Intraspecific variation in palatability and defensive chemistry of brown seaweeds: effects on herbivore fitness

When offered a choice between brown seaweeds (Phaeophyta) from shallow inshore populations versus deeper offshore populations along the mid-Atlantic coast of the United States of America, the herbivorous amphipod Ampithoe longimana consistently preferred plants from the inshore populations. This was the case for three species (Dictyota menstrualis, Spatoglossum schroederi, and Sargassum filipendula) collected from each of a single inshore and offshore site, and for one species (D. menstrualis) collected from each of three inshore and three offshore sites. Bioassay-guided fractionation of chemical crude extracts from D. menstrualis suggested that the relative unpalatability of the offshore plants was due to the lipid-soluble secondary metabolites 4beta-hydroxydictyodial A and 18, O-dihydro-4beta-hydroxydictyodial A 18-acetate, along with minor compounds that were not fully identified. The inshore-offshore pattern did not appear to result from induction of defenses due to herbivory by mesograzers, as mesograzer densities were higher on the more palatable inshore plants. Herbivore feeding preferences for inshore versus offshore seaweeds matched the effects of those seaweeds on their fitness. When juvenile amphipods were raised on inshore versus offshore tissues of D. menstrualis, amphipod survivorship, growth, and ovulation were significantly suppressed on the offshore compared to the inshore tissues. Few previous investigations have studied intraspecific variance in seaweed palatability. We extend these by showing that between-population differences in palatability can persist for several years and by demonstrating that this variance is chemically based and has dramatic effects on herbivore fitness.     

Variation in natural selection for growth and phlorotannins in the brown alga Fucus vesiculosus

Directional selection for plant traits associated with resistance to herbivory tends to eliminate genetic variation in such traits. On the other hand, balancing selection arising from trade-offs between resistance and growth or spatially variable selection acts against the elimination of genetic variation. We explore both the amount of genetic variation and variability of natural selection for growth and concentration of phenolic secondary compounds, phlorotannins, in the brown alga Fucus vesiculosus. We measured variation in selection at two growing depths and two levels of nutrient availability in algae that had faced two kinds of past growing environments. Genetic variation was low for growth but high for phlorotannins. The form and strength of selection for both focal traits depended on the past growing environment of the algae. We found strong directional selection for growth rate in algae previously subjected to higher ultraviolet radiation, but not in algae previously subjected to higher nutrient availability. Stabilizing selection for growth occurred especially in the deep growing environment. Selection for phlorotannins was generally weak, but in some past-environment-current-environment combinations we detected either directional selection against phlorotannins or stabilizing selection. Thus, phlorotannins are not selectively neutral but affect the fitness of F. vesiculosus. In particular, there may be a fitness cost of producing phlorotannins, but the realization of such a cost varies from one environment to another. Genetic correlations between selective environments were high for growth but nonexistent for phlorotannins, emphasizing the high phenotypic plasticity of phlorotannin production. The highly heterogeneous selection, including directional, stabilizing, and spatially variable selection as well as temporal change in selection due to responses to past environmental conditions, probably maintains a high amount of genetic variation in phlorotannins. Such variation provides the potential for rapid evolutionary response of phlorotannins under directional selection.     

Brominated phlorethols and nonhalogenated phlorotannins from the brown alga Cystophora congesta

The following phlorotannins were isolated from the brown alga Cystophora congesta and characterized as their acetates: phloroglucinol triacetate, bromodiphlorethol pentaacetate, diphlorethol pentaacetate, bromotriphlorethol-A₁-heptaacetate, bromotriphlorethol-A₂-heptaacetate, tetraphlorethol-C-nonaacetate and fucodiphlorethol-D-decaacetate. The substances bromodiphlorethol pentaacetate, bromotriphlorethol-A₁-heptaacetate and bromotriphlorethol-A₂-heptaacetate are the first brominated members of this series to be described. Triphlorethol-A- heptaacetate was isolated previously from C. congesta.     

