Victoria R. Starczak

Hydrodynamic Facilitation of Gregarious Settlement of a Reef-Building Tube Worm

Experiments testing the effects of hydrodynamic processes and chemical cues on substrate selection were conducted with larvae of the marine tube worm Phragmatopoma lapidosa californica. In flume experiments, larvae were presented an array of sand treatments, including two substrates previously shown to induce metamorphosis in this species, under fast and slow flow regimes. Larvae preferentially metamorphosed on the inductive substrates in both flows. Delivery to the array was higher in fast flow because larvae tumbled along the bottom, whereas in slow flow, larvae were observed swimming in the water column. Thus, in addition to chemical cues, behavioral responses to flow conditions may play an important role in larval recruitment to the benthos.

Complexity and simplification in understanding recruitment in benthic populations

Research of complex systems and problems, entities with many dependencies, is often reductionist. The reductionist approach splits systems or problems into different components, and then addresses these components one by one. This approach has been used in the study of recruitment and population dynamics of marine benthic (bottom-dwelling) species. Another approach examines benthic population dynamics by looking at a small set of processes. This approach is statistical or model-oriented. Simplified approaches identify “macroecological” patterns or attempt to identify and model the essential, “first-order” elements of the system. The complexity of the recruitment and population dynamics problems stems from the number of processes that can potentially influence benthic populations, including (1) larval pool dynamics, (2) larval transport, (3) settlement, and (4) post-settlement biotic and abiotic processes, and larval production. Moreover, these processes are non-linear, some interact, and they may operate on disparate scales. This contribution discusses reductionist and simplified approaches to study benthic recruitment and population dynamics of bottom-dwelling marine invertebrates. We first address complexity in two processes known to influence recruitment, larval transport, and post-settlement survival to reproduction, and discuss the difficulty in understanding recruitment by looking at relevant processes individually and in isolation. We then address the simplified approach, which reduces the number of processes and makes the problem manageable. We discuss how simplifications and “broad-brush first-order approaches” may muddle our understanding of recruitment. Lack of empirical determination of the fundamental processes often results in mistaken inferences, and processes and parameters used in some models can bias our view of processes influencing recruitment. We conclude with a discussion on how to reconcile complex and simplified approaches. Although it appears impossible to achieve a full mechanistic understanding of recruitment by studying all components of the problem in isolation, we suggest that knowledge of these components is essential for simplifying and understanding the system beyond probabilistic description and modeling.

Changes in coral reef communities across a natural gradient in seawater pH

Coral reef community responses vary but bioerosion increases under natural ocean acidification. Ocean acidification threatens the survival of coral reef ecosystems worldwide. The negative effects of ocean acidification observed in many laboratory experiments have been seen in studies of naturally low-pH reefs, with little evidence to date for adaptation. Recently, we reported initial data suggesting that low-pH coral communities of the Palau Rock Islands appear healthy despite the extreme conditions in which they live. Here, we build on that observation with a comprehensive statistical analysis of benthic communities across Palau’s natural acidification gradient. Our analysis revealed a shift in coral community composition but no impact of acidification on coral richness, coralline algae abundance, macroalgae cover, coral calcification, or skeletal density. However, coral bioerosion increased 11-fold as pH decreased from the barrier reefs to the Rock Island bays. Indeed, a comparison of the naturally low-pH coral reef systems studied so far revealed increased bioerosion to be the only consistent feature among them, as responses varied across other indices of ecosystem health. Our results imply that whereas community responses may vary, escalation of coral reef bioerosion and acceleration of a shift from net accreting to net eroding reef structures will likely be a global signature of ocean acidification.

