Diving For Science 2015
Proceedings of the
American Academy of Underwater Sciences
34th Scientific Symposium
Lisa K. Lobel
Editor
Key West, FL
September 28 – October 3, 2015
The American Academy of Underwater Sciences (AAUS) was formed in 1977 and incorporated in
the State of California in 1983 as a 501c6 non-profit corporation. Visit: www.aaus.org.
The AAUS Foundation was incorporated in the State of Alabama in 2012 as a 501.c.3 not-for-profit
organization.
The mission of AAUS is to facilitate the development of safe and productive scientific divers through
education, research, advocacy, and the advancement of standards for scientific diving practices,
certifications, and operations.
Acknowledgements
Heather Fletcher from the AAUS main office deserves tremendous credit for organizing the 2015
American Academy of Underwater Sciences annual meeting and scientific symposium and for
keeping the business of AAUS on track. Appreciation is also extended to Genevieve Dardeau for
assistance in manuscript reviews for this volume. Special thanks go to Kathy Johnston for her original
artwork donations (www.kathyjohnston.com) and Kevin Gurr (http://technologyindepth.com) for his
dive computer donations. Both provide continued support of the AAUS scholarship program. Cover
art by Kathy Johnston.
Major financial support was provided by Divers Alert Network.
Text and images in this publication, including cover and interior designs, are owned either by AAUS,
by contributing authors, or by third parties. Fair use of materials is permitted for personal,
educational, or noncommercial purposes. Users must cite author and source of content, must not alter
or modify copyrighted content, and must comply with all other terms or restrictions that may be
applicable. Users are responsible for securing permission from a rights holder for any other use.
Lobel, L.K. editor. 2015. Diving for Science 2015: Proceedings of the AAUS 34th Scientific
Symposium, September 28- October 3, 2015, Key West, FL. Dauphin Island, AL: American Academy
of Underwater Sciences.
ISBN 978-0-9962343-0-6
Copyright © by the American Academy of Underwater Sciences
Dauphin Island Sea Lab, 101 Bienville Boulevard, Dauphin Island, AL 36528
ii
Table of Contents
Short Abstracts
AN OVERVIEW OF THE HISTORY OF DIVING
Sally E. Bauer………………………………………...……...……………………………………..… 1
CLASSROOM UNDER THE SEA: A WORLD RECORD-SETTING UNDERSEA
EDUCATIONAL MISSION
Bruce E. Cantrell, Jessica N. Fain……………….……...................................................………...… 2
LIFE AFTER LIONFISH: ASSESSING THE SAFETY, SCIENCE AND OPPORTUNITY
OF INVASIVE LIONFISH MANAGEMENT IN BISCAYNE NATIONAL PARK
Megan M. Davenport, Shelby Moneysmith……………………………………….……..….…….…. 3
THE MARINEGEO NETWORK: INTEGRATED ECOLOGICAL OBSERVATORIES
FOR CHANGING MARINE ECOSYSTEMS
J. Emmett Duffy, Ross Whippo……………………………………………………………..…….…. 4
SCIENTIFIC DIVER TRAINING FOR UNDERGRADUATES: EXPERIENTIAL
LEARNING IN COASTAL MARINE SCIENCE AND POLICY
David W. Ginsburg, Karla B. Heidelberg…………………...……………...…………………...…… 5
PROJECT POSEIDON: A 100 DAY UNDERSEA EXPLORATION AND RESEARCH
EXPEDITION AT AQUARIUS REEF BASE
J. R. Guined………………………………………………………………………..…………..….….. 6
