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Showing papers in "The Biological Bulletin in 2003"


Journal ArticleDOI
TL;DR: In an attempt to connect laboratory results to field data and investigate how habitat structure affects agonistic interactions, the nocturnal behavior of two crayfish species was observed by scuba diving and snorkeling in two northern Michigan lakes.
Abstract: Agonistic behavior is a fundamental aspect of ecological theories on resource acquisition and sexual se- lection. Crustaceans are exemplary models for agonistic behavior within the laboratory, but agonistic behavior in natural habitats is often neglected. Laboratory studies do not achieve the same ecological realism as field studies. In an attempt to connect laboratory results to field data and in- vestigate how habitat structure affects agonistic interac- tions, the nocturnal behavior of two crayfish species was observed by scuba diving and snorkeling in two northern Michigan lakes. Intraspecific agonistic interactions were analyzed in three habitats: two food resources—macro- phytes and detritus—and one sheltered habitat. The overall observations reinforce the concept that resources influence agonistic bouts. Fights in the presence of shelters were longer and more intense, suggesting that shelters have a higher perceived value than food resources. Fights in the presence of detritus patches had higher average intensities and ended with more tailflips away from an opponent, suggesting that detritus was a more valuable food resource than macrophytes. In addition, observations of aggressive behavior within a natural setting can add validity to labo- ratory studies. When fights in nature are compared with laboratory fights, those in nature are shorter, less intense, and less likely to end with a tailflip, but do show the fundamental fight dynamics associated with laboratory stud- ies. Extrinsic and intrinsic factors affect intraspecific ag- gression in many ways, and both should always be recog- nized as having the potential to alter agonistic behavior.

195 citations


Journal ArticleDOI
TL;DR: It is demonstrated that the thermal limits of oysters are relatively plastic, and that these limits are correlated with changes in the expression of one family of heat-shock proteins (HSP70), and that the elevated level of HSCs during the summer was associated with moderate, 2–3 °C, increases in the upper thermal limits for survival.
Abstract: Pacific oysters, Crassostrea gigas, living at a range of tidal heights, routinely encounter large seasonal fluctuations in temperature. We demonstrate that the ther- mal limits of oysters are relatively plastic, and that these limits are correlated with changes in the expression of one family of heat-shock proteins (HSP70). Oysters were cul- tured in the intertidal zone, at two tidal heights, and moni- tored for changes in expression of cognate (HSC) and inducible (HSP) heat-shock proteins during the progression from spring through winter. We found that the "control" levels (i.e., prior to laboratory heat shock) of HSC77 and HSC72 are positively correlated with increases in ambient temperature and were significantly higher in August than in January. The elevated level of HSCs during the summer was associated with moderate, 2-3 °C, increases in the upper thermal limits for survival. We measured concomitant in- creases in the threshold temperatures (Ton) required for induction of HSP70. Total hsp70 mRNA expression re- flected the seasonal changes in the expression of inducible but not cognate members of the HSP70 family of proteins. A potential cost of increased Ton in the summer is that there was no extension of the upper thermal limits for survival (i.e., induction of thermotolerance) after sublethal heat shock at temperatures that were sufficient to induce ther- motolerance during the winter months.

176 citations


Journal ArticleDOI
TL;DR: These mats may be direct descendents of the most ancient biological communities in which even oxygenic photosynthesis might have developed and are excellent natural laboratories to help to learn how microbial populations associate to control dynamic biogeochemical gradients.
Abstract: Photosynthetic microbial mats are remarkably complete self-sustaining ecosystems at the millimeter scale, yet they have substantially affected environmental processes on a planetary scale. These mats may be direct descendents of the most ancient biological communities in which even oxygenic photosynthesis might have developed. Photosynthetic mats are excellent natural laboratories to help us to learn how microbial populations associate to control dynamic biogeochemical gradients.

149 citations


Journal ArticleDOI
TL;DR: Members of Symbiodinium, both cultured and in hospite, are haploid, and based on the phylogenetics of the dinoflagellates, haploidy in vegetative cells appears to be an ancestral trait that extends to all 2000 extant species of these important unicellular protists.
Abstract: Microscopic and cytological evidence suggest that many dinoflagellates possess a haploid nuclear phase. However, the ploidy of a number of dinoflagellates remains unknown, and molecular genetic support for haploidy in this group has been lacking. To elucidate the ploidy of symbiotic dinoflagellates belonging to the genus Symbiodinium, we used five polymorphic microsatellites to examine popula- tions harbored by the Caribbean gorgonians Plexaura kuna and Pseudopterogorgia elisabethae;we also studied a series of Symbiodinium cultures. In 690 out of 728 Symbiodinium samples in hospite (95% of the cases) and in all 45 Sym- biodinium cultures, only a single allele was recovered per locus. Statistical testing of the Symbiodinium populations harbored by P. elisabethae revealed that the observed ge- notype frequencies deviate significantly from those ex- pected under Hardy-Weinberg equilibrium. Taken together, our results confirm that, in the vegetative life stage, mem- bers of Symbiodinium, both cultured and in hospite, are haploid. Furthermore, based on the phylogenetics of the dinoflagellates, haploidy in vegetative cells appears to be an ancestral trait that extends to all 2000 extant species of these important unicellular protists.

138 citations


Journal ArticleDOI
TL;DR: Genetic maps observed in this study are longer than the cytogenetic map, possibly because of low marker density, and probably due to deleterious recessive genes.
Abstract: Amplified fragment length polymorphisms (AFLPs), along with some microsatellite and Type I markers, were used for linkage analysis in Crassostrea virginica Gmelin, the eastern oyster. Seventeen AFLP primer combinations were selected for linkage analysis with two parents and their 81 progeny. The 17 primer combinations produced 396 polymorphic markers, and 282 of them were segregating in the two parents. Chi-square analysis indicated that 259 (91.8%) markers segregated in Mendelian ratio, while the other 23 (8.2%) showed significant (P < 0.05) segregation distortion, primarily for homozygote deficiency and probably due to deleterious recessive genes. Moderately dense linkage maps were constructed using 158 and 133 segregating markers (including a few microsatellite and Type I markers) from male and female parents, respectively. The male framework map consisted of 114 markers in 12 linkage groups, covering 647 cM. The female map had 84 markers in 12 linkage groups with a length of 904 cM. The estimated genome length was 858 cM for the male map and 1296 cM for the female map. The observed genome coverage was 84% for the male and female map when all linked markers were considered. Genetic maps observed in this study are longer than the cytogenetic map, possibly because of low marker density.

