Larval responses to turbulence and temperature in a tidal inlet: Habitat selection by dispersing gastropods?

Author Posting. © Sears Foundation for Marine Research, 2010. This article is posted here by permission of Sears Foundation for Marine Research for personal use, not for redistribution. The definitive version was published in Journal of Marine Research 68 (2010): 153-188, doi:10.1357/002224010793079013.Marine larval dispersal is affected by hydrodynamic transport and larval behavior, but little is known about how behavior affects large-scale patterns of dispersal and recruitment. Intertidal habitats are characterized by strong and variable turbulence relative to shelf and pelagic waters, so larval responses to turbulence may affect both dispersal and habitat selection. This study combined observations and theoretical approaches to model gastropod larval responses to multiple physical variables in a well-mixed tidal inlet. Physical measurements and larvae were collected in July 2004 in Barnstable Harbor, Massachusetts (USA). Physical measurements were incorporated in an advection-diffusion model where larval vertical velocity is a function of turbulence dissipation rate, temperature, and the temperature gradient. Modeled larval distributions were fitted to observed concentration profiles by maximum likelihood to estimate larval behavioral velocity (swimming or sinking) as a function of environmental conditions. These quantitative behavior estimates were used to test hypotheses about behavioral differences among groups and to assess the relative impact of different cues on overall larval behavior. Larvae of five common gastropod species from different coastal habitats reacted most strongly to turbulence but had genus-specific responses to environmental cues. Larvae of a species from tidal inlets (the mud snail Nassarius obsoletus) had near-zero velocities under calmer conditions and sank in strong turbulence. In contrast, larvae from exposed beach habitats (Crepidula spp. and Anachis spp.) sank in weak turbulence and swam up in strong turbulence, with additional responses to temperature and temperature gradient. Larval responses also differed between small and large size classes and between flood and ebb tides. Behavior of mud snail larvae would contribute to retention inside the inlet and near adult habitats, whereas behavior of beach snail larvae would contribute to rapid export from muddy inlets lacking suitable adult habitats.This work was funded by the Woods Hole Oceanographic Institution (WHOI) Coastal Ocean Institute, the WHOI Rinehart Coastal Research Center, the National Science Foundation (NSF OCE- 0326734), NSF and US Office of Naval Research grants to S. Elgar and B. Raubenheimer, and the WHOI Sea Grant (National Oceanic and Atmospheric Administration, Grant No. NA16RG2273, project no. R/O-38-PD). Analyses were completed while HLF was a postdoctoral scholar at Scripps Institution of Oceanography (SIO), supported by the California Current Ecosystem Long-Term Ecological Research program (NSF OCE-0417616) and by SIO funding to P. Franks

Photographic identification guide to larvae at hydrothermal vents

The purpose of this guide is to assist researchers in the identification of larvae of benthic invertebrates at hydrothermal vents. Our work is based on plankton sampling at the East Pacific Rise 9-10°N vent field from 1991-2007, supplemented by benthic collections of juveniles. In addition to images and descriptions of the species, we included frequency data from large-volume plankton pump samples taken between 1998 and 2004 and time-series sediment trap samples from 2004-2005.Funding provided by NSF grants OCE-9619605, OCE-9712233, OCE-0424593 and ATM-0428122 and ChEss Grant #WHOI 1334800

Desperate planktotrophs : decreased settlement selectivity with age in competent eastern oyster Crassostrea virginica larvae

Author Posting. © The Author(s), 2018. This is the author's version of the work. It is posted here under a nonexclusive, irrevocable, paid-up, worldwide license granted to WHOI. It is made available for personal use, not for redistribution. The definitive version was published in Marine Ecology Progress Series 599 (2018): 93-106, doi:10.3354/meps12653.For larvae of benthic marine invertebrate species, settlement from planktonic to benthic life is a critical transition. The “desperate larva” concept describes the tendency of larvae to accept suboptimal settlement habitats as they age. We quantified swimming behavior in planktotrophic larvae of the eastern oyster, Crassostrea virginica, to determine whether settlement behaviors, such as swimming downward and remaining on the bottom, increased with age and whether these ontogenetic changes were more apparent in larvae exposed to suboptimal conditions than to preferred conditions (settlement cue absent or present, respectively). In two experiments, the proportion of competent larvae remaining near the bottom of experimental flasks (indicating settlement) increased with larval age, but only in larvae that were not exposed to the settlement cue. This result is consistent with the hypothesis that larvae encountering suboptimal habitat become “desperate” (i.e. more likely to settle) as they age. Exploratory behaviors, such as upward swimming, meandering, or helices, were expected to decrease with age, especially in the absence of the settlement cue, but this pattern was detected in only one of the five swimming metrics tested (helices in downward swimming larvae). Surprisingly, pre-competent larvae exhibited settlement behavior when exposed to the cue, raising the question of whether a response at this stage would have positive or negative consequences. Acceptance of suboptimal settlement habitats by aging larvae may increase the resilience of a species by allowing populations to persist in variable environmental conditions.Funding was provided by NSF grant OCE-0850419, NOAA Sea Grant NA14OAR4170074, grants from WHOI Coastal Ocean Institute, discretionary WHOI funds, a WHOI Ocean Life Fellowship to LSM, a WHOI Summer Student Fellowship to EH, and a WHOI Postdoctoral Scholarship to KSM

