The phylogeny of a mutualism: evolution and coadaptation between Trollius and its seed-parasitic pollinators

Interactions between seed-parasitic pollinators and their hosts provide useful model systems for the analysis of evolution of mutualism and potential coevolution between plants and insects. Here I present the systematics, pollination ecology and evolution of one of these interactions. I have documented and analysed the phylogenetic and geographic associations between Trollius (Ranunculaceae: 18 spp.) and Chiastocheta (Diptera: Anthomyiidae; 17 spp.), a host-specific genus of seed-parasitic flies that pollinate their host plants to varying extent. Their interactions are usually facultative mutualisms, but in the specialized T. europaeus three fly species are obligate mutualists and a fourth species is an antagonist. The distribution patterns of fly species among Trollius species suggest that the flies evolved in associations with five highly derived Trollius species, and secondarily colonized four more primitive taxa in the parts of their ranges that overlapped with primary hosts. In general, host specificity is maintained primarily through allopatry, with colonization occurring in regions of overlap between parapatric taxa. Fly speciation has occurred in allopatry, both within and among host taxa. Cospeciation is not evident, but convergent evolution in Trollius flowers of several traits, viz. orange sepals, elongated staminodia and increased carpel number per flower, may be the result of mutualism with Chiastocheta.     

Hermit crab biocoenoses: a worldwide review of the diversity and natural history of hermit crab associates

The symbiotic associates of hermit crabs (excluding parasites and flora) are reviewed worldwide. The review includes species found on the shells occupied by hermit crabs (epibiotic species), species boring into these shells (endolithic species), species living within the lumen of the shell (either free-living or attached to the shell), species attached to the hermit crabs themselves, and hypersymbionts. In total over 550 invertebrates, from 16 phyla are found associated with over 180 species of hermit crabs. Among these associates, 114 appear to be obligate commensals of hermit crabs, 215 are facultative commensals, and 232 are incidental associates. The taxa exhibiting the highest number of associates are arthropods (126), polychaetes (105), and cnidarians (100). The communities of species associated with Dardanus arrosor, Paguristes eremita, Pagurus bernhardus, Pagurus cuanensis, and Pagurus longicarpus are the best studied and harbor the most diverse assemblages of species. While trends in biodiversity of hermit crab assemblages do not follow predicted patterns (e.g., hermit crabs within the Indo-West Pacific do not harbor more species than those from temperate regions), this is suggested to reflect a lack of sampling rather than a true representation of the number of associates. Hermit crabs date to at least the Cretaceous and provided a niche for a number of groups (e.g., hydractinians, bryozoans, polydorids), which were already associates of living gastropods. Apparently hermit crab shells initially supplied a substrate for settlement and then these symbiotic relationships were reinforced by enhanced feeding of symbionts through the activity of the hosts. Through their use and recycling of gastropods shells, hermit crabs are important allogenic ecosystem engineers in marine habitats from the intertidal to the deep sea. Hermit crabs benefit from some symbionts, particularly cnidarians and bryozoans, through extension of shell apertures (alleviating need to switch into new shells) and by providing protection from predators. However, hermit crabs are also negatively impacted (e.g., decreased reproductive success, increased predation) by some symbionts and a review of egg predators is provided. Thus, the symbiotic relationships between hermit crabs and many associates are difficult to characterize and often exhibit temporal changes depending on environmental and biological factors. Research on the biology of these symbionts and the costs/benefits of their associations with hermit crabs are analyzed. While some associates (e.g., Hydractinia spp.) have been studied in considerable detail, for most associations little is known in terms of the impacts of symbionts on hosts, and future experimental studies on the multitude of relationships are suggested.     

Effects of acute and chronic UV-B exposure on a green alga: a continuous culture study using a computer-controlled dynamic light regime

The green alga Selenastrum capricornutum was grown in a specially developed continuous culture system to study long-term effects of chronic UV-B exposure. The new system improves upon previous laboratory culture approaches. It is demonstrated that short-term experiments underestimate UV-B effects. It is also shown that photoinhibition cannot explain the effects under chronic exposure. Under both nutrient-replete and phosphorus-limiting conditions a UV-B mediated delay in cell division rate and an increase in the cellular content of proteins, carbohydrates and chlorophyll a was measured. Transition experiments showed that complete acclimatisation to UV-B took several cell cycles. DNA damage appears to be the major cause of the observed long-term UV-B effects.     