SUNKEN SHIPS AND SUBMERGED CAVES: ADVENTURES IN UNDERWATER
ARCHAEOLOGY AT TEXAS STATE UNIVERSITY
Frederick H. Hanselmann ………………..…………………………………………………….…… 7
MOVEMENT PATTERNS OF THE CALIFORNIA TWO SPOT OCTOPUS, OCTOPUS
BIMACULATUS, USING ACOUSTIC TELEMETRY
Jennifer K. Hoffmeister, Kelly M. Voss, Connor White…………………....……………………..… 8
ECOLOGICAL CHARACTERISTICS AND TRENDS IN HEALTH OF ROBUST IVORY
CORAL (OCULINA ROBUSTA) OF THE FLORIDA NATURE COAST
Cole Kolasa ….…………………………….…….…..………………….……..……………...…..….. 9
USE OF DUAL LASER PHOTOGRAMMETRY FOR USE IN MEASURING REEF FISH:
TECHNIQUES, PITFALLS AND LIMITATIONS
Chris Ledford……………………...……………………………..…………….……………………. 10
ECOLOGICAL IMPLICATION OF A NORTHERN RANGE EXPANSION OF BLACK
SEA BASS, CENTROPRISTIS STRIATA
Marissa D. McMahan, Jonathan H. Grabowski……………………….….…….……………….… 11
iii
STEROPHOTOGRAMMETRY IN TEMPERATE MARINE ENVIRONMENTS
Andrew O. M. Mogg, Martin D. J. Sayer……………………………………….……………….… 12
IN SITU STUDIES OF LIMESTONE DISSOLUTION IN A COASTAL SUBMARINE
SPRING
Rachel M. Schweers, James R. Garey………………………..........................................……….…. 13
LIONFISH INVASION IN PANAMA: MULTIAGENCY COLLABORATION CASE
STUDY
Andrew Sellers, Edgardo Ochoa, Yazmin Villareal, Gabriel López Dupuis……….…………..….. 14
DEVELOPING THE NEXT GENERATION OF AQUATIC STEWARDS: THE
NATIONAL ASSOCIATION OF BLACK SCUBA DIVERS FOUNDATION SCIENTIFIC
DIVING PROGRAM
Paul L. Washington Jr., Jay Haigler……………………….……………………….…………..…. 15
BREAKING THROUGH BARRIERS FOR MARINE CONSERVATION
Liv Wheeler, Phil Dustan………………………………………….………………………...……… 16
Extended Abstracts and Full Manuscripts
LOST AT ELBOW REEF: COLLABORATIVE RESEARCH ON STEAMSHIP
SHIPWRECKS IN THE FLORIDA KEYS NATIONAL MARINE SANCTUARY
Jay Haigler, Paul L. Washington Jr., Albert José Jones ……………..……….….…………..…… 17
USING SCIENTIFIC DIVING AS A TOOL TO TELL THE STORY OF HUMAN
HISTORY: BRINGING THE SÃO JOSÉ PAQUETE AFRICA INTO MEMORY
Jay Haigler Paul L. Washington Jr., Kamau Sadiki, Albert José Jones ……………..……...…… 23
DIVING FOR CURES: MAPPING MICROBIAL GENOMICS UNDERWATER
Nasreen S. Haque, Bernie Chowdhury …………..………………….……………………..………. 29
USING DIVERS AND 3D SONAR TECHNOLOGY TO STUDY HISTORIC
SHIPWRECKS IN LAKE MICHIGAN
Kira E. Kaufman…………………………………………………………………….………….….... 40
CHOOSING ORGANISMS FOR MONITORING CONTAMINANT EXPOSURE ON
CORAL REEFS: CASE STUDIES FROM JOHNSTON ATOLL, CENTRAL PACIFIC
OCEAN
Lisa K. Lobel, Phillip S. Lobel……………………………………………………………….……... 48
MILESTONES IN UNDERWATER ICHTHYOLOGY: AN UPDATED HISTORICAL
PERSPECTIVE
Phillip S. Lobel, Lisa K. Lobel…………….…………….………………………………….………. 65
iv
OCTOPUS RUBESCENS’ PREY HANDLING PROCEDURES ARE INFLUENCED BY
BIVALVE SHELL THICKNESS AND ADDUCTOR MUSCLE STRENGTH
Jillian Perron, Alan Verde…………………………..……………………………………….…..…. 78
HEAVY BREATHING: HOW MUCH GAS IS CONSUMED IN A DIVING
EMERGENCY?
Martin D. J. Sayer, Nic Bailey …….…………..…...…………………………………………..…... 95
MAPPING THE 1860 WRECK OF THE U.S. COAST SURVEY VESSEL ROBERT J.
WALKER
Peter F. Straub, Stephen D. Nagiewicz, Vincent Capone, Daniel Lieb, and Steven P. Evert…… 100
v
In: Lobel L.K. ed. Diving for Science 2015.
Proceedings of the American Academy of Underwater Sciences 34th Symposium.