DNA variation in the phenotypically-diverse brown alga Saccharina japonica

ABSTRACT: BACKGROUND: Saccharina japonica (Areschoug) Lane, Mayes, Druehl et Saunders is an economically important and highly morphologically variable brown alga inhabiting the northwest Pacific marine waters. On the basis of nuclear (ITS), plastid (rbcLS) and mitochondrial (COI) DNA sequence data, we have analyzed the genetic composition of typical Saccharina japonica (TYP) and its two common morphological varieties, known as the "longipes" (LON) and "shallow-water" (SHA) forms seeking to clarify their taxonomical status and to evaluate the possibility of cryptic species within S. japonica. RESULTS: The data show that the TYP and LON forms are very similar genetically in spite of drastic differences in morphology, life history traits, and ecological preferences. Both, however, are genetically quite different from the SHA form. The two Saccharina lineages are distinguished by 109 fixed single nucleotide differences as well as by seven fixed length polymorphisms (based on a 4,286 bp concatenated dataset that includes three gene regions). The GenBank database reveals a close affinity of the TYP and LON forms to S. japonica and the SHA form to S. cichorioides. The three gene markers used in the present work have different sensitivity for the algal species identification. COI gene was the most discriminant gene marker. However, we have detected instances of interspecific COI recombination reflecting putative historical hybridization events between distantly related algal lineages. The recombinant sequences show highly contrasted level of divergence in the 5'- and 3'- regions of the gene, leading to significantly different tree topologies depending on the gene segment (5'- or 3'-) used for tree reconstruction. Consequently, the 5'-COI "barcoding" region (~ 650 bp) can be misleading for identification purposes, at least in the case of algal species that might have experienced historical hybridization events. CONCLUSION: Taking into account the potential roles of phenotypic plasticity in evolution, we conclude that the TYP and LON forms represent examples of algae phenotypic diversification that enables successful adaptation to contrasting shallow- and deep-water marine environments, while the SHA form is very similar to S. cichorioides and should be considered a different species. Practical applications for algal management and conservation are briefly considered.     

Tree hybridization and genotypic variation drive cryptic speciation of a specialist mite herbivore

Few studies have investigated the roles that plant hybridization and individual plant genotype play in promoting population divergence within arthropod species. Using nrDNA sequence information and reciprocal transfer experiments, we examined how tree cross type (i.e., pure Populus angustifolia and P. angustifolia x P. fremontii F(1) type hybrids) and individual tree genotype influence host race formation in the bud-galling mite Aceria parapopuli. Three main findings emerged: (1) Strong genetic differentiation of mite populations found on pure P. angustifolia and F(1) type hybrids indicates that these mites represent morphologically cryptic species. (2) Within the F(1) type hybrids, population genetic analyses indicate migration among individual trees; however, (3) transfer experiments show that the mites found on heavily infested F(1) type trees perform best on their natal host genotype, suggesting that genetic interactions between mites and their host trees drive population structure, local adaptation, and host race formation. These findings argue that hybridization and genotypic differences in foundation tree species may drive herbivore population structure, and have evolutionary consequences for dependent arthropod species.     

Enhanced fitness and greater herbivore resistance: implications for dandelion invasion in an alpine habitat

Several hypotheses have been proposed to explain the defense strategies of invasive plants in new ranges. In the absence of specialist herbivores, it is believed that invasive plants may allocate fewer resources to resistance and more to growth and reproduction, thus increasing tolerance to damage in the invasive genotypes. In order to test these predictions, we compared both performance (growth and reproduction) and defense strategies (tolerance and resistance) of two populations of Taraxacum officinale, one from the native range in the French Alps, and one from the introduced range in the Chilean Andes. Individuals from the introduced population demonstrated improved reproductive traits relative to those from the native population, although there was no discernible difference in biomass accumulation. Additionally, reduced tolerance was evident in the case of the former; whereas fitness traits of native plants were unaffected by damage, invasive plants reduced growth and seed output by 25 and 30% respectively following damage treatments. Increases in levels of phenols and anthocyanins, produced as a defense response to herbivory, were observed in introduced plants. Our results suggest that reallocation of resources to reproduction may be an important factor favouring invasive success of T. officinale in Chile, and that a higher investment in chemical resistance traits in this population may also be a factor in this regard.     