Dispersal and recruitment of a canopy-forming intertidal alga: the relative roles of propagule availability and post-settlement processes

The daily settlement of eggs and zygotes of the monoecious brown alga Pelvetia compressa (J. Agardh) De Toni was measured on artificial substrata in areas inside and outside patches of adults in the high intertidal zone of central California. Settlement was generally 1–2 orders of magnitude higher under the adult canopy. This pattern seems to be due to the synchronous release of gametes during the daytime low tide. The release of gametes also appears periodic over longer time scales (e.g., 3- and 14-day cycles). In spite of the high availability of propagules under the adult canopy, juveniles were most abundant outside patches, where propagule availability was lower. In both areas, juveniles were disproportionately associated with patches of a red algal turf [primarily Endocladia muricata (Postels & Ruprecht) J. Agardh and Masticarpus papillata (C. Agardh) Kützing]. The turf, which is less common under the P. compressa canopy, may offer protection from dislodgment, grazing, and/or desiccation and thus facilitate recruitment at this site. Overall, post-settlement processes appear more important in determining population structure than does the availability of propagules in areas in and around patches of adults. However, the apparent small range of dispersal of P. compressa may make propagule availability an important limitation to the establishment of new populations and may restrict gene flow between populations. Received: 31 October 1997 / Accepted: 31 August 1998     

Critical population size for fig/wasp mutualism in a seasonal environment: effect and evolution of the duration of female receptivity

Fig trees and their pollinating wasps form ca. 750 pairs of obligate mutualists, mainly in the tropics. Survival of each partner depends on that of its associated species. Here, we examine the possible outcome of such an interaction at small population size. Using phenology data collected on Ficus natalensis in Gabon, we modelled wasp survival and the reproductive success of the trees according to the duration of receptivity of the tree, the amplitude of flowering seasonality, and the size of the fig tree population. Since the duration of receptivity is critical in these population level models, we also determined the influence of individual selection on this phenological trait. The models give three major results: (1) The minimum fig population size required to sustain a wasp population increases with the amplitude of seasonality, and decreases with increasing duration of receptivity; (2) tree population reproductive success is higher when the duration of receptivity is longer and when the population is large, but (3) individual selection toward a long duration of receptivity is weak or absent.     

Spatial variation in the strength of mutualism between a jumping spider and a terrestrial bromeliad: Evidence from the stable isotope N

Psecas chapoda, a neotropical jumping spider strictly associated with the terrestrial bromeliad Bromelia balansae in cerrados and semi-deciduous forests in South America, effectively contributes to plant nutrition and growth. In this study, our goal was to investigate if spider density caused spatial variations in the strength of this spider–plant mutualism. We found a positive significant relationship between spider density and δ¹⁵N values for bromeliad leaves in different forest fragments. Open grassland Bromeliads were associated with spiders and had higher δ¹⁵N values compared to forest bromeliads. Although forest bromeliads had no association with spiders their total N concentrations were higher. These results suggest that bromeliad nutrition is likely more litter-based in forests and more spider-based in open grasslands. This study is one of the few to show nutrient provisioning and conditionality in a spider–plant system.     

Biology of the Epichloë–Botanophila interaction: An intriguing association between fungi and insects