136 citations


Journal ArticleDOI
TL;DR: This paper summarizes the scientific literature on the capture, collection, and culture of gelatinous zooplankton and incorporates many unpublished methods developed at the Monterey Bay Aquarium in the past 15 years.
Abstract: Gelatinous zooplankton are the least under- stood of all planktonic animal groups. This is partly due to their fragility, which typically precludes the capture of intact specimens with nets or trawls. Specialized tools and techniques have been developed that allow researchers and aquarists to collect intact gelatinous animals at sea and to maintain many of these alive in the laboratory. This paper summarizes the scientific literature on the capture, collec- tion, and culture of gelatinous zooplankton and incorporates many unpublished methods developed at the Monterey Bay Aquarium in the past 15 years.

122 citations


Journal ArticleDOI
TL;DR: Under common conditions in the mid-intertidal zone, Hsp70 levels reflected the different thermal sensitivities of the physiological systems of these two species.
Abstract: Although previous studies have demonstrated that heat-shock protein 70 (Hsp70) can be induced by environmental stress, little is known about natural variation in this response over short time scales. We examined how Hsp70 levels varied over days to weeks in two intertidal snail species of the genus Tegula: Sampling was conducted both under naturally changing environmental conditions and in different vertical zones on a rocky shore. The subtidal to low-intertidal T. brunnea was transplanted into shaded and unshaded mid-intertidal cages to assess temporal variation in Hsps under conditions of increased stress. For comparison, the low to mid-intertidal T. funebralis was transplanted into mid-intertidal cages, within this species' natural zone of occurrence. Snails were sampled every 3 to 4 days for one month, and endogenous levels of two Hsp70-kDa family members (Hsp72 and Hsp74) were quantified using solid-phase immunochemistry. Following periods of midday low tides, levels of Hsps increased greatly in transplanted T. brunnea but not in T. funebralis. Levels of Hsps increased less in T. brunnea transplanted to shaded cages than to unshaded cages, suggesting that prolonged emersion and reduction in feeding time per se are factors that are only mildly stressful. Upregulated levels of Hsps returned to base levels within days. In unmanipulated snails collected from their natural zones, Hsp levels showed little change with thermal variation, indicating that these species did not experience thermally stressful conditions during this study. However, under common conditions in the mid-intertidal zone, Hsp70 levels reflected the different thermal sensitivities of the physiological systems of these two species.

120 citations


Journal ArticleDOI
TL;DR: It is reported here on some experiments that demonstrate that viruses can influence community composition in natural marine communities and the cumulative effect over months or years would be substantial.
Abstract: Bacterial viruses, or bacteriophages, have numerous roles in marine systems. Although they are now considered important agents of mortality of bacteria, a second possible role of regulating bacterial community composition is less well known. The effect on community composition derives from the presumed species-specificity and density-dependence of infection. Although models have described the "kill the winner" hypothesis of such control, there are few observational or experimental demonstrations of this effect in complex natural communities. We report here on some experiments that demonstrate that viruses can influence community composition in natural marine communities. Although the effect is subtle over the time frame suitable for field experiments (days), the cumulative effect over months or years would be substantial. Other virus roles, such as in genetic exchange or microbial evolution, have the potential to be extremely important, but we know very little about them.

102 citations


Journal ArticleDOI
TL;DR: This work has collected small leptocephali from around Sulawesi, Indonesia, and has used species-specific genetic markers to identify them as larvae of Anguilla celebesensis and A. borne-ensis, which provides the first definitive information about the general spawning areas of these tropical eels.
Abstract: The freshwater eels have fascinated biologists because of their spectacular long-distance migrations between their freshwater habitats and their spawning areas far out in the ocean (1, 2, 3). Recent progress on the molecular phylogeny of freshwater eels suggests that they originated in the tropics (4), and information on the reproductive ecology and recruitment of tropical species will provide new insight into the evolution of the spawning migration of the freshwater eels (5, 6). However, the larvae (leptocephali) of the many sympatric tropical species are morphologically similar (7), so they are impossible to identify, and their spawning areas are thus virtually unknown. Recently, however, we have collected small leptocephali from around Sulawesi, Indonesia, and have used species-specific genetic markers to identify them as larvae of Anguilla celebesensis and A. borne-ensis, which provides the first definitive information about the general spawning areas of these tropical eels. Moreover, the discovery of a spawning area of A. celebesensis in Tomini Bay and the presence of small specimens of two species in the Celebes Sea indicate that, in contrast to the long migrations made by temperate eels, tropical eels make much shorter migrations to spawn in areas near their freshwater habitats. This difference in migratory behavior may reflect an evolutionary cline among freshwater eels that extends from tropical to temperate regions.

