Life cycle evolution and systematics of Campanulariid hydrozoans

Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy at the Massachusetts Institute of Technology and the Woods Hole Oceanographic Institution September 2004The purpose of this thesis is to study campanulariid life cycle evolution and systematics. The Campanulariidae is a hydrozoan family with many life cycle variations, and provide an excellent model system to study life cycle evolution. Additionally, the unique campanulariid Obelia medusae may have been "re-invented" from ancestors without medusae. Chapter 1 reviews campanulariid life cycles and taxonomy. Chapter 2 presents a phylogeny based on 18S rDNA, calmodulin, L6S rDNA and cytochrome c oxidase I (COI). Ancestral life cycles are reconstructed using parsimony. Medusa loss is common, and Obelia may derive from ancestors with typical medusae. Taxonomic results are discussed in Chapter 3. Bilardia, a nominal campanulariid, appears phylogenetic ally distant, while Bonneviella spp. (Bonneviellidae), are nested within the Campanulariidae. Campanulariid genera are not monophyletic. Orthopyxis integra and elytia gracilis may represent cryptic species, while Obelia longissima may be cosmopolitan. Chapter 4 investigates Obelia geniculata phylogeography. Japanese and North Atlantic 16S rDNA and COI sequences are calibrated against the opening of the Bering Strait. Substitution rates are faster than in anthozoans and comparable to non-cnidarian invertebrates. Comparison of Pacific and Atlantic sequences suggests cryptic species exist. Finally, hydroids in New Brunswick, Canada and Iceland may have survived the last glaciation.Funding for my thesis was provided by WHOI Academic Programs, an NSF PEET grant to Cliff Cunningham (DEB-9978131), WHOI Ocean Ventures Fund, the Society for Integrative and Comparative Biology, WHOI Biology, and the MIT-Italy club

Species–specific crab predation on the hydrozoan clinging jellyfish Gonionemus sp. (Cnidaria, Hydrozoa), subsequent crab mortality, and possible ecological consequences

© The Author(s), 2017. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in PeerJ 5 (2017): e3966, doi:10.7717/peerj.3966.Here we report a unique trophic interaction between the cryptogenic and sometimes highly toxic hydrozoan clinging jellyfish Gonionemus sp. and the spider crab Libinia dubia. We assessed species–specific predation on the Gonionemus medusae by crabs found in eelgrass meadows in Massachusetts, USA. The native spider crab species L. dubia consumed Gonionemus medusae, often enthusiastically, but the invasive green crab Carcinus maenus avoided consumption in all trials. One out of two blue crabs (Callinectes sapidus) also consumed Gonionemus, but this species was too rare in our study system to evaluate further. Libinia crabs could consume up to 30 jellyfish, which was the maximum jellyfish density treatment in our experiments, over a 24-hour period. Gonionemus consumption was associated with Libinia mortality. Spider crab mortality increased with Gonionemus consumption, and 100% of spider crabs tested died within 24 h of consuming jellyfish in our maximum jellyfish density containers. As the numbers of Gonionemus medusae used in our experiments likely underestimate the number of medusae that could be encountered by spider crabs over a 24-hour period in the field, we expect that Gonionemus may be having a negative effect on natural Libinia populations. Furthermore, given that Libinia overlaps in habitat and resource use with Carcinus, which avoids Gonionemus consumption, Carcinus populations could be indirectly benefiting from this unusual crab–jellyfish trophic relationship.This work was supported by the Oak Bluffs Community Preservation Committee under Grant 45908900; Oak Bluffs Community Preservation Committee under Grant 45785700; USGS-WHOI Cooperative Program under Grant 48010601, the Adelaide M. and Charles B. Link Foundation, and the Kathleen M. and Peter E. Naktenis Family Foundation

Diversity and distribution of nearshore barnacle cyprids in southern California through the 2015-16 El Nino