An Overview of the History of Diving
Sally E. Bauer
Florida Keys History of Diving Museum, 82990 Overseas Hwy., Islamorada, FL 33036 USA
[email protected]
Abstract
This presentation provides an historical perspective of the 4500 year old story of the history of
man’s quest to explore under the sea, from the earliest record of a breath hold diver, through
bell divers, early diving machines, the development of the diving helmet, treasure hunting,
one atmosphere diving armor to modern SCUBA. Why and how did early man first venture
under water? The evolution of the equipment to bring air to or along with the diver is
discussed. Highlights will include new, previously unrecognized links in the early progress of
diving as well as ”open bottom” or shallow water diving helmets that were a significant
contribution of South Florida and the Keys to the worldwide history of diving. These helmets
fostered the beginnings of modern marine biology and treasure salvage, underwater
photography and sports diving. Through their extensive collecting and research, Drs. Joe and
Sally Bauer, founded both the Florida Keys History of Diving Museum in Islamorada
(www.DivingMuseum.org) and the International Historical Diving Society. Through these
endeavors, diving history research continues. The Museum is dedicated to collecting,
preserving, displaying and interpreting artifacts, antiques, books, documents, photographs and
oral history relative to the History of Diving and contains one of the largest collections of
diving artifacts in the world. Diving scholars can request access to the Diving History
Research library with approximately 2500 volumes dating from as early as 1535.
Keywords: diving bells, diving helmets, freediving, SCUBA, shallow water helmets, treasure
1
In: Lobel L.K. ed. Diving for Science 2015.
Proceedings of the American Academy of Underwater Sciences 34th Symposium.
Classroom Under the Sea: A World Record-Setting Undersea
Educational Mission
Bruce E. Cantrell*#, Jessica N. Fain*
Mathematics and Sciences, Roane State Community College, 276 Patton Lane, Harriman, TN 37748,
USA
[email protected]
*
co-presenting authors
#
corresponding author
Abstract
On October 3, 2014 Bruce Cantrell and Jessica Fain entered Jules’ Undersea Lodge in Key
Largo, Florida to begin their world record-breaking 73-day “Classroom Under the Sea”
educational mission. They did not resurface until December 15. The primary focus of this
joint mission between Roane State Community College and the Marine Resources
Development Foundation was to produce a weekly live broadcast aimed at middle and high
school students. The goal was to get more young people involved in science and technology
by having experts talk about current events regarding the oceans. These highly successful
broadcasts were available internationally without cost. The second goal of the mission was to
conduct a live college-credit hybrid class originating from the undersea habitat for Roane
State students. The result was that a college-credit class was conducted online in real time
from an undersea habitat to a college campus almost 1,000 miles away. Having a live,
regularly scheduled, long-running weekly broadcast and a complete semester-long college
credit class, both originating from an underwater habitat, had never been done in the history
of marine science or education. The final goal was to break the existing world record for
underwater habitation. The former record of 69 days was set in 1992 in Jules Undersea Lodge,
the same habitat where Bruce and Jessica were living. On Thursday, December 11 at 11:28
am Bruce and Jessica established a new world record. A youth-oriented “Lunch with the
Aquanaut” program was also conducted on the weekends. SCUBA certified young people
would dive to the habitat and have lunch while learning first-hand about underwater
habitation. Live Skype sessions and interviews were regularly held with schools, media, and
other organizations from around the world. Classroom Under the Sea mission media coverage
has appeared in over 40 countries.
Keywords: coral restoration, invasive species, saturation diving, STEM, underwater
archeology
2
In: Lobel L.K. ed. Diving for Science 2015.
Proceedings of the American Academy of Underwater Sciences 34th Symposium.
Life After Lionfish: Assessing the Safety, Science, and Opportunity
of Invasive Lionfish Management in Biscayne National Park
Megan M. Davenport1, 2*, Shelby Moneysmith2
1
University of Miami, Department of Marine Biology and Ecology, 4600 Rickenbacker Causeway, Miami, FL
33149, USA
2
Biscayne National Park, 9700 SW 328th St, Homestead, FL 33033, USA
[email protected]
*
presenting and corresponding author
Abstract
Situated between Miami and Key Largo, Biscayne National Park covers an area of 173,000
acres and is 95% underwater. The Park is home to 21 federally listed species and includes
coral reef, seagrass, mangrove, and island ecosystems. Invasive lionfish (Pterois volitans)
were first observed in 2009 and have since increased rapidly in both size and numbers in the
Park, posing a threat to native resources. Management actions, recommended in a National
Park-wide Lionfish Response Plan, include continual collection and removal of the species.