Sesquiterpene lactone stereochemistry influences herbivore resistance and plant fitness in the field

Background and Aims

Stereochemical variation is widely known to influence the bioactivity of compounds in the context of pharmacology and pesticide science, but our understanding of its importance in mediating plant–herbivore interactions is limited, particularly in field settings. Similarly, sesquiterpene lactones are a broadly distributed class of putative defensive compounds, but little is known about their activities in the field.

Methods

Natural variation in sesquiterpene lactones of the common cocklebur, Xanthium strumarium (Asteraceae), was used in conjunction with a series of common garden experiments to examine relationships between stereochemical variation, herbivore damage and plant fitness.

Key Results

The stereochemistry of sesquiterpene lactone ring junctions helped to explain variation in plant herbivore resistance. Plants producing cis-fused sesquiterpene lactones experienced significantly higher damage than plants producing trans-fused sesquiterpene lactones. Experiments manipulating herbivore damage above and below ambient levels found that herbivore damage was negatively correlated with plant fitness. This pattern translated into significant fitness differences between chemotypes under ambient levels of herbivore attack, but not when attack was experimentally reduced via pesticide.

Conclusions

To our knowledge, this work represents only the second study to examine sesquiterpene lactones as defensive compounds in the field, the first to document herbivore-mediated natural selection on sesquiterpene lactone variation and the first to investigate the ecological significance of the stereochemistry of the lactone ring junction. The results indicate that subtle differences in stereochemistry may be a major determinant of the protective role of secondary metabolites and thus of plant fitness. As stereochemical variation is widespread in many groups of secondary metabolites, these findings suggest the possibility of dynamic evolutionary histories within the Asteraceae and other plant families showing extensive stereochemical variation.     

Induced chemical defenses in a freshwater macrophyte suppress herbivore fitness and the growth of associated microbes

The freshwater macrophyte Cabomba caroliniana induces a chemical defense when attacked by either the crayfish Procambrus clarkii or the snail Pomacea canaliculata. Induction by either consumer lowers the palatability of the plant to both consumers. When offered food ad libitum, snails feeding on non-induced C. caroliniana grew 2.6–2.7 times more than those feeding on induced C. caroliniana. Because snails fed less on induced plants, this could be a behavioral effect (reduced feeding), a physiological effect of the induced metabolites on the consumer, or both. To assess these possibilities, we made artificial diets with lipid extracts of induced versus non-induced C. caroliniana and restricted control snails to consuming only as much as treatment snails consumed. Growth measured as shell diameter was significantly lower on the diet containing extract from induced, as opposed to non-induced, plants; change in snail mass was more variable and showed a similar, but non-significant, trend. Thus, snails may reduce feeding on induced plants to avoid suppression of fitness. The induced defenses also suppressed growth of co-occurring microbes that might attack the plant through herbivore-generated feeding scars. When two bacteria and three fungi isolated from C. caroliniana surfaces were cultured with the lipid extract from induced and non-induced C. caroliniana, both extracts inhibited the microbes, but the induced extract was more potent against three of the five potential pathogens. Thus, induced plant defenses can act against both direct consumers and microbes that might invade the plant indirectly through herbivore-generated wounds.     

To grow and defend: lack of tradeoffs for brown algal phlorotannins

The concept of cost is an integral element of ecological theories, including optimal defense theory, resource availability theory, and growth-differentiation balance theory. Indeed most frameworks that attempt to explain within-plant patterns of secondary metabolites, as well as account for the evolution of induced defenses, presume that defenses are 'costly'. One way in which investigators have sought to quantify the cost of secondary metabolites is to examine growth/defense tradeoffs, which are predicted to occur wherever resources cannot be simultaneously allocated to both growth and defense. However, emerging evidence suggests that these critical assumptions may not be valid for brown algal phlorotannins, compounds that occur throughout the division Phaeophyta and have served as analogs to vascular plant tannins in numerous tests of terrestrial-derived ecological theories in the marine environment. Here we present a model of phlorotannins as metabolites with both primary and secondary roles and argue that apparent trade-offs between algal growth and phlorotannin content are not a reliable indicator for establishing a cost of defense. We suggest the ecological theories which presume that defenses are costly because resources allocated to defense cannot also be allocated to other 'primary' functions are unlikely to accurately predict the striking variations in algal phlorotannin concentrations that are observed in nature.     