Epichloë fungi (Ascomycota: Clavicipitaceae) are endophytes of grasses that can produce epiphytic stromata on the culms of their hosts. The fungal stromata are visited by Botanophila flies for feeding and egg laying. We review research that has documented the heterothallic mating system of Epichloë, the mutualistic service of spermatization flies provide for the fungus, and host selection by flies. Flies display an active, stereotypical behavior immediately following oviposition by which spermatia are transferred endozoochorously to stromata. After eggs hatch larvae feed on developing perithecia. Several studies have focused on the cost (consumption of ascospores) to the fungus of engaging in the mutualism with its insect visitors. Generally, researchers have found benefits outweigh costs suggesting the mutualism is stable, however exceptions have been reported for Epichloë infecting some commercially cultivated grasses. Because Epichloë fungi are obligate outcrossers and flies are the major (perhaps only) vector of spermatia, the possibility exists that flies could promote reproductive isolation among Epichloë species through specific behavior. This idea has been tested using different approaches including observations of flies within screened cages containing Epichloë species and an analysis of fly gut content, which revealed no or very moderate selectivity by flies. Volatile fungal compounds are responsible for fly attraction and differ among Epichloë species. However, in a field bioassay using species-specific blends of the two predominant volatiles – a sesquiterpene alcohol (chokol K) and a methyl ester – flies showed no preference for specific blends. That is, flies do not appear able to distinguish between different fungal species based on their odor profiles. Thus, it appears that the flies' role in maintaining reproductive isolation among Epichloë species may be minor and that mechanisms of post-zygotic reproductive isolation are more important in keeping compatible species distinct. However, ethological mechanisms such as ‘stroma constancy’ favoring intraspecific mating may operate at a local scale and need to be investigated further.     

Competitive interactions between the lake-dwelling leeches Glossiphonia complanata and Helobdella stagnalis: an experimental investigation of the significance of a food refuge

The glossiphoniid leeches Helobdella stagnalis and Glossiphonia complanata co-exist on the stony shores of British lakes. Because both species have a similar life-style and are food limited, the question arises as to how coexistence persists. Laboratory experiments investigated if either leech has a competitive advantage on three foods, viz. oligochaete worms (Tubifex sp.), snails (Lymnaea peregra), and a worm-plus-snail mixture. A variety of densities with a range of ratios of the two leeches, and monospecific controls were used. The level of feeding ensured increasing food shortage with rising leech density. Experiments, conducted at 14° C, lasted 3 months. Regression values for growth against density in the controls indicated the occurrence of intraspecific competition in both leech species. Light mortality occurred at the highest densities. G. complanata gained significantly less weight in mixed leech cultures than in monospecific cultures at some of the highest densities when fed worms, but more weight when fed on snails. The opposite was true for H. stagnalis. When both prey types were provided, no differences at any density were observed for either leech. Differences in bodysize and feeding strategy between the leeches may be implicated in determining their feeding success on the prey types. Because the anti-predatory responses (e.g. shaking) exhibited by L. peregra are less when encountering an inactive than an active leech, the sit-and-wait strategy of G. complanata may aid snail capture. In contrast, the seek-out strategy of H. stagnalis, coupled with its relatively smaller size, may result in fewer successful captures. The active hunting strategy of H. stagnalis may be advantageous for the capture of oligochaetes which are relatively less mobile than snails. Offering both prey types simultaneously would have had an ameliorating influence on interactions between the two leeches. Findings provide support for the hypothesis that long-term co-existence between the two glossiphoniids in British lakes may depend, in part at least, on the occurrence of a snail food refuge for G. complanata.     

The theory and application of plant competition models: an agronomic perspective

Many studies of plant competition have been directed towards understanding how plants respond to density in monocultures and how the presence of weeds affects yield in crops. In this Botanical Briefing, the development and current understanding of plant competition is reviewed, with particular emphasis being placed on the theory of plant competition and the development and application of mathematical models to crop-weed competition and the dynamics of weeds in crops. By consolidating the results of past research in this manner, it is hoped to offer a context in which researchers can consider the potential directions for future research in competition studies and its application to integrated weed management.     

Evidence for mutualism between a flower-piercing carpenter bee and ocotillo: use of pollen and nectar by nesting bees

Abstract.