Observations of the thermal environment on Red Sea platform reefs: a heat budget analysis

Hydrographic measurements were collected on nine offshore reef platforms in the eastern Red Sea shelf region, north of Jeddah, Saudi Arabia. The data were analyzed for spatial and temporal patterns of temperature variation, and a simple heat budget analysis was performed with the goal of advancing our understanding of the physical processes that control temperature variability on the reef. In 2009 and 2010, temperature variability on Red Sea reef platforms was dominated by diurnal variability. The daily temperature range on the reefs, at times, exceeded 5°C—as large as the annual range of water temperature on the shelf. Additionally, our observations reveal the proximity of distinct thermal microclimates within the bounds of one reef platform. Circulation on the reef flat is largely wave driven. The greatest diurnal variation in water temperature occurs in the center of larger reef flats and on reefs protected from direct wave forcing, while smaller knolls or sites on the edges of the reef flat tend to experience less diurnal temperature variability. We found that both the temporal and spatial variability in water temperature on the reef platforms is well predicted by a heat budget model that includes the transfer of heat at the air–water interface and the advection of heat by currents flowing over the reef. Using this simple model, we predicted the temperature across three different reefs to within 0.4°C on the outer shelf using only information about bathymetry, surface heat flux, and offshore wave conditions.

Divergence between populations of a monogamous polychaete with male parental care: Premating isolation and chromosome variation

Low dispersal and sexual selection are characteristic of the coastal polychaeteNereis acuminata Ehlers 1868 [also known asNereis arenaceodentata Moore 1903 andNereis (Neanthes) caudata Delle Chiaje 1841]. We assessed levels of premating isolation between populations of this polychaete. Four North American populations were used, two from the Atlantic and two from the Pacific. Worms from all sites (1) were collected in 1987 and 1988 from the same habitat type, (2) were morphologically similar and keyed out asN. acuminata, and (3) reproduced monogamously and exhibited male parental care, an extremely rare reproductive mode in marine invertebrates. There was no evidence from 10-min or 36-h trials of premating isolation between the two Pacific populations. Incomplete premating isolation was found between the two Atlantic populations. High aggression and non-pairing occurred in some 10-min trials between males and females. However, in 36-h trials males and females from the two Atlantic populations always paired to mate. Complete premating isolation was found between Atlantic and Pacific populations. During 10-min trials, males and females from different oceans often attacked and then avoided each other, and they never paired to mate. Nor did they pair to mate in longer, 36-h trials. One Pacific and one Atlantic population were compared for tolerance to cold temperature. Pacific individuals were less able to tolerate cold water than Atlantic individuals. Two Atlantic populations studied had karyotypes with 11 pairs of small acrocentric chromosomes (2n=22), while the two Pacific populations had nine pairs of large metacentric or submetacentric chromosomes (2n=18). Such extreme dissimilarity in karyotype was not expected considering the similarity in morphology, habitat, and reproductive mode. Results suggest strongly that the Atlantic and Pacific populations have been allopatric for a long time, and are different species.

Cytochrome P4501A1 expression, polychlorinated biphenyls and hydroxylated metabolites, and adipocyte size of bottlenose dolphins from the Southeast United States

Persistent organic pollutants (POPs) bioaccumulate in blubber of marine mammals. Therefore, it is important to understand the structure and dynamics of blubber layers and how they affect the accumulation of POPs and subsequent biochemical responses. We used established histological and immunohistochemical methods to document the structure of bottlenose dolphin (Tursiops truncatus) blubber and to assess the expression of cytochrome P4501A1 (CYP1A1) in skin-blubber biopsies of dolphins sampled in the waters off Charleston, SC (CHS) (N=38), and Indian River Lagoon, FL (IRL) (N=36). CYP1A1 expression was strongest and most frequent in capillary endothelial cells and was stratified in blubber; the greatest CYP1A1 staining was in the deepest layer. CYP1A1 expression in deep blubber and 2,3,7,8-TCDD Toxic Equivalents measured in the entire blubber were significantly higher in dolphins from CHS as compared to those from IRL. Adipocyte size was associated with the extent of CYP1A1 expression. Male dolphins with smaller adipocytes from CHS and IRL had higher levels of CYP1A1 expression in deep blubber. In CHS females, CYP1A1 expression in vascular endothelial cells varied with reproductive status. CYP1A1 expression in the deep layer was highest in simultaneously pregnant-lactating dolphins, and these dolphins had the smallest adipocytes in deep blubber. In all dolphins, CYP1A1 expression in the deep blubber layer was positively related to concentrations of hydroxylated PCBs (OH-PCBs) in plasma. In summary, redistribution of AHR agonists from blubber into the circulatory system may enhance PCB metabolism and production of OH-PCBs by induction of CYP1A1 in hepatocytes and, possibly, by induction of CYP1A1 in endothelial cells of the deep blubber. The OH-PCBs thus formed have the potential to interfere with thyroid hormone homeostasis.