Seasonal variation in the antifouling defence of the temperate brown alga Fucus vesiculosus

The important role of marine epibiotic biofilms in the interactions of the host with its environment has been acknowledged recently. Previous studies with the temperate brown macroalga Fucus vesiculosus have identified polar and non-polar compounds recovered from the algal surface that have the potential to control such biofilms. Furthermore, both the fouling pressure and the composition of the epibiotic bacterial communities on this macroalga varied seasonally. The extent to which this reflects a seasonal fluctuation of the fouling control mechanisms of the host is, however, unexplored in an ecological context. The present study investigated seasonal variation in the anti-settlement activity of surface extracts of F. vesiculosus against eight biofilm-forming bacteria isolated from rockweed-dominated habitats, including replication of two populations from two geographically distant sites. The anti-settlement activity at both sites was found to vary temporally, reaching a peak in summer/autumn. Anti-settlement activity also showed a consistent and strong difference between sites throughout the year. This study is the first to report temporal variation of antifouling defence originating from ecologically relevant surface-associated compounds.     

Temporal variation in predation risk: stage-dependency, graded responses and fitness costs in tadpole antipredator defences

Temporal variation in predation risk may be an important determinant of prey antipredator behaviours. According to the risk allocation hypothesis, the strongest antipredator behaviours are expected when periods of high risk are short and infrequent. We tested this prediction in a laboratory experiment where common frog Rana temporaria tadpoles were raised form early larval stages until metamorphosis. We manipulated the time a predatory Aeshna dragonfly larva was present and recorded behavioural responses (activity) of the tadpoles at three different time points during the tadpoles' development. We also investigated how tadpole shape, size and age at metamorphosis were affected by temporal variation in predation risk. We found that during the two first time points activity was always lowest in the constant high-risk situation. However, antipredator response in the two treatments with brief high-risk situation increased as tadpoles developed, and by the third time point, when the tadpoles were close to metamorphosis, activity was as low as in the constant high-risk situation. Exposure to chemical cues of a predation event tended to reduce activity during the first time period, but caused no response later on. Induced morphological changes (deeper tail and shorter relative body length) were graded the response being stronger as the time spent in the proximity of predator increased. Tadpoles in the brief risk and chemical cue treatments showed intermediate responses. Modification of life history was only found in the constant high-risk treatment in which tadpoles had longer larval period and larger metamorphic size. Our results indicate that both behavioural and morphological defences were sensitive to temporal variation in predation risk, but behaviour did not respond in the manner predicted by the risk allocation model. We discuss the roles of concentration of predator chemical cues and prey stage-dependency in determining these responses.     

Induced resistance in mountain birch: defence against leaf-chewing insect guild and herbivore competition

Summary The effect of leaf damage simulating the feeding of early season insect herbivore species, e.g. Epirrita autumnata, to mountain birch, Betula pubescens ssp. tortuosa, on the performance of insect larvae was studied with eleven leaf-chewing sawfly species. I found variation in the results that was due to short- and long-term inducible responses and to the phenology of herbivore species. In general, early and mid-season species were more strongly affected by induced reactions than late-season species. This finding is in accordance with earlier results but I could show that the persistance of induced reactions rather than the influence of timing of damage is responsible for the result. The growth of the larvae of mid-season sawfly species was affected by both short- and long-term induced reactions. This result shows that early season species may escape short-term induced reactions of mountain birch in current year but may not avoid long-term effects. It is supposed that seasonal deterioration of leaf quality either masks the effects of induced defences or late-season species are better adapted to low-quality leaves. Some species show variation in their response to induced defence in different years. This may be due to yearly differences in induced reactions as well as to species-specific responses. Induced defence reactions may play a role in competitive interactions between herbivore species in leaf-chewing guild of mountain birch.     