Since management efforts began in 2010, BNP has collected over 4500 lionfish specimens.
An agreement between the National Park Service and University of Miami’s (UM)
Cooperative Ecosystem Studies Unit has allowed seven NPS Blue Card Divers and six
University of Miami scientific divers to devote more than 1500 hours to the collection,
removal, and research of lionfish. The lionfish invasion has encouraged a rapid increase in the
number, variety, and complexity of dives completed by Park staff and University of Miami
scientific divers. This paper assesses the changes in the Biscayne National Park dive program
since the lionfish invasion began, including the agreement between NPS and UM which
allows cooperation with an increasing number of UM research divers, and presents case
studies of the science opportunities, which have resulted from these changes.
Keywords: invasive lionfish, National Park Service, resource management
3
In: Lobel L.K. ed. Diving for Science 2015.
Proceedings of the American Academy of Underwater Sciences 34th Symposium.
The MarineGEO Network: Integrated Ecological Observatories for
Changing Marine Ecosystems
J. Emmett Duffy1, 2, Ross Whippo2*
1
Tennenbaum Marine Observatories Network, Smithsonian Institution, PO Box 37012, Washington DC 200137012, USA
2
Smithsonian Environmental Research Center, 647 Contees Wharf Rd., Edgewater, MD 21037, USA
[email protected]
*
presenting author
Abstract
The ocean dominates the Earth’s surface and plays diverse and critical roles in the planet’s
physical, chemical, and biological processes. However, many fundamental gaps exist in our
knowledge about the structure and function of marine ecosystems. On land, networks have
formed that undertake coordinated measurements and experiments across sites to answer
questions about spatial and temporal changes in biological processes. Remarkably, no such
programs exist for the ocean. Instead, scattered around the world are a multitude of local-toregional marine research efforts, which are largely unconnected and span a diverse range of
topics, with different goals, and often using different methodologies. MarineGEO seeks to
address this critical gap by implementing a coordinated program of standardized biological
measures and experiments in coastal regions across a global network of marine sites. The
most important aspects of the MarineGEO design are (1) the application of standardized
measurements and experiments, (2) the replication of these measurements and experiments
through time to detect meaningful long-term changes in marine ecosystems, (3) the evaluation
of mechanisms that drive the structure, change, and function of marine ecosystems, and (4)
the comparisons of these measurements across space to understand patterns of global
variation. MarineGEO is designed explicitly as a collaborative program that seeks to build
long-term strategic partnerships with government agencies, universities, NGOs, other
organizations, and individual scientists across the globe to realize its full potential. All
MarineGEO sites will implement a set of core measures, which are replicated in space and
repeated through time. More broadly, MarineGEO will provide an increasingly valuable
framework over time, attracting many independently-funded research projects that can benefit
from, leverage, and extend our understanding across network sites. The unique, long-term,
and global strategy for measurements and experiments gives MarineGEO the power to
address big picture questions about biodiversity, human impacts, and drivers of change only
previously attempted on smaller local scales in the ocean.
Keywords: biodiversity, coordinated experiments, long-term monitoring, nearshore habitat
4
In: Lobel L.K. ed. Diving for Science 2015.
Proceedings of the American Academy of Underwater Sciences 34th Symposium.
Scientific Diver Training for Undergraduates: Experiential Learning in
Coastal Marine Science and Policy
David W. Ginsburg*, Karla B. Heidelberg
University of Southern California, Environmental Studies Program, Los Angeles, CA 90089, USA
[email protected]
*
presenting and corresponding author
Abstract
The USC Environmental Studies Program uses experiential learning and mobile technology
tools in remote field locations such as the Caroline Islands in the western Pacific Ocean.
Undergraduates are trained as scientific divers then immediately use this new skill in the
Republic of Palau to study the impacts of development on coral reef environments. Over the
past six years, more than 130 undergraduates have participated in a long-term ecological
monitoring project to assess the status of fishery resources in and around coastal marine
conservation areas in partnership with the Koror State Government and local scientists.
