Carol S. Thornber

Functional properties of the isomorphic biphasic algal life cycle

Many species of marine algae have life cycles that involve multiple separate, free-living phases that frequently differ in ploidy levels. These complex life cycles have received increasing scientific attention over the past few decades, due to their usefulness for both ecological and evolutionary studies. I present a synthesis of our current knowledge of the ecological functioning and evolutionary implications of the isomorphic, biphasic life cycles commonly found in many species of marine algae. There are both costs and benefits to life cycles with 2 morphologically similar but separate, free-living phases that differ in ploidy levels (haploids and diploids). Evolutionary theory predicts that the existence of subtle yet important differences between the phases may be what allows these life cycles to be maintained. Different phases of the same species can vary in abundance, in demographic parameters such as mortality and fecundity, in their physiology, and in their resistance to herbivory. Some taxonomic groups within the red algae have received significant attention toward these issues, while our knowledge of these properties for brown and green algae remains limited.

TISSUE TYPE MATTERS: SELECTIVE HERBIVORY ON DIFFERENT LIFE HISTORY STAGES OF AN ISOMORPHIC ALGA

Selective grazing by herbivores can have large effects on the population dynamics and community structure of primary producers. However, the ecological impacts of within-species herbivore preference for tissues of different phases (e.g., ploidy levels) or reproductive status remain relatively poorly known, especially among algae and other species with free-living haploid (gametophyte) and diploid (sporophyte) phases. We tested for herbivore selectivity among tissue types of the isomorphic (identical haploid and diploid free-living stages) red alga Mazzaella flaccida. Laboratory feeding assays demonstrated that the snail Tegula funebralis exhibited more than a threefold preference for gametophyte reproductive tissue over other tissue types, due to morphological differences. In contrast, the urchin Strongylocentrotus purpuratus did not distinguish as clearly between gametophytes and sporophytes; but it did prefer sporophyte reproductive to nonreproductive tissue, due to differences in water-soluble chemicals. Field surveys of grazer damage on M. flaccida blades were consistent with these laboratory preferences, with more damage found on gametophytes than sporophytes and reproductive than nonreproductive tissues. Differential fecundity can contribute to a skew in relative frequencies of phases in the field, and our results suggest that differential grazing by snails may contribute to this pattern and thus play a role in algal population biology.

Molecular and morphological diversity of Narragansett Bay (RI, USA) Ulva (Ulvales, Chlorophyta) populations

Macroalgal bloom‐forming species occur in coastal systems worldwide. However, due to overlapping morphologies in some taxa, accurate taxonomic assessment and classification of these species can be quite challenging. We investigated the molecular and morphological characteristics of 153 specimens of bloom‐forming Ulva located in and around Narragansett Bay, RI, USA. We analyzed sequences of the nuclear internal transcribed spacer 1 region (ITS1) and the chloroplast‐encoded rbcL; based on the ITS1 data, we grouped the specimens into nine operational taxonomic units (OTUs). Eight of these OTUs have been previously reported to exist, while one is novel. Of the eight OTUs, all shared sequence identity with previously published sequences or differed by less than 1.5% sequence divergence for two molecular markers. Previously, 10 species names were reported for Ulva in Rhode Island (one blade and nine tube‐forming species) based upon morphological classification alone. Of our nine OTUs, three contained blade‐forming specimens (U. lactuca, U. compressa, U. rigida), one OTU had a blade with a tubular stipe, and six contained unbranched and/or branched tubular morphologies (one of these six, U. compressa, had both a blade and a tube morphology). While the three blade‐forming OTUs in Narragansett Bay can frequently be distinguished by careful observations of morphological characteristics, and spatial/temporal distribution, it is much more difficult to distinguish among the tube‐forming specimens based upon morphology or distribution alone. Our data support the molecular species concept for Ulva, and indicate that molecular‐based classifications of Ulva species are critical for proper species identification, and subsequent ecological assessment or mitigation of Ulva blooms.