98 citations


Journal ArticleDOI
TL;DR: The coevolved predator-prey relationship be-tween L. helicina and C. antarctica provides a uniqueopportunity to study the ecological and trophic conse-quences of a depression in primary productivity in the RossSea.
Abstract: BRAD A. SEIBEL* AND HEIDI M. DIERSSEN†Monterey Bay Aquarium Research Institute, Moss Landing, California 95039A significant reduction in phytoplankton biomass in theRoss Sea was reported in the austral summer of 2000–2001,a possible consequence of a disruption in sea-ice retreatdue to the presence of an immense iceberg, B15 (1) (Fig. 1).Our observations in McMurdo Sound suggest temporallyand trophically cascading impacts of that depression inproductivity. Reduced phytoplankton stocks clearly affectedthe pteropod Limacina helicina (Phipps, 1774) (Gastro-poda: Mollusca), an abundant primary consumer in theregion (2, 3), as indicated by depressed metabolic rates in2000–2001. The following season, for the first time onrecord, L. helicina was absent from McMurdo Sound. Manyimportant predators, including whales and fishes, relyheavily on L. helicina for food (3, 4). However, most obvi-ously impacted by its absence was Clione antarctica (Smith,1902), an abundant pteropod mollusc (Gastropoda) thatfeeds exclusively on L. helicina (5). Metabolic rates of C.antarctica were depressed by 50% in 2001–2002. BothL.helicina and C. antarctica are important components ofpolar ecosystems and may be good indicators of overallecosystem “health” in McMurdo Sound and perhaps in theRoss Sea. In this last austral summer, 2002–2003, sea-iceextent was much higher and phytoplankton stocks weredramatically lower than any reported previously, effectspossibly associated with El Nin˜o conditions, and we hypoth-esize that pteropods and their consumers may be furtherimpacted.In the Southern Ocean, phytoplankton production islinked strongly to the seasonal oscillations in the extent ofthe sea ice (6, 7) and survival of higher trophic levels isdependent on reproductive cycles that are synchronous withphytoplankton blooms. This is especially true of the directfood link between L. helicina and C. antarctica. L. helicinalives and feeds in the water column by extending a web ofmucus that traps phytoplankton and, to a lesser extent, smallzooplankton (3). L. helicina is the exclusive food source ofC. antarctica throughout the life cycle, and the two specieshave parallel life histories. They grow in concert, with thepreferred prey size increasing with predator size (3). Suchspecificity within the context of a highly seasonal environ-ment requires precise timing to ensure that predator andprey coexist. The coevolved predator-prey relationship be-tween L. helicina and C. antarctica provides a uniqueopportunity to study the ecological and trophic conse-quences of a depression in primary productivity in the RossSea.A 50% to 75% reduction in phytoplankton biomass, es-timated as chlorophyll a (Chl) concentrations, and highsea-ice cover was observed in December 2000–2001 rela-tive to previous years (Table 1; Fig. 2; 8). A limited bloomdid form by February, but annual primary production wasstill only 60% of the previous year (1). We believe that thereduced phytoplankton stocks in 2000–2001 had pro-nounced impacts on the condition of primary consumers inthe region, causing cascading effects through higher trophiclevels in the following year. This assertion is supported hereby a series of metabolic measurements made on L. helicinaand C. antarctica between 1999 and 2002.Nutritional state is known to be among the primary de-terminants of metabolism in all organisms, including ptero-pods (3), and is especially important in the highly seasonalAntarctic environment (9, 10). Food availability will influ-ence, among other things, the rates of protein synthesis,oxygen consumption, growth, and reproduction (9–11). Wecollected L. helicina and C. antarctica at four samplingstations along Ross Island (Fig. 1) and measured the oxygen

94 citations


Journal ArticleDOI
TL;DR: Experimental data support the current view that mycorrhizal symbioses are often tripartite associations, and demonstrate that during colonization the cellular organization of the two eukaryotes is completely remodeled.
Abstract: This review focuses on mycorrhizas, which are associations between fungi and the roots of 90% of terrestrial plants. These are the most common symbioses in the world; they involve about 6000 species of fungi distributed through all the fungal phyla and about 240,000 species of plants, including forest and crop plants. Thanks to mycorrhizal symbiosis and nutrient exchanges, regulated by complex molecular signals, the plant improves its vegetative growth, while the fungus accomplishes its life cycle. Molecular and cellular analyses demonstrate that during colonization the cellular organization of the two eukaryotes is completely remodeled. For example, in cortical cells, structural modifications involve both the host and the microbiont. Recent studies revealed that in arbuscular mycorrhizas (AM), system complexity is increased by the presence of a third symbiont: a bacterium living inside the fungus. The presence of this resident genome makes the investigation of the molecular dialogues among the symbiotic ...

Journal ArticleDOI
TL;DR: This work isolates phylogenetically diverse protists in order to characterize and compare ion-transporting ATPases from cultured acidophiles with those from neutrophilic counterparts, and predicts that special properties of these ion transporters allow protists to survive in the Rio Tinto.
Abstract: Spain's Rio Tinto, or Red River, an example of an extremely acidic (pH 1.7-2.5) environment with a high metal content, teems with prokaryotic and eukaryotic microbial life. Our recent studies based on small-subunit rRNA genes reveal an unexpectedly high eukaryotic phylogenetic diversity in the river when compared to the relatively low prokaryotic diversity. Protists can therefore thrive in and dominate extremely acidic, heavy-metal-laden environments. Further, because we have discovered protistan acidophiles closely related to neutrophiles, we can hypothesize that the transition from neutral to acidic environments occurs rapidly over geological time scales. How have these organisms adapted to such environments? We are currently exploring the alterations in physiological mechanisms that might allow for growth of eukaryotic microbes at acid extremes. To this end, we are isolating phylogenetically diverse protists in order to characterize and compare ion-transporting ATPases from cultured acidophiles with those from neutrophilic counterparts. We predict that special properties of these ion transporters allow protists to survive in the Rio Tinto.

Journal ArticleDOI
TL;DR: It is predicted that the counterclockwise, gyre-like circulation within the Chesapeake Bay will initially distribute larvae northward along the western side of the DelMarVa peninsula, and eventually to the lower sections of all major subestuaries of the western shore of the Bay.
Abstract: The lack of quantitative data on the environmental tolerances of the early life-history stages of invading species hinders estimation of their dispersal rates and establishment ranges in receptor environments. We present data on salinity tolerance for all stages of the ontogenetic larval development of the invading predatory gastropod Rapana venosa, and we propose that salinity tolerance is the dominant response controlling the potential dispersal (=invasion) range of the species into the estuaries of the Atlantic coast of the United States from the current invading epicenter in the southern Chesapeake Bay. All larval stages exhibit 48-h tolerance to salinities as low as 15 ppt with minimal mortality. Below this salinity, survival grades to lower values. Percentage survival of R. venosa veligers was significantly less at 7 ppt than at any other salinity. There were no differences in percentage survival at salinities greater than 16 ppt. We predict that the counterclockwise, gyre-like circulation within th...