Functional traits provide new insight into recovery and succession at deep-sea hydrothermal vents

© The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Dykman, L. N., Beaulieu, S. E., Mills, S. W., Solow, A. R., & Mullineaux, L. S. Functional traits provide new insight into recovery and succession at deep-sea hydrothermal vents. Ecology, 102(8), (2021): e03418, https://doi.org/10.1002/ecy.3418.Investigation of communities in extreme environments with unique conditions has the potential to broaden or challenge existing theory as to how biological communities assemble and change through succession. Deep-sea hydrothermal vent ecosystems have strong, parallel gradients of nutrients and environmental stress, and present unusual conditions in early succession, in that both nutrient availability and stressors are high. We analyzed the succession of the invertebrate community at 9°50′ N on the East Pacific Rise for 11 yr following an eruption in 2006 in order to test successional theories developed in other ecosystems. We focused on functional traits including body size, external protection, provision of habitat (foundation species), and trophic mode to understand how the unique nutritional and stress conditions influence community composition. In contrast to established theory, large, fast-growing, structure-forming organisms colonized rapidly at vents, while small, asexually reproducing organisms were not abundant until later in succession. Species in early succession had high external protection, as expected in the harsh thermal and chemical conditions after the eruption. Changes in traits related to feeding ecology and dispersal potential over succession agreed with expectations from other ecosystems. We also tracked functional diversity metrics over time to see how they compared to species diversity. While species diversity peaked at 8 yr post-eruption, functional diversity was continuing to increase at 11 yr. Our results indicate that deep-sea hydrothermal vents have distinct successional dynamics due to the high stress and high nutrient conditions in early succession. These findings highlight the importance of extending theory to new systems and considering function to allow comparison between ecosystems with different species and environmental conditions.Funding for L. Dykman, L. Mullineaux, and S. Beaulieu was provided by NSF OCE-1829773. The Synthesis Centre of the German Centre for Integrative Biodiversity Research (sDiv) funded the sFDvent working group and database

Isolating the hydrodynamic triggers of the dive response in eastern oyster larvae

© The Author(s), 2015. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Limnology and Oceanography 60 (2015): 1332–1343, doi:10.1002/lno.10098.Understanding the behavior of larval invertebrates during planktonic and settlement phases remains an open and intriguing problem in larval ecology. Larvae modify their vertical swimming behavior in response to water column cues to feed, avoid predators, and search for settlement sites. The larval eastern oyster (Crassostrea virginica) can descend in the water column via active downward swimming, sinking, or “diving,” which is a flick and retraction of the ciliated velum to propel a transient downward acceleration. Diving may play an important role in active settlement, as diving larvae move rapidly downward in the water column and may regulate their proximity to suitable settlement sites. Alternatively, it may function as a predator-avoidance escape mechanism. We examined potential hydrodynamic triggers to this behavior by observing larval oysters in a grid-stirred turbulence tank. Larval swimming was recorded for two turbulence intensities and flow properties around each larva were measured using particle image velocimetry. The statistics of flow properties likely to be sensed by larvae (fluid acceleration, deformation, vorticity, and angular acceleration) were compared between diving and non-diving larvae. Our analyses showed that diving larvae experienced high average flow accelerations in short time intervals (approximately 1–2 s) prior to dive onset, while accelerations experienced by non-diving larvae were significantly lower. Further, the probability that larvae dove increased with the fluid acceleration they experienced. These results indicate that oyster larvae actively respond to hydrodynamic signals in the local flow field, which has ecological implications for settlement and predator avoidance.This work was supported by NSF grant OCE-0850419, NOAA Sea Grant NA14OAR4170074, grants from the WHOI Coastal Ocean Institute, discretionary WHOI funds, a WHOI Ocean Life Fellowship to LM, and a Grove City College Swezey Fellowship to EA