Invasion of the Red Seaweed Heterosiphonia japonica Spans Biogeographic Provinces in the Western North Atlantic Ocean

The recent invasion of the red alga Heterosiphonia japonica in the western North Atlantic Ocean has provided a unique opportunity to study invasion dynamics across a biogeographical barrier. Native to the western North Pacific Ocean, initial collections in 2007 and 2009 restricted the western North Atlantic range of this invader to Rhode Island, USA. However, through subtidal community surveys, we document the presence of Heterosiphonia in coastal waters from Maine to New York, USA, a distance of more than 700 km. This geographical distribution spans a well-known biogeographical barrier at Cape Cod, Massachusetts. Despite significant differences in subtidal community structure north and south of Cape Cod, Heterosiphonia was found at all but two sites surveyed in both biogeographic provinces, suggesting that this invader is capable of rapid expansion over broad geographic ranges. Across all sites surveyed, Heterosiphonia comprised 14% of the subtidal benthic community. However, average abundances of nearly 80% were found at some locations. As a drifting macrophyte, Heterosiphonia was found as intertidal wrack in abundances of up to 65% of the biomass washed up along beaches surveyed. Our surveys suggest that the high abundance of Heterosiphonia has already led to marked changes in subtidal community structure; we found significantly lower species richness in recipient communities with higher Heterosiphona abundances. Based on temperature and salinity tolerances of the European populations, we believe Heterosiphonia has the potential to invade and alter subtidal communities from Florida to Newfoundland in the western North Atlantic.

Ecological Impacts of Macroalgal Blooms on Salt Marsh Communities

Despite excessive growth of macroalgae in estuarine systems, little research has been done to examine the impacts of increased algal biomass that drifts into nearby salt marshes and accumulates on intertidal flats. The accumulation of macroalgal mats and subsequent decomposition-related releases of limiting nutrients may potentially alter marsh communities and impact multiple trophic levels. We conducted a 2-year in situ study, as well as laboratory mesocosm experiments, to determine the fate of these nutrients and any bottom-up impacts from the blooms on the dominant salt marsh plant (Spartina alterniflora) and herbivores. Mesocosm results showed that macroalgal decomposition had a positive impact on sediment nitrogen concentrations, as well as S. alterniflora growth rates. In contrast, our in situ results suggested that S. alterniflora growth was hindered by the presence of macroalgal mats. From our results, we suggest that macroalgal accumulation and subsequent release of nitrogen during decomposition may be beneficial in nitrogen limited areas. However, as marshes are becoming increasingly eutrophic, releasing lower marsh plants from nitrogen limitation, this accumulation of macroalgal biomass may hinder S. alterniflora growth through smothering and breakage of culms. As macroalgal blooms are predicted to intensify with rising temperatures and increased eutrophication, the ecological impacts associated with these changes need to be continuously monitored in order to preserve these fragile ecosystems.

Sargassum fusiforme Fraction is a Potent and Specific Inhibitor of HIV-1 Fusion and Reverse Transcriptase

Sargassum fusiforme (Harvey) Setchell has been shown to be a highly effective inhibitor of HIV-1 infection. To identify its mechanism of action, we performed bioactivity-guided fractionation on Sargassum fusiforme mixture. Here, we report isolation of a bioactive fraction SP4-2 (S. fusiforme), which at 8 μg/ml inhibited HIV-1 infection by 86.9%, with IC50 value of 3.7 μg. That represents 230-fold enhancement of antiretroviral potency as compared to the whole extract. Inhibition was mediated against both CXCR4 (X4) and CCR5 (R5) tropic HIV-1. Specifically, 10 μg/ml SP4-2 blocked HIV-1 fusion and entry by 53%. This effect was reversed by interaction of SP4-2 with sCD4, suggesting that S. fusiforme inhibits HIV-1 infection by blocking CD4 receptor, which also explained observed inhibition of both X4 and R5-tropic HIV-1. SP4-2 also inhibited HIV-1 replication after virus entry, by directly inhibiting HIV-1 reverse transcriptase (RT) in a dose dependent manner by up to 79%. We conclude that the SP4-2 fraction contains at least two distinct and biologically active molecules, one that inhibits HIV-1 fusion by interacting with CD4 receptor, and another that directly inhibits HIV-1 RT. We propose that S. fusiforme is a lead candidate for anti-HIV-1 drug development.

Abundance and Species Composition Surveys of Macroalgal Blooms in Rhode Island Salt Marshes

Abstract Excessive growth of macroalgae in estuarine systems is becoming increasingly common among coastal communities throughout the world. Despite repeated observations of macroalgae growing or deposited among the stems of lower marsh plants, few studies have quantitatively documented the presence of macroalgae in salt marsh communities. We conducted monthly surveys during 2009 and 2010 to document the species composition and abundance of the macroalgal community, along with associated biological and physical parameters, in 9 Rhode Island salt marshes. Macroalgae were found in every site during each month sampled, with a peak biomass during the fall, reaching densities up to 1500 g/m2 (wet mass). Nearly 80% of the macroalgae was found in the first 2 m of the lower marsh zone. Fucus spp. were dominant throughout the year, accounting for almost 70% of the annual abundance. While several biological parameters were measured in this study that may contribute to macroalgal accumulation, it is likely that a combination of biotic and abiotic factors drive macroalgal accumulation patterns in these systems.