• 1 Carpenter bees (Xylocopa californica arizonensis) in west Texas, U.S.A., gather pollen and ‘rob’ nectar from flowers of ocotillo (Fouquieria splendens). When common, carpenter bees are an effective pollen vector for ocotillo. We examined ocotillo's importance as a food source for carpenter bees.
• 2 The visitation rate of carpenter bees to ocotillo flowers in 1988 averaged 0.51 visits/flower/h and was 4 times greater than that of queen bumble bees (Bombus pennsylvanicus sonorus), the next most common visitor. Nectar was harvested thoroughly and pollen was removed from the majority of flowers. Hummingbird visits were rare.
• 3 Pollen grains from larval food provisions were identified from sixteen carpenter bee nests. On average, 53% of pollen grains sampled were ocotillo, 39% were mesquite (Prosopis glandulosa), and 8% were Zygophyllaceae (Larrea tridentata or Guaiacum angustifolium). Carpenter bee brood size averaged 5.8 per nest.
• 4 We measured the number of flowers, and production of pollen and nectar per flower by mature ocotillo plants, as well as the quantity of pollen and sugar in larval provisions. An average plant produced enough pollen and nectar sugar to support the growth of eight to thirteen bee larvae. Ocotillo thus has the potential to contribute significantly to population growth of one of its key pollinators.
• 5 Although this carpenter bee species, like others, is a nectar parasite of many plant species, it appears to be engaged in a strong mutualism with a plant that serves as both a pollen and as a nectar source during carpenter bee breeding periods.

     

First record of an epibiosis between the sand crab Emerita analoga (Stimpson, 1857) (Decapoda: Hippidae) and the mussel Semimytilus algosus (Gould, 1850) (Bivalvia, Mytilidae) in southern Peru

Coastal zones of the Humboldt Current Upwelling System (HCUS) are composed both of rocky and sandy beaches inhabited by macrozoobenthic communities. These show oscillating changes in the dominance of species; the abundance of the sand crab Emerita analoga is linked to phases of the El Niño Southern Oscillation (ENSO). The biogenic surfaces of these crabs serve as substrate for opportunistic colonizers. This study is the first record of an epibiosis between E. analoga and the rock mussel Semimytilus algosus, detected at a southern Peruvian sandy beach. Mussels fouled a wide size-range of adult E. analoga (7.3%) but they themselves belonged to small-size classes. The largest S. algosus was 17.4 mm in length. Highest permanence of epibionts was found on larger sand crabs (maximum between 24 and 27 mm). Significantly more mussels were found on the ventral surface (39.4%) compared to 10 other surface areas of the sand crab. Possible benefits and disadvantages of the observed epibiosis for both the basibiont and the epibiont are discussed.     

The influence of vines on an oligohaline marsh community: results of a removal and fertilization study

The effects of competitive suppression by vines on the non-vine plant community have received little attention in temperate habitats. This study investigated the impact vines have on their herbaceous hosts in a wetland community at two soil fertility levels. Plots in an oligohaline marsh were treated in a 2 × 2 factorial design with vine removal and fertilization over two growing seasons. There was no significant interaction between removal and fertilization treatments on any of the measured variables. Vine removal initially caused an increase in light penetration through the canopy, but by the end of the study, plots with vines removed had less light due to a 25% increase in biomass by the plants released from competition with vines. For plots with vines removed, species richness was higher during a brief period in the spring of the second year, but by the end of the study, richness in removal plots decreased relative to controls. Fertilization caused a 40% increase in biomass overall, although only two species, Sagittaria lancifolia L. and Polygonum punctatum Ell., showed dramatic increases. Despite fertilization causing a 40% decrease in light penetration to the ground, no change in species richness was observed. Overall, these results show that vine cover in this wetland suppresses non-vine species and reduces community biomass. Removal of vines increased biomass of non-vine dominants but resulted in only an ephemeral change in species richness. Fertilization did not increase the effects of vines on the non-vine community. Received: 14 November 1996 / Accepted: 10 June 1997     

Control of foraging behavior of individuals within an ecosystem context: the clam Macoma balthica and interactions between competition and siphon cropping