Rapid experimental shift in host use traits of a polyphagous marine herbivore reveals fitness costs on alternative hosts

The host breadth of any particular herbivore reflects a compromise between evolutionary forces that promote specialism and those that promote polyphagy. Because most terrestrial herbivorous insects specialize, explorations of this evolutionary balance have focused largely on specialist than on polyphagous herbivores. Here, we experimentally tested whether fitness-based tradeoffs in utilizing alternative hosts can be detected within a polyphagous marine herbivore. The marine amphipod Ampithoe longimana occurs on multiple seaweeds year-round (especially the genera Sargassum, Ulva and Hypnea), but is particularly abundant on the diterpene-rich genus Dictyota during warmer summer months. If fitness-based tradeoffs in using these alternative hosts are present, A. longimana may experience fluctuating selection across seasons. To test this possibility, we performed a controlled natural-selection experiment in which amphipods were isolated on Dictyota or a mixed seaweed assemblage that did not include Dictyota. Within 15 weeks (less than five overlapping generations), Dictyota-lines had greater feeding tolerance for Dictyota and its secondary metabolites than did mixed-seaweed-lines. Dictyota-line females reproduced more quickly than did mixed-seaweed-line females on Dictyota, but mixed-seaweed-line juveniles had greater growth on Sargassum and Ulva and higher fecundity on all hosts than did Dictyota-line juveniles. While experimental shifts in preference and performance are likely genetically-mediated, our experimental protocol does not preclude a role for phenotypic plasticity. The presence of a fitness cost to evolving greater preference for Dictyota suggests that fluctuating selection may operate on feeding preference across seasons, but our test of this hypothesis was equivocal. We suggest that one reason that polyphagy persists within A. longimana and potentially other marine grazers is because polyphagy broadens resource use across seasons, and this benefit outweighs the fitness-based costs that can favor specialism. Our results also reinforce the notion that timescales of ecological and evolutionary dynamics can overlap.     

Depth-related variation in epiphytic communities growing on the brown alga Lobophora variegata in a Caribbean coral reef

Lobophora variegata is a dominant macroalga on coral reefs across the Caribbean. Over the last two decades, it has expanded its vertical distribution to both shallow and deep reefs along the leeward coast of the island of Cura?ao, Southern Caribbean. However, the ecological implications of this expansion and the role of L. variegata as a living substratum are poorly known. This study compared epiphytic algal communities on L. variegata blades along two depth transects (6?C40?m). The epiphytic community was diverse with a total of 70 species of which 49 were found directly attached to L. variegata. The epiphytic community varied significantly between blade surface, depth and site. The greatest number of genera per blade was found growing on the underside of the blades regardless of site and depth. Filamentous red algae (e.g. Neosiphonia howei) were commonly found on the upperside of the blades over the whole depth gradient, whereas the underside was mainly colonized by calcifying (e.g. Hydrolithon spp., Jania spp., Amphiroa fragillissima), fleshy red algae (e.g. Champia spp., Gelidiopsis spp., Hypnea spinella) and foliose brown alga (e.g. Dictyota spp.). Anotrichum tenue, a red alga capable of overgrowing corals, was a common epiphyte of both blade surfaces. L. variegata plays an important role as a newly available substratum. Thus, its spread may influence other algal species and studies of benthic macroalgae such as L. variegata should also take into consideration their associated epiphytic algal communities.     

Sterols of Agarum cribosum: desmosterol in a brown alga

The sterol composition of the cold water brown alga Agarum cribosum was determined by GC—MS. Six of the seven sterols found were identified as stigmata-5,(E)-24(28)-dien-3β-ol (fucosterol), 24-methylenecholest-5-en-3β-ol (24-methylenecholesterol), cholest-5-en-3β-ol (cholesterol), 3β-hydroxycholest-5-en-24-one (24-ketocholesterol), 24ξ-stigmasta-5,28-diene-3β,24-diol (saringosterol) and cholesta-5, 24-dien-3β-ol (desmosterol).