© The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Hagerty, M. L., Reyns, N., Pineda, J., & Govindarajan, A. F. Diversity and distribution of nearshore barnacle cyprids in southern California through the 2015-16 El Nino. Peerj, 7, (2019): e7186, doi: 10.7717/peerj.7186.Abundance, species diversity, and horizontal distributions of barnacle cyprids offshore of La Jolla, southern California were described from May 2014 to August 2016 to determine how the nearshore barnacle larval assemblage changed before, during, and after the 2015–16 El Niño. The entire water column was sampled at five stations located within one km of shore with water depths of 4, 6, 8, 10, and 12 m during 33 cruises that encompassed the time when El Niño conditions impacted the area. Nearshore temperature and thermal stratification was concurrently measured using a CTD. Six identified cyprid species, including Chthamalus fissus, Pollicipes polymerus, Megabalanus rosa, Tetraclita rubescens, Balanus glandula, and B. trigonus, along with four unknown species, were collected in our samples. DNA barcoding was used to confirm identifications in a subset of the larvae. C. fissus was more than eight times more abundant than any other species, and while abundance varied by species, cyprid density was highest for all species except for M. rosa before and after the El Niño event, and lower during the environmental disturbance. There were significant differences in cross-shore distributions among cyprid species, with some located farther offshore than others, along with variability in cross-shore distributions by season. C. fissus cyprids were closest to shore during spring-summer cruises when waters were the most thermally stratified, which supports previous findings that C. fissus cyprids are constrained nearshore when thermal stratification is high. Relative species proportions varied throughout the study, but there was no obvious change in species assemblage or richness associated with El Niño. We speculate that barnacle cyprid species diversity did not increase at our study site during the 2015–16 El Niño, as it has in other areas during previous El Niño Southern Oscillation events, due to the lack of anomalous northward flow throughout the 2015–16 event.Funding for this project was provided by the National Science Foundation under grants OCE-1357290, OCE-1357327, OCE-1630459, and OCE-1630474, with supplemental funding provided by the University of San Diego and Woods Hole Oceanographic Institution. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript

Phylogeographic structure and northward range expansion in the barnacle Chthamalus fragilis

© The Author(s), 2015. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in PeerJ 3 (2015): e926, doi:10.7717/peerj.926.The barnacle Chthamalus fragilis is found along the US Atlantic seaboard historically from the Chesapeake Bay southward, and in the Gulf of Mexico. It appeared in New England circa 1900 coincident with warming temperatures, and is now a conspicuous member of rocky intertidal communities extending through the northern shore of Cape Cod, Massachusetts. The origin of northern C. fragilis is debated. It may have spread to New England from the northern end of its historic range through larval transport by ocean currents, possibly mediated by the construction of piers, marinas, and other anthropogenic structures that provided new hard substrate habitat. Alternatively, it may have been introduced by fouling on ships originating farther south in its historic distribution. Here we examine mitochondrial cytochrome c oxidase I sequence diversity and the distribution of mitochondrial haplotypes of C. fragilis from 11 localities ranging from Cape Cod, to Tampa Bay, Florida. We found significant genetic structure between northern and southern populations. Phylogenetic analysis revealed three well-supported reciprocally monophyletic haplogroups, including one haplogroup that is restricted to New England and Virginia populations. While the distances between clades do not suggest cryptic speciation, selection and dispersal barriers may be driving the observed structure. Our data are consistent with an expansion of C. fragilis from the northern end of its mid-19th century range into Massachusetts.Funding was provided by the Woods Hole Oceanographic Institution in an Independent Study Award to J Pineda and AF Govindarajan, a WHOI summer fellowship to F Bukša, and NSF Biological Oceanography #1029526 to JP Wares

Mitochondrial diversity in Gonionemus (Trachylina:Hydrozoa) and its implications for understanding the origins of clinging jellyfish in the Northwest Atlantic Ocean

© The Author(s), 2017. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in PeerJ 5 (2017): e3205, doi:10.7717/peerj.3205.Determining whether a population is introduced or native to a region can be challenging due to inadequate taxonomy, the presence of cryptic lineages, and poor historical documentation. For taxa with resting stages that bloom episodically, determining origin can be especially challenging as an environmentally-triggered abrupt appearance of the taxa may be confused with an anthropogenic introduction. Here, we assess diversity in mitochondrial cytochrome oxidase I sequences obtained from multiple Atlantic and Pacific locations, and discuss the implications of our findings for understanding the origin of clinging jellyfish Gonionemus in the Northwest Atlantic. Clinging jellyfish are known for clinging to seagrasses and seaweeds, and have complex life cycles that include resting stages. They are especially notorious as some, although not all, populations are associated with severe sting reactions. The worldwide distribution of Gonionemus has been aptly called a “zoogeographic puzzle” and our results refine rather than resolve the puzzle. We find a relatively deep divergence that may indicate cryptic speciation between Gonionemus from the Northeast Pacific and Northwest Pacific/Northwest Atlantic. Within the Northwest Pacific/Northwest Atlantic clade, we find haplotypes unique to each region. We also find one haplotype that is shared between highly toxic Vladivostok-area populations and some Northwest Atlantic populations. Our results are consistent with multiple scenarios that involve both native and anthropogenic processes. We evaluate each scenario and discuss critical directions for future research, including improving the resolution of population genetic structure, identifying possible lineage admixture, and better characterizing and quantifying the toxicity phenotype.This work was supported by the Woods Hole Sea Grant, the Town of Oak Bluffs Community Preservation Committee, the Nantucket Biodiversity Initiative, the Kathleen M. and Peter E. Naktenis Family Foundation, and the Russian Science Foundation (No. 14-50-00034)