Journal ArticleDOI
TL;DR: The thermotolerance of vent animals dwelling on sulfide chimneys in the Northeast Pacific was determined by maintaining them in pressurized chambers under controlled temperature and chemical conditions, and observations indicated that lethal temperature correlates strongly with distributions observed in nature.
Abstract: Dense biological communities on sulfide structures at deep-sea hydrothermal vents survive in one of Earth’s most extreme environments. The thermotolerance of vent animals dwelling on sulfide chimneys in the Northeast Pacific was determined by maintaining them in pressurized chambers under controlled temperature and chemical conditions. Observations indicated that lethal temperature correlates strongly with distributions observed in nature. One species studied, the alvinellid sulfide wormParalvinella sulfincola, exhibited a thermal limit of 50 ‐56 °C. Since observations of survival under controlled conditions are the only unambiguous means of demonstrating that an animal can tolerate a given environmental condition, the documented thermal limit for metazoan life at hydrothermal vents should be considered to be above 45 °C, but less than 60 °C. Although the biology of hydrothermal vents has been actively investigated over the past 20 years, delineating linkages between the physical environment and the biota has been difficult. Gradients and temporal changes are pronounced. Therefore, to know what conditions a vent organism routinely encounters, measurements would ideally be conducted with spatial resolution at the sub-centimeter level, with temporal resolution over the course of days to weeks, and without modifying fluid flow by the presence of the sensor or submersible. Consequently, investigators are generally cautious in inferring physiological tolerance from

Journal ArticleDOI
TL;DR: Preliminary results on the microbial composition of a laminated community that occurs in a crystallized gypsum-halite matrix in near-saturated salt water indicate the ubiquitous dominance of uncultured organisms of phylogenetic kinds not generally thought to be associated with hypersaline environments.
Abstract: The goal of this project is to describe and understand the organismal composition, structure, and physiology of microbial ecosystems from hypersaline environments. One collection of such ecosystems occurs at North America's largest saltworks, the Exportadora de Sal, in Guerrero Negro, Baja California Sur. There, seawater flows through a series of evaporative basins with an increase in salinity until saturation is reached and halite crystallization begins. Several of these ponds are lined with thick (10 cm) microbial mats that have received some biological study. To determine the nature and extent of diversity of the microbial organisms that constitute these ecosystems, we are conducting a phylogenetic analysis using molecular approaches, based on cloning and sequencing of small subunit (SSU) rRNA genes (16S for Bacteria and Archaea, 18S for Eukarya). In addition, we report preliminary results on the microbial composition of a laminated community that occurs in a crystallized gypsum-halite matrix in near-saturated salt water. Exposure of the interior of these large (kilogram) wet, endoevaporite crystals reveals a multitude of colors: layers of yellow, green, pink, and purple microbiota. To date, analyses of these two environments indicate the ubiquitous dominance of uncultured organisms of phylogenetic kinds not generally thought to be associated with hypersaline environments.

Journal ArticleDOI
TL;DR: This study is the first to show that juvenile zebrafish can recognize and prefer their siblings to unrelated conspecifics based on olfactory cues, and it is shown that kin recognition mechanisms based on learning processes as Tang-Martinez (9) emphasized.
Abstract: Genetic analyses of numerous fish species have shown that shoals formed by larvae often consist of closely related kin (1). Aggregating with kin may be an altruistic trait that evolved through kin selection (2). Individuals would increase their inclusive fitness by sharing the benefits of shoaling among related individuals (3). Laboratory experiments on recognition of kin vs. non-kin groups of Atlantic Salmon (Salmo salar) (4) demonstrated possible advantages: kin groups had fewer aggressive interactions, used a greater proportion of “threat” behavior as opposed to fighting, and subordinates especially had improved growth. The mechanisms by which these kin groups develop and stay separate from each other are not known. The genes of the major histocompatibility complex (MHC) are a source of individual odors released into the water via urine (5). Such pheromones might be involved in olfactory kin recognition. Here, we tested the hypothesis that zebrafish can recognize kin based on olfactory cues. Zebrafish (Danio rerio) live in freshwater streams and rice paddies in the Ganges River of East India, Bangladesh, and Burma. Although this species is widely used as a model in genetic and developmental research, little is known about its natural behavior. Zebrafish spawn up to several hundred eggs at a time, and these develop in the substrate without any parental care. Larvae (G.G. pers. obs.), and sometimes adults, can be observed in shoals (6, 7), but their genetic relatedness is unknown. We observed wild-type juvenile zebrafish, aged 6–8 weeks; the fish were kept in 2.5-1 aquaria under a day/night cycle of 14/10 h and fed on a standard diet of brine shrimp nauplii and dry fish food. Twenty-four hours before an experiment started, 2 separate kin groups consisting of 12 full siblings each were placed into two 9-1 aquaria with standing water. From each kin group, 3 fish were tested in the flume, one at a time, for a total of 6 fish. This procedure was repeated 3 times for a total of 6 kin groups and 18 test animals. Water from each of the two aquaria was used as the two stimuli in an olfactory preference test. Single individuals of either group were used as test fish and were placed into a choice flume (20 cm long 4 cm wide, water level 2.5 cm) that maintained two separate water columns (Fig. 1) (8). Uniform and unidirectional water flow was maintained at a constant rate of 40 ml/min ( 3.5 mm/s). Periodic dye tests showed that the two water columns remained well separated. Prior to each trial, formulated fresh water was run through both channels of the flume for 5 min to allow the subject to acclimate. Each trial consisted of four 3-min periods, during which water from kin and non-kin aquaria was presented on alternate sides of the flume to correct for the possibility of unrelated side bias. Every 10 s, we recorded which side of the flume (A or B, Fig. 1) the fish was swimming on. The number of times each animal was recorded on the side with kin stimulus was expressed as a percentage of the total number of recorded observations (i.e., kin plus non-kin). A score greater than 50% (random distribution) indicated a preference for the kin stimulus; and when the percentages of all the fish were compared using a Wilcoxon matched-pairs signed-ranks (WSR) test, the preference for kin was significant (WSR 45.0, P 0.050) (Fig. 1). Our study is the first to show that juvenile zebrafish can recognize and prefer their siblings to unrelated conspecifics based on olfactory cues. There are two general categories of kin recognition mechanisms, both based on learning processes as Tang-Martinez (9) emphasized. The first (“indirect”) mechanism is based on familiarity, where individuals behave nepotistically to conspecifics with whom they grow up. The second (“direct”) kin recognition mechanism allows individuals to identify even unfamiliar kin. Direct recognition is thought to be based on ‘phenotype matching’, in which an individual must learn cues, either from the phenotypes of close relatives (familial imprinting) (10), or from itself, to form a template for comparison with the phenotype of other individuals. Our results cannot distinguish between these recognition mechanisms.