Herbivore impacts on two morphologically similar bloom-forming Ulva species in a eutrophic bay

Herbivore impacts on macrophyte growth vary with the identity of the herbivores and macrophytes, as well as under different abiotic conditions. This interaction is further complicated by anthropogenic alterations to the environment, such as eutrophication. In this study, we utilized in situ herbivore exclusion experiments and mesocosm feeding preference assays to examine the impacts of different herbivores on the growth of two morphologically similar, co-occurring macroalgal bloom Ulva species in a nutrient-rich environment. We found that herbivory had a measurable impact on Ulva biomass, though the rate of consumption rarely surpassed growth for either Ulva species. We determined that the primary herbivores within the blooms were amphipods and mud crabs, and that their effects varied among study sites and months. Our results also confirmed that, even with a diverse suite of consumers, Ulva blooms are capable of escaping herbivore control, particularly early in the growing season when growth rates peak and herbivore activity is limited. Furthermore, our experiments revealed species-specific feeding preferences among herbivores, as well as differences in growth rates and chemistry between the two Ulva species, which likely influence bloom dynamics.

Two invasive herbivores on a shared host: patterns and consequences of phytohormone induction

Herbivore-induced changes in host quality mediate indirect interactions between herbivores. The nature of these indirect interactions can vary depending on the identity of herbivores involved, species-specific induction of defense-signaling pathways, and sequence of attack. However, our understanding of the role of these signaling pathways in the success of multiple exotic herbivores is less known. Eastern hemlock (Tsuga canadensis) is attacked by two invasive herbivores [elongate hemlock scale (EHS; Fiorinia externa) and hemlock woolly adelgid (HWA; Adelges tsugae)] throughout much of its range, but prior attack by EHS is known to deter HWA. The potential role of phytohormones in this interaction is poorly understood. We measured endogenous levels of phytohormones in eastern hemlock in response to attack by these invasive herbivores. We also used exogenous application of methyl jasmonate (MJ) and acibenzolar-S-methyl (ASM), a salicylic acid (SA) pathway elicitor, to test the hypothesis that defense-signaling phytohormones typically induced by herbivores could deter HWA. Resistance to adelgid attack was assessed using a behavioral assay. Adelgid feeding significantly elevated both abscisic acid (ABA) and SA in local tissues, while EHS feeding had no detectable effect on either phytohormone. HWA progrediens and sistens crawlers preferred to settle on ASM-treated foliage. In contrast, HWA crawlers actively avoided settlement on MJ-treated foliage. We suggest that induction of ABA- and SA-signaling pathways, in concert with defense-signaling interference, may aid HWA invasion success, and that defense-signaling interference, induced by exotic competitors, may mediate resistance of native hosts.

Conspecific tolerance and heterospecific competition as mechanisms for overcoming resistance to invasion by an intertidal crab

The success of the invasive Asian shore crab, Hemigrapsus sanguineus, stems partly from its ability to exclude established crab species from preferred rocky and cobble intertidal habitat. Here, we assessed preference and competition for habitat types (cobble vs. sand) for H. sanguineus and two competitor species; the previous invasive green crab, Carcinus maenas, and the native rock crab, Cancer irroratus, in New England. In simple laboratory experiments, we paired similarly sized heterospecifics and conspecifics from each species, and also grouped combinations of C. maenas and H. sanguineus in a series of four-individual sets in order to dissect the outcome of intra- and inter-specific competition at different densities. Individually, all three species preferred cobble substrate. With paired conspecifics, H. sanguineus individuals would cohabitate in cobble, whereas C. maenas and C. irroratus individuals each excluded conspecifics from cobble. In heterospecific pairs, H. sanguineus excluded both C. maenas and C. irroratus from cobble. C. maenas and C. irroratus, were equally likely to exclude the other species, but rarely excluded H. sanguineus. In larger assemblages, H. sanguineus preferentially grouped under cobble, whereas C. maenas were more evenly distributed among habitat types. These observations demonstrate that conspecific tolerance and heterospecific competition can be effective, complementary mechanisms for overcoming invasion resistance. Such mechanisms help explain the well-studied success of H. sanguineus following its introduction into New England coastal habitats, and the resulting exclusion of preexisting crab species.