Modeling characterization of the vertical and temporal variability of environmental DNA in the mesopelagic ocean

© The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Allan, E. A., DiBenedetto, M. H., Lavery, A. C., Govindarajan, A. F., & Zhang, W. G. Modeling characterization of the vertical and temporal variability of environmental DNA in the mesopelagic ocean. Scientific Reports, 11(1), (2021): 21273, https://doi.org/10.1038/s41598-021-00288-5.Increasingly, researchers are using innovative methods to census marine life, including identification of environmental DNA (eDNA) left behind by organisms in the water column. However, little is understood about how eDNA is distributed in the ocean, given that organisms are mobile and that physical and biological processes can transport eDNA after release from a host. Particularly in the vast mesopelagic ocean where many species vertically migrate hundreds of meters diurnally, it is important to link the location at which eDNA was shed by a host organism to the location at which eDNA was collected in a water sample. Here, we present a one-dimensional mechanistic model to simulate the eDNA vertical distribution after its release and to compare the impact of key biological and physical parameters on the eDNA vertical and temporal distribution. The modeled vertical eDNA profiles allow us to quantify spatial and temporal variability in eDNA concentration and to identify the most important parameters to consider when interpreting eDNA signals. We find that the vertical displacement by advection, dispersion, and settling has limited influence on the eDNA distribution, and the depth at which eDNA is found is generally within tens of meters of the depth at which the eDNA was originally shed from the organism. Thus, using information about representative vertical migration patterns, eDNA concentration variability can be used to answer ecological questions about migrating organisms such as what depths species can be found in the daytime and nighttime and what percentage of individuals within a species diurnally migrate. These findings are critical both to advance the understanding of the vertical distribution of eDNA in the water column and to link eDNA detection to organism presence in the mesopelagic ocean as well as other aquatic environments.This research is part of the Woods Hole Oceanographic Institution’s Ocean Twilight Zone project, funded as part of The Audacious Project housed at TED

Exploring the use of environmental DNA (eDNA) to detect animal taxa in the Mesopelagic Zone

© The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Govindarajan, A. F., Francolini, R. D., Jech, J. M., Lavery, A. C., Llopiz, J. K., Wiebe, P. H., & Zhang, W. Exploring the use of environmental DNA (eDNA) to detect animal taxa in the Mesopelagic Zone. Frontiers in Ecology and Evolution, 9, (2021): 574877, https://doi.org/10.3389/fevo.2021.574877.Animal biodiversity in the ocean’s vast mesopelagic zone is relatively poorly studied due to technological and logistical challenges. Environmental DNA (eDNA) analyses show great promise for efficiently characterizing biodiversity and could provide new insight into the presence of mesopelagic species, including those that are missed by traditional net sampling. Here, we explore the utility of eDNA for identifying animal taxa. We describe the results from an August 2018 cruise in Slope Water off the northeast United States. Samples for eDNA analysis were collected using Niskin bottles during five CTD casts. Sampling depths along each cast were selected based on the presence of biomass as indicated by the shipboard Simrad EK60 echosounder. Metabarcoding of the 18S V9 gene region was used to assess taxonomic diversity. eDNA metabarcoding results were compared with those from net-collected (MOCNESS) plankton samples. We found that the MOCNESS sampling recovered more animal taxa, but the number of taxa detected per liter of water sampled was significantly higher in the eDNA samples. eDNA was especially useful for detecting delicate gelatinous animals which are undersampled by nets. We also detected eDNA changes in community composition with depth, but not with sample collection time (day vs. night). We provide recommendations for applying eDNA-based methods in the mesopelagic including the need for studies enabling interpretation of eDNA signals and improvement of barcode reference databases.This research was part of the Woods Hole Oceanographic Institution’s Ocean Twilight Zone Project, funded as part of The Audacious Project housed at TED. Funding for the NOAA Ship Henry B Bigelow was provided by NOAA’s Office of Marine and Aviation Operations (OMAO)