Journal ArticleDOI
TL;DR: Not all individuals showed the same temporal dynamics of ferritin transport, suggesting that nutrient transfer to oocytes is either not a continuous process, or that among individuals, transfer is not synchronized on short time scales.
Abstract: The mechanism of nutrient transfer from the digestive system to the gonad acini and developing oocytes was investigated in the gonad-intestinal loop system of the queen scallop Pecten maximus L. Ferritin was injected directly into the purged intestine of specimens from the wild. Subsequently, a histochemical reaction and transmission electron microscopy were used to localize ferritin in various cell types. Ferritin was rapidly absorbed by the intestinal epithelium, and then appeared in hemocytes in the surrounding connective tissue. In the hemocytes, ferritin was stored in variously sized inclusions, as well as in the general cytoplasm. In all sections examined for the 12 experimental individuals, hemocytes were always found in association with connective tissue fibers extending from the base of the intestinal epithelium to gonad acini. After 30-min incubation, ferritin appeared inside the acini of all individuals. Ferritin-bearing cells were rarely found in association with male acini or gametes, nor with mature female gametes, but often with developing female gametes. Not all individuals showed the same temporal dynamics of ferritin transport, suggesting that nutrient transfer to oocytes is either not a continuous process, or that among individuals, transfer is not synchronized on short time scales. This is the first demonstration of a pathway of nutrient transfer from the intestine, and more generally the digestive system, to developing oocytes in the Bivalvia.

Journal ArticleDOI
TL;DR: Although colonial invertebrates like P. elisabethae grow through the addition of polyps, branches behave as modules with determinate growth in which branch growth rates were greatest at the time the branch originated and branches seldom grew beyond a length of 8 cm.
Abstract: Growth rates of branches of colonies of the gorgonian Pseudopterogorgia elisabethae were monitored for 2 years on a reef at San Salvador Island, Bahamas. Images of 261 colonies were made at 6-month intervals and colony and branch growth analyzed. Branch growth rates differed between colonies and between the time intervals in which the measurements were made. Colonies developed a plumelike morphology through a pattern of branch origination and determinate growth in which branch growth rates were greatest at the time the branch originated and branches seldom grew beyond a length of 8 cm. A small number of branches had greater growth rates, did not stop growing, and were sites for the origination of subsequent "generations" of branches. The rate of branch origination decreased with each generation of branching, and branch growth rates were lower on larger colonies, leading to determinate colony growth. Although colonial invertebrates like P. elisabethae grow through the addition of polyps, branches behave as modules with determinate growth. Colony form and size is generated by the iterative addition of branches.

Journal ArticleDOI
TL;DR: Data show that an unexpected diversity of microorganisms directly participate in rock weathering at the seafloor, and imply that endolithic microbial communities contribute to rock, mineral, and carbon transformations.
Abstract: The delicate balance of the major global biogeochemical cycles greatly depends on the transformation of Earth materials at or near its surface. The formation and degradation of rocks, minerals, and organic matter are pivotal for the balance, maintenance, and future of many of these cycles. Microorganisms also play a crucial role, determining the transformation rates, pathways, and end products of these processes. While most of Earth’s crust is oceanic rather than terrestrial, few studies have been conducted on ocean crust transformations, particularly those mediated by endolithic (rock-hosted) microbial communities. The biology and geochemistry of deep-sea and sub-seafloor environments are generally more complicated to study than in terrestrial or near-coastal regimes. As a result, fewer, and more targeted, studies usually homing in on specific sites, are most common. We are studying the role of endolithic microorganisms in weathering seafloor crustal materials, including basaltic glass and sulfide minera...

Journal ArticleDOI
TL;DR: Together, exogenous and endogenous factors control emergence of trematode cercariae, mitigating the vagaries of an intertidal environment.
Abstract: Trematode parasites in intertidal estuaries ex- perience constantly varying conditions, with the presence or absence of water potentially limiting larval transport be- tween hosts. Given the short life spans (24 h) of cercariae, emergence timing should be optimized to enhance the prob- ability of successful transmission. In the present study, field measurements and laboratory experiments identified pro- cesses that regulate the emergence of cercariae from their first intermediate snail hosts in an intertidal marsh. Larvae emerged over species-specific temperature ranges, exclu- sively during daylight hours, and only when snails were submerged. The three factors operate over different tempo- ral scales: temperature monthly, light diurnally (24-h pe- riod), and water depth tidally (12-h period). Each stimulus creates a necessary condition for the next, forming a hier- archy of environmental cues. Emergence as the tide floods would favor transport within the estuary, and light may trigger direct (downward or upward) swimming toward host habitats. Abbreviated dispersal would retain asexually re- produced cercariae within the marsh, and local mixing would diversify the gene pool of larvae encysting on sub- sequent hosts. In contrast to the timing of cercarial release, emergence duration was under endogenous control. Dura- tion of emergence decreased from sunrise to sunset, perhaps in response to the diminishing lighted interval as the day progresses. Circadian rhythms that control cercarial emer- gence of freshwater species (including schistosomes) are often set by the activity patterns of subsequent hosts. In this estuary, however, the synchronizing agent is the tides. To-

Journal ArticleDOI
TL;DR: Genomic markers for anaerobic microbial processes in marine sediments reveal the structure of sulfate-reducing, methanogenic, and methane-oxidizing microbial communities (including uncultured members) and open genomic windows into extreme microbial habitats that are analogs for the early Earth and for extraterrestrial microbiota.
Abstract: Genomic markers for anaerobic microbial processes in marine sediments—sulfate reduction, methanogenesis, and anaerobic methane oxidation—reveal the structure of sulfate-reducing, methanogenic, and methane-oxidizing microbial communities (including uncultured members); they allow inferences about the evolution of these ancient microbial pathways; and they open genomic windows into extreme microbial habitats, such as deep subsurface sediments and hydrothermal vents, that are analogs for the early Earth and for extraterrestrial microbiota.