Unlike teaching within a traditional classroom, experiential learning allows for more learners
to be successful by increasing the pedagogical approaches to the material. Students
understand topics more fully by actively engaging in a field activity rather than by only
reading about a concept. Compared to a traditional course, field programs are conducted over
a three-week period. Students develop a research strategy on a given topic and write technical
blog posts targeted towards a non-expert audience. In the field, each student is required to not
only incorporate the primary literature related to their topic, but also integrate their collective
field experience into a short video and reflective blog. The scientific diving and research skills
our students learn provide an important boost in advancing their professional and academic
careers, as well as increase their ability to communicate with both specialized and general
audiences.
Keywords: undergraduate research, experiential learning, long-term monitoring
5
In: Lobel L.K. ed. Diving for Science 2015.
Proceedings of the American Academy of Underwater Sciences 34th Symposium.
Project Poseidon: A 100 Day Undersea Exploration and Research
Expedition at Aquarius Reef Base
Jamie R. Guined1, 2
1
2
SeaSpace Exploration & Research Society, 191 Smokehouse Rd., Cordele, GA 31015, USA
Project PoSSUM, 1830 22nd St. Suite 6, Boulder, CO, 80302, USA
[email protected]
[email protected]
Abstract
Project Poseidon is a proposed 100-day in situ scientific undersea expedition of the SeaSpace
Exploration & Research Society’s SeaSpace Research Institute. The mission crew will be
comprised of a team of highly-skilled professionals with cross-disciplinary backgrounds, each
accomplished in their respective area of expertise. This will be the first long-duration
undersea mission (>90 days) in the history of undersea human exploration and habitation, and
if successful, will surpass multiple world records. The expedition will take place at Aquarius
Reef Base, managed by Florida International University, in the Florida Keys. The two
overarching objectives of the expedition are to conduct cross-disciplinary research across
multiple, yet complementary, fields of study, and to effectively communicate and disseminate
the mission’s scientific findings through a comprehensive education and public outreach
program. Expedition research activities will span the fields of marine biology, health &
human performance, engineering, and geospatial imaging, and will also incorporate space
analog research activities. The proposed expedition research will be conducted in
collaboration with academic, government, and/or commercial and private industry. Research
activities for the first ~60 days will focus on human health, performance, and physiology in a
confined space, extreme space analog environment. Notable research projects include:
seafloor extravehicular activity functional task assessment, evaluation of candidate
physiological monitoring system technologies for monitoring crew health and performance,
changes in crew health and performance during a 100-day undersea space analog mission,
Google Earth as an aide for identifying key seafloor topography during seafloor
extravehicular activity, viability of an integrated exercise countermeasures and human health
program in the confined space of an undersea habitat, and the use of remotely operated
vehicle technology for seafloor extravehicular activity reconnaissance and planning.
Keywords: conservation, health, human performance, physiology, seaspace, space analog
6
In: Lobel L.K. ed. Diving for Science 2015.
Proceedings of the American Academy of Underwater Sciences 34th Symposium.
Sunken Ships and Submerged Caves: Adventures in Underwater
Archaeology at Texas State University
Frederick H. Hanselmann
The Meadows Center for Water and the Environment at Texas State University, 601 University Dr., San
Marcos, TX 78666 USA
[email protected]
Abstract
The Underwater Archaeology and Exploration Initiative at Texas State University's Meadows
Center for Water and the Environment seeks to make physical connections with our past and
to uncover stories that have been lost to us over time. The initiative focuses on the
archaeological exploration of submerged prehistoric sites and the search for the lost ships of
famous privateers, pirates, and the colonial Spanish, from inside underwater caves to a mile
deep in the ocean. Prehistoric underwater archaeological efforts include the Spring Lake site
on campus, prehistoric sites now submerged offshore, and submerged caves and
caverns. Maritime archaeological efforts entail the search for, documentation of, and
excavation of shipwrecks that belonged to colonial Spanish, 18th century maritime conflict
and naval engagement, 17th and 19th century pirates and privateers, and anything else found
throughout the course of the explorations in the Caribbean. The initiative also involves best
practices in the management of underwater cultural heritage, capacity-building in less
developed countries, conservation of aquatic resources, and sustainable economic
development.
Keywords: shipwrecks, maritime archaeology, submerged archaeological sites
7
In: Lobel L.K. ed. Diving for Science 2015.
Proceedings of the American Academy of Underwater Sciences 34th Symposium.