Larvae from afar colonize deep-sea hydrothermal vents after a catastrophic eruption

Author Posting. © The Authors, 2010. This is the author's version of the work. It is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences of the United States of America 107 (2010): 7829-7834, doi:10.1073/pnas.0913187107.The planktonic larval stage is a critical component of life history in marine benthic species because it confers the ability to disperse, potentially connecting remote populations and leading to colonization of new sites. Larval-mediated connectivity is particularly intriguing in deep-sea hydrothermal vent communities, where the habitat is patchy, transient and often separated by tens or hundreds of kilometers. A recent catastrophic eruption at vents near 9°50’N on the East Pacific Rise created a natural clearance experiment and provided an opportunity to study larval supply in the absence of local source populations. Previous field observations have suggested that established vent populations may retain larvae and be largely self-sustaining. If this hypothesis is correct, the removal of local populations should result in a dramatic change in the flux, and possibly species composition, of settling larvae. Fortuitously, monitoring of larval supply and colonization at the site had been established before the eruption and resumed shortly afterward. We detected a striking change in species composition of larvae and colonists after the eruption, most notably the appearance of the gastropod Ctenopelta porifera, an immigrant from possibly >300 km away, and the disappearance of a suite of species that formerly had been prominent. This switch demonstrates that larval supply can change markedly after removal of local source populations, enabling recolonization via immigrants from distant sites with different species composition. Population connectivity at this site appears to be temporally variable, depending not only on stochasticity in larval supply, but also on the presence of resident populations.Support was provided by NSF grants OCE-969105, OCE-9712233, and OCE-0424953), WHOI grants from DOEI and the Ocean Venture Fund, a NDSEG graduate fellowship to DA, and the WHOI Jannasch Chair for Excellence in Oceanography to LM

Persistent effects of disturbance on larval patterns in the plankton after an eruption on the East Pacific Rise

Author Posting. © The Author(s), 2013. This is the author's version of the work. It is posted here by permission of Inter-Research for personal use, not for redistribution. The definitive version was published in Marine Ecology Progress Series 491 (2013): 67-76, doi:10.3354/meps10463.To predict how benthic communities will respond to disturbance, it is necessary to understand how disturbance affects the planktonic larval supply available to recolonize the area. Deep-sea hydrothermal vent fauna along the East Pacific Rise (EPR) experience frequent local extinctions due to tectonic and magmatic events, but the effects on regional larval abundance and diversity are unknown. We had been monitoring larvae at 9° 50' N on the EPR prior to the 2006 eruption and were able to resume collections shortly afterward. We found that many species that were common before the eruption became significantly less so afterward, whereas a few other species experienced a transient spike in abundance. Surprisingly, overall species richness in the plankton was high 9 mo after the eruption, but then decreased sharply after 1 yr and had not returned to pre-eruption levels after 2 yr. These results suggest that recovery from disturbance may continue to be affected by limited larval supply even several years after a disturbance event. This delay in recovery means that larvae of pioneer species may dominate potential colonists, even after benthic habitats have transitioned to conditions that favor later-successional species. Moreover, the combined effects of natural and anthropogenic disturbance (e.g. mining) would be likely to cause more profound and long-lasting changes than either event alone. Our results indicate that we do not have sufficient data to predict the timing of recovery after disturbance in the deep sea, even in a well-studied vent system.Support was provided by National Science Foundation Grant OCE-0424953 and a Woods Hole Oceanographic Institution grant from the Deep Ocean Exploration Institute

Early exposure of bay scallops (Argopecten irradians) to high CO2 causes a decrease in larval shell growth

© The Author(s), 2013. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in PLoS ONE 8 (2013): e61065, doi:10.1371/journal.pone.0061065.Ocean acidification, characterized by elevated pCO2 and the associated decreases in seawater pH and calcium carbonate saturation state (Ω), has a variable impact on the growth and survival of marine invertebrates. Larval stages are thought to be particularly vulnerable to environmental stressors, and negative impacts of ocean acidification have been seen on fertilization as well as on embryonic, larval, and juvenile development and growth of bivalve molluscs. We investigated the effects of high CO2 exposure (resulting in pH = 7.39, Ωar = 0.74) on the larvae of the bay scallop Argopecten irradians from 12 h to 7 d old, including a switch from high CO2 to ambient CO2 conditions (pH = 7.93, Ωar = 2.26) after 3 d, to assess the possibility of persistent effects of early exposure. The survival of larvae in the high CO2 treatment was consistently lower than the survival of larvae in ambient conditions, and was already significantly lower at 1 d. Likewise, the shell length of larvae in the high CO2 treatment was significantly smaller than larvae in the ambient conditions throughout the experiment and by 7 d, was reduced by 11.5%. This study also demonstrates that the size effects of short-term exposure to high CO2 are still detectable after 7 d of larval development; the shells of larvae exposed to high CO2 for the first 3 d of development and subsequently exposed to ambient CO2 were not significantly different in size at 3 and 7 d than the shells of larvae exposed to high CO2 throughout the experiment.This work was funded by a Woods Hole Oceanographic Institution Interdisciplinary Award to Mullineaux & McCorkle; and awards to Mullineaux & White, to McCorkle, and to Cohen & McCorkle through NOAA (National Oceanic and Admosphereic Administration) Sea Grant #NA10OAR4170083. White was funded through a National Defense Science and Engineering Graduate Fellowship through the American Society for Engineering Education