Journal ArticleDOI
TL;DR: Observations on the structure and operation of the arm-tip light organs, the character of the luminous cloud, and how the light they produce is incorporated into behavioral patterns are presented.
Abstract: The archaic, deep-sea cephalopod Vampyroteu- this infernalis occurs in dark, oxygen-poor waters below 600 m off Monterey Bay, California. Living specimens, collected gently with a remotely operated vehicle (ROV) and quickly transported to a laboratory ashore, have re- vealed two hitherto undescribed means of bioluminescent expression for the species. In the first, light is produced by a new type of organ located at the tips of all eight arms. In the second, a viscous fluid containing microscopic luminous particles is released from the arm tips to form a glowing cloud around the animal. Both modes of light production are apparently linked to anti-predation strategies. Use of the tip-lights is readily educed by contact stimuli, while fluid expulsion has a much higher triggering threshold. Coelen- terazine and luciferase are the chemical precursors of light production. This paper presents observations on the struc- ture and operation of the arm-tip light organs, the character of the luminous cloud, and how the light they produce is incorporated into behavioral patterns.

Journal ArticleDOI
TL;DR: Little change was observed in the vigor of the escape response to rapid decreases in visible light over a wide range of adaptation intensities.
Abstract: The copepod Acartia tonsa exhibits a vigorous escape jump in response to rapid decreases in light intensity, such as those produced by the shadow of an object passing above it. In the laboratory, decreases in light intensity were produced using a fiber optic lamp and an electronic shutter to abruptly either nearly eliminate visible light or reduce light intensity to a constant proportion of its original inten- sity. The escape responses of A. tonsa to these rapid de- creases in visible light were recorded on high-speed video using infrared illumination. The speed, acceleration, and direction of movement of the escape response were quan- tified from videotape by using automated motion analysis techniques. A. tonsa typically responds to decreases in light intensity with an escape jump comprising an initial reori- entation followed by multiple power strokes of the swim- ming legs. These escape jumps can result in maximum speeds of over 800 mm s 1 and maximum accelerations of over 200 m s 2 .I nA. tonsa, photically stimulated escape responses differ from hydrodynamically stimulated re- sponses mainly in the longer latencies of photically stimu- lated responses and in the increased number of power strokes, even when the stimulus is near threshold; these factors result in longer escape jumps covering greater dis- tances. The latency of responses of A. tonsa to this photic stimulus ranged from a minimum of about 30 ms to a maximum of more than 150 ms, compared to about 4 ms for hydrodynamically stimulated escape jumps. Average re- sponse latency decreased with increasing light intensity or increasing proportion of light eliminated. Little change was observed in the vigor of the escape response to rapid de- creases in visible light over a wide range of adaptation intensities.

Journal ArticleDOI
TL;DR: The analysis of life-history data suggests a fine tuning of different reproductive traits over the entire life cycle that results in roughly equivalent lifetime fecundity for both species.
Abstract: Analyses of life-history data show that both the size-specific batch fecundities and the age-specific spawning frequencies differ for two halfbeak species, Hemiramphus brasiliensis, the ballyhoo, and H. balao, the balao. Halfbeak ages were determined from sectioned otoliths; histological data was used to describe oocyte development and estimate spawning frequency; and batch fecundity was measured from counts of whole oocytes in final maturation. Hemiramphus brasiliensis lived longer (4 versus 2 years) and had a higher survival rate (14.9% versus 7.5% annually) than H. balao did. Of the two species the larger and longer-lived congener, H. brasiliensis, reached sexual maturity at a larger size (fork length 198 versus 160 mm). The spawning period of age-0 females was strongly related to season, whereas spawning by older females occurred throughout the year. Reproduction by both species peaked during late spring or early summer, and all mature females were spawning daily during April (H. brasiliensis) or June (H. balao). This is the first demonstration of iteroparity for the family Hemiramphidae. H. brasiliensis had a lower batch fecundity (about 1164 versus 3743 hydrated oocytes for a 100-g female) than H. balao did. Such low batch fecundities are typical of the order Beloniformes, but quite different from those of other fishes that live in association with coral reef habitats. H. balao's higher batch fecundity is consistent with the life-history theory that predicts higher numbers of eggs for shorter-lived species; this is possible because H. balao produces smaller hydrated oocytes than H. brasiliensis (modal diameter about 1.6 versus 2.4 mm). The high spawning frequency of Hemiramphus species compensates for their low batch fecundity. The annual fecundity of both species is similar to that of other reef fish species, after adjusting for body size and spawning frequency. The lifetime fecundity of H. balao was very similar to that of H. brasiliensis, after accounting for the differences in survival for each species. This suggests a fine tuning of different reproductive traits over the entire life cycle that results in roughly equivalent lifetime fecundity for both species.

Journal ArticleDOI
TL;DR: Metabolic rates of both species were very similar to previous data for a congener, H. rufescens, suggesting that larval metabolism and energy utilization may be conserved among closely related species that also share similar developmental morphology and feeding modes.
Abstract: An understanding of the biochemical and phys- iological energetics of lecithotrophic development is useful for interpreting patterns of larval development, dispersal potential, and life-history evolution. This study investigated the metabolic rates and use of biochemical reserves in two species of abalone, Haliotis fulgens (the green abalone) and H. sorenseni (the white abalone). Larvae of H. fulgens utilized triacylglycerol as a primary source of endogenous energy reserves for development (50% depletion from egg to metamorphic competence). Amounts of phospholipid re- mained constant, and protein dropped by about 30%. After embryogenesis, larvae of H. fulgens had oxygen consump- tion rates of 81.7 5.9 (SE) pmol larva 1 h 1 at 15 °C through subsequent development. The loss of biochemical reserves fully met the needs of metabolism, as measured by oxygen consumption. Larvae of H. sorenseni were exam- ined during later larval development and were metabolically and biochemically similar to H. fulgens larvae at a compa- rable stage. Metabolic rates of both species were very sim- ilar to previous data for a congener, H. rufescens, suggesting that larval metabolism and energy utilization may be con- served among closely related species that also share similar developmental morphology and feeding modes.