Macoma balthica (L.) is a common clam of the estuarine seafloor, belonging to an important group of invertebrates possessing the capacity to choose between the two fundamental modes of feeding available, using its siphon to inhale either suspended food particles from the water or food particles deposited on the sediment surface. Field experiments demonstrate that intraspecific competition, effects of other competing benthic invertebrates, and complex interactions between competition and partial predation (siphon cropping by fishes) modify the foraging behavior of Macoma. When protected by caging from siphon nipping by fishes, Macoma demonstrated greater siphon regeneration at lower density, indicating the importance of competition for limited resources. In the absence of siphon croppers, these same clams also exhibited more deposit feeding at the lower density either because of improved ability to deposit-feed with longer siphons or because deposited foods become more rapidly depleted than suspended foods on local spatial scales. Addition of siphon-nipping fishes caused greater reductions in siphon size of clams at lower density, presumably because the intensity of nipping per clam was greater where clam targets were fewer and because deposit feeding, which was more intense at lower densities, confers a greater risk of cropping from greater siphon extension and activity than characterize suspension feeding. Deposit feeding by Macoma was reduced in the presence of siphon croppers at both high and low density of clams, but the intensity of deposit-feeding activity at low density was substantially higher than predicted by additive effects of clam density and cropping. This suggests operation of a balancing strategy in Macoma whereby it is accepting greater risks of partial predation when rewards of greater food harvest are larger. The surprising failure to adopt a risk-averse stratery may be explained by the non-lethal nature of partial predation, which renders siphon loss an energetic penalty replacable through regeneration. The presence of a bed of suspension-feeding Rangia cuneata also altered foraging behavior of Macoma by inducing a switch to more intense deposit feeding, in response either to the documented near-bottom depletion of suspended foods or to likely enhanced biodeposition from feces and pseudofeces. The induction of greater deposit feeding by the presence of this competing suspension feeder led to greater siphon losses during exposure to croppers because Macoma was practicing more risky feeding behavior. This enhanced loss of siphon tissues to croppers in the presence of the suspension-feeding Rangia induced an interaction between the effects of siphon croppers and Rangia, such that Macoma exhibited a larger switch away from deposit feeding in the presence of siphon croppers when Rangia were also present. Clearly, the foraging decisions made by individuals can only be understood in a broad holistic context of population, community, and ecosystem processes.     

Gene structure of a chlorophyll a/c-binding protein from a brown alga: Presence of an intron and phylogenetic implications

A Laminaria saccharina genomic library in the phage EMBL 4 was used to isolate and sequence a full-length gene encoding a fucoxanthin-chlorophyll a/c-binding protein. Contrary to diatom homologues, the coding sequence is interrupted by an intron of about 900 bp which is located in the middle of the transit peptide. The deduced amino acid sequence of the mature protein is very similar to those of related proteins from Macrocystis pyrifera (Laminariales) and, to a lesser extent, to those from diatoms and Chrysophyceae. Seven of the eight putative chlorophyll-binding amino acids determined in green plants are also present. Alignments of different sequences related to the light-harvesting proteins (LHC) demonstrate a structural similarity among the three transmembrane helices and suggest a unique ancestral helix preceded by two β-turns. The β-turns are conserved in front of the second helices of the chlorophyll a/c proteins more so than in chlorophyll a/b proteins. Phylogenetic trees generated from sequence data indicate that fucoxanthin-chlorophyll-binding proteins diverged prior to the separation of photosystem I and photosystem II LHC genes of green plants. Among the fucoxanthin-containing algae, LHC I or II families could not be distinguished at this time. Received: 14 February 1996 / Accepted: 4 April 1996     

Mutualism between Maieta guianensis Aubl., a myrmecophytic melastome,and one of its ant inhabitants: ant protection against insect herbivores

Summary The hypothesis that ants (Pheidole minutula) associated with the myrmecophytic melastome Maieta guianensis defend their host-plant against herbivores was investigated in a site near Manaus, Amazonas, Brazil. M. guianensis is a small shrub that produces leaf pouches as ant domatia. Plants whose ants were experimentally removed suffered a significant increase in leaf damage compared with control plants (ants maintained). Ants patrol the young and mature leaves of Maieta with the same intensity, presumably since leaves of both ages are equally susceptible to herbivore attack. The elimination of the associated ant colony, and consequent increase in herbivory, resulted in reduced plant fitness. Fruit production was 45 times greater in plants with ants than in plants without ants 1 year after ant removal.     