A crab swarm at an ecological hotspot : patchiness and population density from AUV observations at a coastal, tropical seamount

© The Author(s), 2016. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in PeerJ 4 (2016): e1770, doi:10.7717/peerj.1770.A research cruise to Hannibal Bank, a seamount and an ecological hotspot in the coastal eastern tropical Pacific Ocean off Panama, explored the zonation, biodiversity, and the ecological processes that contribute to the seamount’s elevated biomass. Here we describe the spatial structure of a benthic anomuran red crab population, using submarine video and autonomous underwater vehicle (AUV) photographs. High density aggregations and a swarm of red crabs were associated with a dense turbid layer 4–10 m above the bottom. The high density aggregations were constrained to 355–385 m water depth over the Northwest flank of the seamount, although the crabs also occurred at lower densities in shallower waters (∼280 m) and in another location of the seamount. The crab aggregations occurred in hypoxic water, with oxygen levels of 0.04 ml/l. Barcoding of Hannibal red crabs, and pelagic red crabs sampled in a mass stranding event in 2015 at a beach in San Diego, California, USA, revealed that the Panamanian and the Californian crabs are likely the same species, Pleuroncodes planipes, and these findings represent an extension of the southern endrange of this species. Measurements along a 1.6 km transect revealed three high density aggregations, with the highest density up to 78 crabs/m2, and that the crabs were patchily distributed. Crab density peaked in the middle of the patch, a density structure similar to that of swarming insects.This work was sponsored by a grant from the Dalio Foundation, Inc, through the Woods Hole Oceanographic Institution

Twilight zone observation network: a distributed observation network for sustained, real-time interrogation of the ocean’s twilight zone

© The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Thorrold, S. R., Adams, A., Bucklin, A., Buesseler, K., Fischer, G., Govindarajan, A., Hoagland, P., Jin, D., Lavery, A., Llopez, J., Madin, L., Omand, M., Renaud, P. G., Sosik, H. M., Wiebe, P., Yoerger, D. R., & Zhang, W. Twilight zone observation network: a distributed observation network for sustained, real-time interrogation of the Ocean’s Twilight Zone. Marine Technology Society Journal, 55(3), (2021): 92–93, https://doi.org/10.4031/MTSJ.55.3.46.The ocean's twilight zone (TZ) is a vast, globe-spanning region of the ocean. Home to myriad fishes and invertebrates, mid-water fishes alone may constitute 10 times more biomass than all current ocean wild-caught fisheries combined. Life in the TZ supports ocean food webs and plays a critical role in carbon capture and sequestration. Yet the ecological roles that mesopelagic animals play in the ocean remain enigmatic. This knowledge gap has stymied efforts to determine the effects that extraction of mesopelagic biomass by industrial fisheries, or alterations due to climate shifts, may have on ecosystem services provided by the open ocean. We propose to develop a scalable, distributed observation network to provide sustained interrogation of the TZ in the northwest Atlantic. The network will leverage a “tool-chest” of emerging and enabling technologies including autonomous, unmanned surface and underwater vehicles and swarms of low-cost “smart” floats. Connectivity among in-water assets will allow rapid assimilation of data streams to inform adaptive sampling efforts. The TZ observation network will demonstrate a bold new step towards the goal of continuously observing vast regions of the deep ocean, significantly improving TZ biomass estimates and understanding of the TZ's role in supporting ocean food webs and sequestering carbon.This research is part of the Woods Hole Oceanographic Institution’s Ocean Twilight Zone Project, funded as part of The Audacious Project housed at TED

Mesobot : An Autonomous Underwater Vehicle for Tracking and Sampling Midwater Targets

Mesobot, a new class of autonomous underwater vehicle, will address specific unmet needs for observing slow-moving targets in the midwater ocean. Mesobot will track targets such as zooplankton, fish, and descending particle aggregates using a control system based on stereo cameras and a combination of thrusters and a variable buoyancy system. The vehicle will also be able to collect biogeochemical and environmental DNA (eDNA) samples using a pumped filter sampler