Non-selective settlement of Mercenaria mercenaria (L.) larvae in short-term, still-water, laboratory experiments

Abstract Sediment selection by settling larvae of the hard clam Mercenaria mercenaria (L.) was determined in 4-h, still-water, laboratory experiments where larvae were given a choice between two highly contrasting sediment treatments: a natural, organic-rich mud, and an abiotic, glass-bead mixture with a grain-size distribution similar to the mud. The experiments were designed to evaluate the effects of intrinsic (larval age) and extrinsic (sea water temperature) factors on sediment selectivity. These specific effects were tested because results of initial experiments designed to replicate those of Butman et. al, where M. mercenaria larvae had selected beads over mud in still water but not in flow, showed no significant selection. In the present study, only five of the 23 experiments conducted showed significant selection and, in all cases, for mud over beads. Larval age and water temperature had no significant effect on the outcome. In the earliest of these experiments, we discovered a problem with larval preservation in mud samples (dissolution of the larval shell due to low pH) that may have resulted in underestimates of the number of larvae settled in mud in Butman et al., thus confounding interpretation of those results. The conclusions of Butman et al. are therefore modified based on results of the experiments presented here: settling M. mercenaria larvae do not select between two extreme sediment treatments in 4-h, still-water, laboratory experiments. In addition, competency tests used here failed to establish a consistent, predictable, precipitous rise in competency for a given batch of M. mercenaria larvae. This may be due to natural, large variation in physiological development within a given larval pool such that a small proportion of competent larvae are available each day over an extended period. Furthermore, the between-experiment variability in selectivity and some results of the competency tests suggest that the duration of these experiments may be too short to document definitive, initial larval settlement. Occasional selection would then reflect continual redistribution of larvae prior to final settlement and metamorphosis.

Cytochrome P450 diversity and induction by gorgonian allelochemicals in the marine gastropod Cyphoma gibbosum

BackgroundIntense consumer pressure strongly affects the structural organization and function of marine ecosystems, while also having a profound effect on the phenotype of both predator and prey. Allelochemicals produced by prey often render their tissues unpalatable or toxic to a majority of potential consumers, yet some marine consumers have evolved resistance to host chemical defenses. A key challenge facing marine ecologists seeking to explain the vast differences in consumer tolerance of dietary allelochemicals is understanding the biochemical and molecular mechanisms underlying diet choice. The ability of marine consumers to tolerate toxin-laden prey may involve the cooperative action of biotransformation enzymes, including the inducible cytochrome P450s (CYPs), which have received little attention in marine invertebrates despite the importance of allelochemicals in their evolution.ResultsHere, we investigated the diversity, transcriptional response, and enzymatic activity of CYPs possibly involved in allelochemical detoxification in the generalist gastropod Cyphoma gibbosum, which feeds exclusively on chemically defended gorgonians. Twelve new genes in CYP family 4 were identified from the digestive gland of C. gibbosum. Laboratory-based feeding studies demonstrated a 2.7- to 5.1-fold induction of Cyphoma CYP4BK and CYP4BL transcripts following dietary exposure to the gorgonian Plexaura homomalla, which contains high concentrations of anti-predatory prostaglandins. Phylogenetic analysis revealed that C. gibbosum CYP4BK and CYP4BL were most closely related to vertebrate CYP4A and CYP4F, which metabolize pathophysiologically important fatty acids, including prostaglandins. Experiments involving heterologous expression of selected allelochemically-responsive C. gibbosum CYP4s indicated a possible role of one or more CYP4BL forms in eicosanoid metabolism. Sequence analysis further demonstrated that Cyphoma CYP4BK/4BL and vertebrate CYP4A/4F forms share identical amino acid residues at key positions within fatty acid substrate recognition sites.ConclusionsThese results demonstrate differential regulation of CYP transcripts in a marine consumer feeding on an allelochemical-rich diet, and significantly advance our understanding of both the adaptive molecular mechanisms that marine consumers use to cope with environmental chemical pressures and the evolutionary history of allelochemical-metabolizing enzymes in the CYP superfamily.