Journal ArticleDOI
TL;DR: Results suggest that E. crispata eats a variety ofulvophytic, coenocytic, and other genera that participate in the slug’s energymetabolism and mucus production, and the persistence of photosynthesis in the endosymbiotic plastids indicatesthat protein turnover must be occurring and that support from the nuclear genome of the slug must be necessary.
Abstract: SIDNEY K. PIERCE*, STEVEN E. MASSEY, JEFFREY J. HANTEN, ANDNICHOLAS E. CURTISDepartment of Biology, University of South Florida, SCA 110, 4202 E. Fowler Ave.,Tampa, Florida 33620The horizontal transfer of functional genes between or-ganisms is the theoretical foundation of the endosymbioticorigin of cellular organelles, as well as the basis of genetictherapies and the technology of genetic modification. With-out doubt, transfer of functional genes is routine betweenprokaryotes (1), has occurred between both mitochondria(2) and chloroplasts (3), and the cell nucleus. In addition,DNA has been transferred from endosymbiotic bacteria intoinsect host cell nuclei (4). However, no direct evidenceexists for the natural transfer of nuclear genes betweenmulticellular organisms. We have recently presented cir-cumstantial and pharmacological evidence that nucleargenes encoding for chloroplast proteins are transferredfrom an alga to an ascoglossan sea slug (5, 6). We nowdemonstrate, using molecular techniques, that such a geneis present in the genomic DNA of the slug.Elysia ( Tridachia) crispata is one of a few species ofelysiid sea slugs that has an intracellular symbiosis of sev-eral months’ duration with chloroplasts acquired from spe-cific, siphonaceous algal food. The slug slits open the algalfilament with its radula and sucks the contents into itsdigestive system. As digestion proceeds, certain cells liningthe digestive diverticula phagocytize the plastids into intra-cellular vacuoles. In some species, the chloroplasts reside intheir vacuole for as long as 8–9 months (5, 6, 7), 3–4months in E. crispata (8, 9). In several elysiid slugs, includ-ing E. crispata, the plastids remain photosynthetically ac-tive, and photosynthetic carbon fixation contributes to avariety of molecules that participate in the slug’s energymetabolism and mucus production (9, 10, 11).Maintenance of a chloroplast’s photosynthetic functionsrequires that a variety of proteins associated with the pho-tosystems turn over, but chloroplast genomes only code fora small fraction of the proteins needed for plastid function(e.g., 11, 12). For example, in chromophytic algae—thefood source of some species of elysiids—the chloroplastgenome encodes only 13% of the plastid proteins (13). Inhigher plants, the genes for as many as 90% of plastidproteins, including many of the photosystem components,are located in the cell nucleus (3). Therefore, the persistenceof photosynthesis in the endosymbiotic plastids indicatesthat protein turnover must be occurring, and that supportfrom the nuclear genome of the slug must be necessary.The algal species providing the plastids in E. crispata(and many other species of elysiid slugs) is unknown andcontroversial. Some reports indicate that E. crispata eats,primarily, species of Caulerpa, especially C. verticellata(14). Others (9) report that E. crispata does not consumeCaulerpa spp. at all, but rather eats other genera, such asBatophora, Bryopsis, Halimeda, and Penicillus. These con-flicting results suggest that E. crispata eats a variety ofulvophytic, coenocytic algae; but whether it retains chloro-plasts from multiple algal species is unknown and is amatter that we are currently investigating. Regardless oftheir origin, the endosymbiotic chloroplasts in E. crispataare unexceptional in that they require substantial proteinsynthesis support from the nucleus. When slugs are incu-bated in

Journal ArticleDOI
TL;DR: A unique multispecies reproductive aggregation located on the Gorda Escarpment, California is described, document some of the highest fish and octopus densities ever reported in the deep sea, and highlight how physical and bathymetric heterogeneity in the environment can result in reproductive hot spots, which may be a critical resource in some deep-sea species.
Abstract: Localized areas of intense biological activity, or hot spots, in the deep sea are infrequent but important features in an otherwise sparsely occupied habitat (1). Hydrothermal vents, methane cold seeps, and the tops of seamounts are well documented areas where dense communities persist for generations (2–5). Reproductive aggregations where conspecifics concentrate for the purposes of spawning or egg brooding could be thought of as transient hot spots. It is likely that they occur in populations with low densities to maximize mate location and increase reproductive success (6). However, only a few deep-sea reproductive aggregations have ever been documented (7–9), demonstrating the paucity of present-day information regarding reproductive behavior of deep-sea animals. In this paper we describe a unique multispecies reproductive aggregation located on the Gorda Escarpment, California. We document some of the highest fish and octopus densities ever reported in the deep sea, with most individuals of both species brooding eggs. We describe the nesting behavior of the blob sculpin, Psychrolutes phrictus, and the egg-brooding behavior of an octopus, Graneledone sp. observed during annual dives of a remotely operated vehicle (ROV) on the Gorda Escarpment. The animals are concentrated at the crest of the local topography and near cold seeps where they may benefit from enhanced current flow and local productivity. These findings provide new information on the reproductive behaviors of deep-sea animals. More importantly, they highlight how physical and bathymetric heterogeneity in the environment can result in reproductive hot spots, which may be a critical resource for reproductive success in some deep-sea species. Fifteen ROV dives were conducted on the Gorda Escarpment and Mendocino Ridge during three visits in August 2000, August 2001, and July 2002 (Fig. 1). The Gorda Escarpment is a submarine plateau offshore of northern California. The Mendocino Ridge extends westward from its northern edge at 40.35° N. The Escarpment’s northern side is characterized by steep topography, frequent rocky outcrops and talus fields, sediment slumps, and drainage channels (10). The depth of investigation ranged from 1300 to 3000 m. Reproductive aggregations of both blob sculpin and octopus were present at Site 1 (Fig. 1). The biomass of P. phrictus alone at this site was equivalent to the average total biomass of fishes on the continental slope. Likewise, the density of Graneledone sp. was considerably greater than previously published estimates (Fig. 2). Eighty-four individuals of P. phrictus and 64 nests (Fig. 3A) were observed. They were present at two sites, with the highest density occurring at Site 1 in both August 2000 and August 2001 (Fig. 1). The fish were found over the steepest topography and at a topographic break between the steep northern side of the ridge and the more gently sloping top (Fig. 4). P. phrictus and associated nests were absent in July 2002. Two hundred and thirty-two individuals of Graneledone sp. (Fig. 3B) were observed across all locations, with the highest densities observed at Site 1 during all three visits (Fig. 1). The octopus co-occurred with the blob sculpin, with 51% of the octopus observed within 5 m of sculpin adults or nests in 2001. Smaller aggregations of brooding blob sculpin and octopus were observed at Site 2. Site 1 (depth 1547–1603 m; dives T208, T349, T448) was Received 14 February 2003; accepted 12 May 2003. * To whom correspondence should be addressed. E-mail: jdrazen@mbari.org Reference: Biol. Bull. 205: 1–7. (August 2003) © 2003 Marine Biological Laboratory