Movement Patterns of the California Two Spot Octopus, Octopus
bimaculatus, Using Acoustic Telemetry
Jennifer K. Hofmeister1*, Kelley M. Voss2, Connor White3
1
Department of Integrative Biology, 3040 Valley Life Sciences Bldg #3140, UC Berkeley, CA, 94720, USA
[email protected]
2
Department of Environmental Science, Alaska Pacific University, Anchorage, AK 99508
3
Department of Biological Sciences, CSU Long Beach, Long Beach, CA 90840
*
presenting and corresponding author
Abstract
Octopuses have significant ecological roles and predatory impacts on prey populations, yet
their movement and activity patterns are very rarely included in studies of habitat selection
and usage. During August 2014 on Catalina Island, CA, nine Octopus bimaculatus were
caught on SCUBA and tagged with VEMCO V9-2L continuous transmitters. Of the nine tags,
six stayed on for the duration of the tags’ battery lives; two tags fell off immediately, and one
fell off after five days. Six of the octopuses were actively tracked for a 24 h period, and daily
GPS locations were recorded for all individuals. Octopus bimaculatus is a very mobile
octopus compared to other octopus species. Octopus movement was highly variable between
individuals. There was no difference in movement between day, night, or crepuscular time
periods or between sexes. Larger octopuses moved more. This study is the first of its kind in
California, and one of the first successful octopus acoustic telemetry studies. Understanding
octopus movement will provide insight to habitat choice and the intersection of octopuses and
anthropogenic activity.
Keywords: tracking, Catalina Island, home range, activity, behavior
8
In: Lobel L.K. ed. Diving for Science 2015.
Proceedings of the American Academy of Underwater Sciences 34th Symposium.
Ecological Characteristics and Trends in Health of Robust Ivory Coral
(Oculina robusta) of the Florida Nature Coast
Cole Kolasa
Scubanauts International, 36181 East Lake Road #400, Palm Harbor, FL, USA
[email protected]
Abstract
Robust ivory coral (Oculina robusta) is the primary branching coral found along the
shallow waters of Florida’s west central Gulf coast where water temperatures
fluctuate from 47°F (8°C) to 92°F (33°C). This hardy slow growing coral provides
habitat for numerous small crabs and fishes. Coral colony size measurements and fish
and crab counts completed at three mid-shore sites located at 12 miles (19 km) and
25 miles (40 km) offshore, revealed a positive relationship (correlation coefficient of
r2 = 0.89) between the volume of coral colonies and the number fish and crabs
inhabiting the colony. Coral colonies located closer to shore (12 miles) were found to
have significant coverage or growth of both algae and encrusting sponge, whereas the
offshore colonies were mostly clean of attached algae and sponge growth. Greater
temperature fluctuation was observed at these shallow mid-shore sites (12 ft, 3.6 m)
than the deeper offshore sites (30 ft,, 9 m). Photos collected at these mid-shore sites
showed mortality of several colonies in 2011 and 2012 as the result of the growth of
encrusting/boring sponge. The colonies most affected were those located along the
outside low edge of the rock outcrops. Growth rates were determined using photos of
individual colonies spanning from 2010 to 2015 and applying measuring tools of
Adobe® Acrobat Pro software. The average growth rate determined for healthy
colonies was 0.2 inches per year (0.5 cm/yr). Based on this average growth rate the
largest colony observed was estimated to be 120 years old, indicating this species has
a significant life span.
Keywords: coral ecology, Eastern Gulf, Hernando, Pasco, Citrus County, hard
bottom
9
In: Lobel L.K. ed. Diving for Science 2015.
Proceedings of the American Academy of Underwater Sciences 34th Symposium.
Use of Dual Laser Photogrammetry for Use in Measuring Reef Fish:
Techniques, Pitfalls and Limitations
Chris Ledford
Texas Parks and Wildlife Department-Artificial Reef Program, Dickinson Marine Lab, 1502 F.M. 517 East,
Dickinson, TX 77539, USA
[email protected]
Abstract
The use of dual lasers to provide a known length standard in an image is a relatively easy and
inexpensive method of non-invasive, in-situ measurement. The key to collecting accurate data
lies in the setup of the system and identifying the error limitations of the specific set up. Three
sources of error are addressed: system specific, photographer specific and measurement
specific. System specific errors include non-parallel lasers and fish eye distortion caused by
the camera lens. Photographer errors include basic camera ability and distance from and angle
of the target. Measurement specific errors include inconsistent scale calibration and
interpretation of fin margins. In-water data acquisition is quick, captures numerous data
points, and, with relatively little training, can be accomplished by any capable diver. The
primary disadvantage of the video methodology is the time required to process the data. An
average of a 6-to-1 ratio of lab time to recorded survey time was typical when documenting
only length measurements of the targeted fish. This time includes screen captures, organism
identification, specimen measurement and measurement transfer to spreadsheet format.