Morphological divergence of Eastern Pacific and Caribbean isopods: effects of a land barrier and the Panama Canal

The Isthmus of Panama rose approximately 3 million years before the present (mybp) and isolated biotas in the tropical eastern Pacific from those in the Caribbean Sea. Populations that were split by the Isthmus and have evolved in allopatry since that time are known as geminates. The surf zone/beach isopod Excirolana braziliensis Richardson was examined between 1984 and 1989 to test the hypothesis that divergence in geminate isopod morphology has occurred, and that geminate divergence is greater than divergence between local populations from the same coastline. Three morphs of Excirolana braziliensis, one in the Caribbean and two in the eastern Pacific, were discovered using numerical taxonomic methods that adjust for body size. The two Pacific morphs have overlapping large-scale distributions, but those morphs are segregated on a smaller scale by beach. We inferred that one Pacific morph and one Caribbean morph were geminates, based on their relative similarity in shape, their geographical ranges, and natural history information about the organisms dispersal capabilities. The origin of the third morph probably predates the Isthmus of Panama, given its relative dissimilarity from the geminate morphs. The presumed geminates differ primarily with respect to the rostrum, antennae and one male reproductive structure. Divergence between geminates is greater than divergence between local populations of any morph along a coastline. Because only one morph occurs in the Caribbean, that region contains less morphological variation than the eastern Pacific, which contains two morphs. There was weak evidence that some introductions may have taken place in the last century from the Caribbean to the Pacific; however, introductions have not masked the pattern of divergence that has developed over millions of years.

Benthic protists and fungi of Mediterranean deep hypsersaline anoxic basin redoxcline sediments

Some of the most extreme marine habitats known are the Mediterranean deep hypersaline anoxic basins (DHABs; water depth ∼3500 m). Brines of DHABs are nearly saturated with salt, leading many to suspect they are uninhabitable for eukaryotes. While diverse bacterial and protistan communities are reported from some DHAB water-column haloclines and brines, the existence and activity of benthic DHAB protists have rarely been explored. Here, we report findings regarding protists and fungi recovered from sediments of three DHAB (Discovery, Urania, L’ Atalante) haloclines, and compare these to communities from sediments underlying normoxic waters of typical Mediterranean salinity. Halocline sediments, where the redoxcline impinges the seafloor, were studied from all three DHABs. Microscopic cell counts suggested that halocline sediments supported denser protist populations than those in adjacent control sediments. Pyrosequencing analysis based on ribosomal RNA detected eukaryotic ribotypes in the halocline sediments from each of the three DHABs, most of which were fungi. Sequences affiliated with Ustilaginomycotina Basidiomycota were the most abundant eukaryotic signatures detected. Benthic communities in these DHABs appeared to differ, as expected, due to differing brine chemistries. Microscopy indicated that only a low proportion of protists appeared to bear associated putative symbionts. In a considerable number of cases, when prokaryotes were associated with a protist, DAPI staining did not reveal presence of any nuclei, suggesting that at least some protists were carcasses inhabited by prokaryotic scavengers.