Journal ArticleDOI
TL;DR: The use of computer animated three-dimensional models to analyze mate choice criteria in zebrafi sh is applied to examine the roles played by two visual characteristics in mate selection, and the indifference of the females who had recently laid eggs suggests that females’ interest in males correlates with their reproductive stage.
Abstract: In many species, individuals of both sexes have developed a variety of visual signals and behavioral patterns with which to broadcast their quality as mating partners (1). The complexity of these signals makes it diffi cult to distinguish those that are most important in mate selection. Animated models offer a solution to this problem by allowing for the alteration of single parameters in the complex stimulus presented. In this study, we have tested the use of computer animated three-dimensional models to analyze mate choice criteria in zebrafi sh; we applied this tool to examine the roles played by two visual characteristics in mate selection. Sexually mature wild-type zebrafi sh, aged at least 8 months, were kept in 9-1 aquaria under a day/night cycle of 14/10 h. Subjects were tested in a 50 cm 32 cm tank; a vertical line drawn on the wall of the tank divided it into two equal sections, A and B. The tank was placed between two 17-inch Dell computer monitors on which animated models of swimming zebrafi sh were displayed. The models were created using 3D Studio Max 1.0 (Kinetix) on a Dell Optiplex GXPro computer and a Targa 1000 board for digital/analog conversion of video signals, as described by Rosenthal (2, 3). Before each trial, an individual fi sh was placed in the tank and allowed to acclimate for 5 min. During each trial, the subject was simultaneously shown two different animated stimuli. Each trial consisted of four 5-min viewing periods separated by 1-min intervals during which black covers were gently slid in front of the monitors. Three pairs of stimuli were shown to the subjects: [1] male versus female body shape (both with natural horizontal stripes), [2] vertical versus horizontal stripes (both with female shape), and [3] vertical versus horizontal stripes (both with male shape). The vertical and horizontal stripe patterns had equal amounts of blue coloration. Female-shaped images differed from male-shaped images only in that their bellies were 10% larger in side view. Stimulus pairs [1] and [2] were presented to both male and female subjects, while stimulus pair [3] was presented to female subjects only. In addition, stimulus pair [1] was shown to females who had spawned on the day of the trial. (The females used in all other trials did not spawn on the day of the trial.) The two animated stimuli were alternated between the monitors to balance for side effects. During each viewing period, the location of the fi sh was recorded every 10 s. The percentage of time the subject spent in proximity to each stimulus (presence on side A or B) was calculated and compared using a Wilcoxon matched-pairs signed-ranks (WSR) test. The results and statistical evaluations are shown in Figure 1. Males did not differentiate between the male and female-shaped images but showed a signifi cant preference (19.6%) for the horizontal stripe pattern over the vertical stripe pattern when the images were female-shaped. Female zebrafi sh preferred a male-shaped stimulus over a female-shaped stimulus by 20.3%. However, females that had just spawned eggs on the morning of the trial did not show a preference for either the male or the female shape. Females also showed a signifi cant preference (10.7%) for the horizontal stripe pattern over the vertical stripe pattern when the images were male-shaped, but did not differentiate between stripe patterns when the images were femaleshaped. The preference of females for the male-shaped stimulus over the female-shaped stimulus indicates that belly size alone allows female zebrafi sh to distinguish between sexes. The indifference of the females who had recently laid eggs suggests that females’ interest in males correlates with their reproductive stage. The signifi cant bias of males and females against vertical stripe pattern in the opposite-sex animation may result from selection against mating with heterospecifi cs.

Journal ArticleDOI
TL;DR: The Cryptasterina group of asterinid sea stars in Australasia comprises cryptic species with derived life histories and the presence of a buoyant egg and functional brachiolaria larva would not be expected in an intragonadal brooder and indicate the potential for life-history reversal to a planktonic existence.
Abstract: The Cryptasterina group of asterinid sea stars in Australasia comprises cryptic species with derived life histories. C. pentagona and C. hystera have planktonic and intragonadal larvae, respectively. C. pentagona has the gonochoric, free-spawning mode of reproduction with a planktonic lecithotrophic brachiolaria larva. C. hystera is hermaphroditic with an intragonadal lecithotrophic brachiolaria, and the juveniles emerge through the gonopore. Both species have large lipid-rich buoyant eggs and well-developed brachiolariae. Early juveniles are sustained by maternal nutrients for several weeks while the digestive tract develops. C. hystera was reared in vitro through metamorphosis. Its brachiolariae exhibited the benthic exploration and settlement behavior typical of planktonic larvae, and they attached to the substratum with their brachiolar complex. These behaviors are unlikely to be used in the intragonadal environment. The presence of a buoyant egg and functional brachiolaria larva would not be expected in an intragonadal brooder and indicate the potential for life-history reversal to a planktonic existence. Life-history traits of species in the Cryptasterina group are compared with those of other asterinids in the genus Patiriella with viviparous development. Modifications of life-history traits and pathways associated with evolution of viviparity in the Asterinidae are assessed, and the presence of convergent adaptations and clade-specific features associated with this unusual mode of parental care are examined.

Journal ArticleDOI
TL;DR: Phylogenetic analyses suggested that the short Fe-hydrogenase genes of entamoeba and diplomonads share a common ancestor, while the long Fe-Hydrogenase gene of entamaeba appears to have been laterally transferred from a bacterium.
Abstract: Entamoeba histolytica and Spironucleus barkhanus have genes that encode short iron-dependent hydrogenases (Fe-hydrogenases), even though these protists lack hydrogenosomes. To understand better the biochemistry of the protist Fe-hydrogenases, we prepared a recombinant E. histolytica short Fe-hydrogenase and measured its activity in vitro. A Giardia lamblia gene encoding a short Fe-hydrogenase was identified from shotgun genomic sequences, and RT-PCR showed that cultured entamoebas and giardias transcribe short Fe-hydrogenase mRNAs. A second E. histolytica gene, which encoded a long Fe-hydrogenase, was identified from shotgun genomic sequences. Phylogenetic analyses suggested that the short Fe-hydrogenase genes of entamoeba and diplomonads share a common ancestor, while the long Fe-hydrogenase gene of entamoeba appears to have been laterally transferred from a bacterium. These results are discussed in the context of competing ideas for the origins of genes encoding fermentation enzymes of these protists.