic variance is a good approximation for trophic niche when comparing populations with access to an assemblage of preys with contrasting biological and isotopic diversity.     

Rational engineering of a synthetic insect-bacterial mutualism

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Geographic structure of lineage associations in a plant-bacterial mutualism

Two species linked by a mutualistic relationship may evolve correlated population differentiation if there is long-term continuity of interactions between specific partners. This phenomenon was analyzed by multilocus enzyme electrophoresis on the annual legume Amphicarpaea bracteata and its nitrogen-fixing bacterial symbionts (Bradyrhizobium sp.) sampled from >20 sites over a 1000 km area. Three analyses indicated that genetic differentiation was correlated in the two organisms. First, the genetic distance between bacterial populations at each pair of sites was significantly positively related to the genetic distance between their host plant populations, as evaluated by the Mantel test. Second, a cluster analysis revealed that several divergent lineages were present both among plants and among bacteria. Bacterial lineages showed a highly nonrandom distribution across plant lineages that was consistent in each of two regions sampled. Finally, there were numerous cases where populations of the same plant lineage 1000 km apart harbored bacterial isolates with an identical multilocus genotype. Thus, despite recurrent opportunities for partner switching, particular genotypes of these two organisms associate consistently across multiple habitats throughout their geographic range.     

Nematode–bacteria mutualism: Selection within the mutualism supersedes selection outside of the mutualism

The coevolution of interacting species can lead to codependent mutualists. Little is known about the effect of selection on partners within verses apart from the association. Here, we determined the effect of selection on bacteria (Xenorhabdus nematophila) both within and apart from its mutualistic partner (a nematode, Steinernema carpocapsae). In nature, the two species cooperatively infect and kill arthropods. We passaged the bacteria either together with (M+), or isolated from (M?), nematodes under two different selection regimes: random selection (S?) and selection for increased virulence against arthropod hosts (S+). We found that the isolated bacteria evolved greater virulence under selection for greater virulence (M?S+) than under random selection (M?S?). In addition, the response to selection in the isolated bacteria (M?S+) caused a breakdown of the mutualism following reintroduction to the nematode. Finally, selection for greater virulence did not alter the evolutionary trajectories of bacteria passaged within the mutualism (M+S+ = M+S?), indicating that selection for the maintenance of the mutualism was stronger than selection for increased virulence. The results show that selection on isolated mutualists can rapidly breakdown beneficial interactions between species, but that selection within a mutualism can supersede external selection, potentially generating codependence over time.     

Cheaters in mutualism networks

Mutualism-network studies assume that all interacting species are mutualistic partners and consider that all links are of one kind. However, the influence of different types of links, such as cheating links, on network organization remains unexplored. We studied two flower-visitation networks (Malpighiaceae and Bignoniaceae and their flower visitors), and divide the types of link into cheaters (i.e. robbers and thieves of flower rewards) and effective pollinators. We investigated if there were topological differences among networks with and without cheaters, especially with respect to nestedness and modularity. The Malpighiaceae network was nested, but not modular, and it was dominated by pollinators and had much fewer cheater species than Bignoniaceae network (28% versus 75%). The Bignoniaceae network was mainly a plant–cheater network, being modular because of the presence of pollen robbers and showing no nestedness. In the Malpighiaceae network, removal of cheaters had no major consequences for topology. In contrast, removal of cheaters broke down the modularity of the Bignoniaceae network. As cheaters are ubiquitous in all mutualisms, the results presented here show that they have a strong impact upon network topology.     

Finding a niche

Although I always knew I wanted to be a scientist, I didn't know I would become a cell biologist. Events in life that you would never have predicted can greatly impact your career trajectory. I have learned to let those events take me in new directions. Following a desire to investigate an understudied area of cell biology, I have found a niche. In this area, my lab is poised to contribute significantly toward understanding the fundamental molecular mechanisms underlying polarized plant cell growth.