Ontogenetic changes in larval swimming and orientation of pre-competent sea urchin Arbacia punctulata in turbulence

© The Author(s), 2016. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Journal of Experimental Biology 219 (2016): 1303-1310, doi:10.1242/jeb.129502.Many marine organisms have complex life histories, having sessile adults and relying on the planktonic larvae for dispersal. Larvae swim and disperse in a complex fluid environment and the effect of ambient flow on larval behavior could in turn impact their survival and transport. However, to date, most studies on larvae–flow interactions have focused on competent larvae near settlement. We examined the importance of flow on early larval stages by studying how local flow and ontogeny influence swimming behavior in pre-competent larval sea urchins, Arbacia punctulata. We exposed larval urchins to grid-stirred turbulence and recorded their behavior at two stages (4- and 6-armed plutei) in three turbulence regimes. Using particle image velocimetry to quantify and subtract local flow, we tested the hypothesis that larvae respond to turbulence by increasing swimming speed, and that the increase varies with ontogeny. Swimming speed increased with turbulence for both 4- and 6-armed larvae, but their responses differed in terms of vertical swimming velocity. 4-Armed larvae swam most strongly upward in the unforced flow regime, while 6-armed larvae swam most strongly upward in weakly forced flow. Increased turbulence intensity also decreased the relative time that larvae spent in their typical upright orientation. 6-Armed larvae were tilted more frequently in turbulence compared with 4-armed larvae. This observation suggests that as larvae increase in size and add pairs of arms, they are more likely to be passively re-oriented by moving water, rather than being stabilized (by mechanisms associated with increased mass), potentially leading to differential transport. The positive relationship between swimming speed and larval orientation angle suggests that there was also an active response to tilting in turbulence. Our results highlight the importance of turbulence to planktonic larvae, not just during settlement but also in earlier stages through morphology–flow interactions.This work was supported by the National Science Foundation [OCE-0850419] and the National Oceanic and Atmospheric Administration Sea Grant [NA14OAR4170074]. K.Y.K.C. was supported by the Postdoctoral Scholar Program at the Woods Hole Oceanographic Institution (WHOI), with funding provided by the Coastal Ocean Institute, the Croucher Foundation and the Royal Swedish Academy of Sciences. K.Y.K.C. is currently funded by the Croucher Foundation. Additional funding was provided to L.S.M. through the WHOI Ocean Life Fellowship and discretionary WHOI funds, and to E.J.A. through the faculty sabbatical program at Grove City College

Bacterial group II introns in a deep-sea hydrothermal vent environment

Author Posting. © American Society for Microbiology, 2002. This article is posted here by permission of American Society for Microbiology for personal use, not for redistribution. The definitive version was published in Applied and Environmental Microbiology 68 (2002): 6392-6398, doi:10.1128/AEM.68.12.6392-6398.2002.Group II introns are catalytic RNAs and mobile retrotransposable elements known to be present in the genomes of some nonmarine bacteria and eukaryotic organelles. Here we report the discovery of group II introns in a bacterial mat sample collected from a deep-sea hydrothermal vent near 9°N on the East Pacific Rise. One of the introns was shown to self-splice in vitro. This is the first example of marine bacterial introns from molecular population structure studies of microorganisms that live in the proximity of hydrothermal vents. These types of mobile genetic elements may prove useful in improving our understanding of bacterial genome evolution and may serve as valuable markers in comparative studies of bacterial communities.This research was supported by a WHOI Townsend postdoctoral scholarship to M.P., by National Science Foundation grant OCE-9712233 to L.M., by NIH grant GM31480 and grant I-1211 from the Robert A. Welch Foundation to P.S.P., and by NASA Astrobiology Cooperative Agreement NCC2-1054 and continuing support from the Unger G. Vetlesen Foundation to M.L.S