Interactions of plant stress and herbivory: intraspecific variation in the susceptibility of a palatable versus an unpalatable seaweed to sea urchin grazing

Summary Interactions among environmental stresses, plant defensive characteristics, and plant nutrient status may significantly affect an alga's susceptibility to herbivores. Following desiccation, the palatable seaweed Gracilaria tikvahiae was less susceptible to grazing by the sea urchin Arbacia punctulata while the unpalatable alga Padina gymnospora became more susceptible. Increased grazing on desiccated Padina appeared to result from a loss of chemical defenses following desiccation. Palatable plants treated with organic extracts from desiccated Padina plants were consumed at more than twice the rate of plants treated with extracts from undesiccated plants. Increased susceptibility of Padina did not correlate with changes in protein content of the alga; reduced grazing on desiccated Gracilaria was associated with a decrease in protein content. When Padina was grazed by Arbacia or mechanically damaged to mimic urchin grazing, its susceptibility to Arbacia decreased within 1 to 5 days. These results demonstrate that history of physical or biological stress may affect a plant's susceptibility to herbivory. We hypothesize that urchins cue primarily on attractiveness features (e.g. nutrient content) of highpreference algae and deterrent features (e.g. chemical defenses) of low-preference algae. Stresses may therefore increase, decrease, or not affect a plant's susceptibility to herbivory depending upon the primary feeding cues used by the herbivore, the defensive mechanisms used by the plant, and the way these are altered by various environmental stresses.     

Implications of rapid changes in chlorophyll-<Emphasis Type="Italic">a</Emphasis> of plankton,epipelon, and epiphyton in a Pampean shallow lake: an interpretation in terms of a conceptual model

Biomass assessments of algae in wetlands usually include only the phytoplankton community without considering the contribution of other algal associations to total algal biomass. This omission prevents an accurate evaluation of the phytoplankton community as an integral part of the total ecosystem. In the present work, the biomass contributions (expressed as chlorophyll-a content per m² of lake) of phytoplankton, epiphyton on both submerged and emergent macrophytes, and epipelon were measured in Lacombe Lake, Argentina, for the purpose of (1) establishing the relative importance of the phytoplankton and (2) evaluating the entire contribution of algal biomass within the context of the Goldsborough & Robinson conceptual model. Our sampling was carried out monthly for a year in sites representative of different conditions with respect to water depth and type of macrophytes. Physicochemical analyses of water were performed following standard methods. Plankton was collected in a five-level profile at deeper stations and in subsurface samples at the shallow one. Samples of sediment obtained with corers were collected for epipelon sampling and segments of plants were cut at different levels, so as to obtain the epiphytes by scraping. Pigment was extracted with aqueous acetone and calculations were made by means of the Lorenzen equation. According to the Goldsborough & Robinson model, a Lake State developed here during the winter (phytoplankton maxima: 150 mg chlorophyll-a per m²). Then, through the subsequent growth of the submerged macrophytes, an Open State was observed, characterized by a maximum epiphyton biomass (at 3,502 mg chlorophyll-a per m²) along with lower levels of phytoplankton biomass. The epiphytic algae on the emergent macrophytes were always present but attained only relatively low biomass values (maximum: 120 mg of chlorophyll-a per m² in February). The epipelon biomass varied between 50 and 252 mg chlorophyll-a per m², registering a considerable contribution of settled algae from the water column (phytoplankton). This study contributes to our knowledge of wetland dynamics through its assessment of the rapid changes in the relative contributions of both planktonic and attached algae to the total algal biomass within the context of specific environmental factors. Guest editors: U. M. Azeiteiro, I. Jenkinson & M. J. Pereira Plankton Studies     

Pollen precedence and stigma closure: a mechanism of competition for pollination between Delphinium nelsonii and Ipomopsis aggregata

Summary Previous experiments showed that the sympatric herbs Delphinium nelsonii and Ipomopsis aggregata compete for hummingbird pollination and that deleterious effects of the former species on seed set of the latter involve interspecific pollen transfer. However, seed set was not reduced when pollen of both species was applied simultaneously to I. aggregata stigmas. Hence a competitive effect may require arrival of foreign pollen before conspecific pollen. To explore this possibility we subjected I. aggregata flowers to a competition treatment in which they received D. nelsonii pollen 6 h before I. aggregata pollen, or to a control in which they received only the conspecific pollen. Foreign pollen precedence decreased mean seed set by almost 50%, which is consistent with effects observed in previous experiments. Reduced seed set can be explained by the fact that foreign pollen often caused stigma lobes to close together within 1.5–6 h, reducing subsequent receptivity. Stigma closure was also elicited by conspecific pollen, but not by mechanical stimulation, and was influenced by size of the pollen load and identity of the plant being pollinated.