Transfer of video files and any video/photo editing is not included in the time estimate. Dual
Laser Photogrammetry is particularly useful when in-water time is limited, but actual
measurements of species are required.
Keywords: measurement, video, fish, underwater
10
In: Lobel L.K. ed. Diving for Science 2015.
Proceedings of the American Academy of Underwater Sciences 34th Symposium.
Ecological Implications of a Northern Range Expansion of Black Sea Bass,
Centropristis striata
Marissa D. McMahan*, Jonathan H. Grabowski
Northeastern University, Marine Science Center, 430 Nahant Rd, Nahant, MA 01908, USA
[email protected]
*
presenting and corresponding author
Abstract
The coastal waters of the Northwest Atlantic contain one of the steepest temperature gradients
in the world. In the past, this significant variation in water temperature has prevented
temperate species from shifting northward. However, the general rise in temperature over the
past two decades has resulted in more temperate species entering the Gulf of Maine (GOM).
For example, black sea bass, Centropristis striata, historically ranged from the Gulf of
Mexico to Cape Cod, but in recent years it has been reported as far north as midcoast Maine.
Very little is known about the population dynamics of the expanded stock or the ecological
impacts of sea bass range expansion on the GOM. We conducted SCUBA surveys to quantify
sea bass from the historical northern edge of their range (Rhode Island) into the GOM
(northern Massachusetts and Maine) and found that abundance increased from spring to fall
and decreased with latitude. Additionally, small juveniles were not present in the northern
GOM. We also examined their diet, growth and reproductive effort throughout the GOM.
Preliminary results indicate that the importance of crustaceans to the diet of sea bass increases
with latitude and that sea bass are not currently spawning in the northern GOM. These results
are the first documentation of sea bass feeding ecology and productivity in the northern GOM,
and will inform efforts to determine the impacts of sea bass on food web dynamics and
fisheries productivity of native GOM species. Furthermore, this study aims to assist efforts to
assess and manage this species in its newly expanded range.
Keywords: Gulf of Maine, distribution shift, fisheries, community structure
11
In: Lobel L.K. ed. Diving for Science 2015.
Proceedings of the American Academy of Underwater Sciences 34th Symposium.
Stereophotogrammetry in Temperate Marine Environments
Andrew O.M. Mogg*, Martin D.J. Sayer
NERC National Facility for Scientific Diving, Scottish Association for Marine Science, Dunstaffnage Marine
Laboratories, Dunbeg, Obanm Argyll, PA37 1QA, SCOTLAND
[email protected]
*
presenting and corresponding author
Abstract
Structure from Motion-Multi View Stereophotogrammetry (SfM-MVS) is the construction of
3D models based on the location of recognizable points in multiple photographs.
Stereophotogrammetry is frequently used by survey companies to map cities and geographic
features with speed and accuracy, using terrestrial and aerial cameras. Stereophotogrammetry
is also used to create digital models of specific objects, for medical, archaeological and
entertainment purposes. There is an increasing interest in using stereophotogrammetry to map
the marine environment because of its ability to provide faithful 3D recreations of a variety of
targets, from biogenic reefs to shipwrecks, which may prove difficult to sample, measure or
recover. However, even in crystal-clear water, underwater stereophotogrammetry is
problematic, owing to the unique optical characteristics of the natural fluid medium. Working
in temperate or eutrophic waters adds an entirely new level of difficulty, owing to increased
particulate matter and variable ambient light levels. We will present the specific challenges
faced during underwater stereophotogrammetric survey, discuss our progress under temperate
conditions, and go on to provide examples of the application of this exciting step-change
technology.
Keywords: 3D, development, stereophotogrammetry, surveying
12
In: Lobel L.K. ed. Diving for Science 2015.
Proceedings of the American Academy of Underwater Sciences 34th Symposium.
In Situ Studies of Limestone Dissolution in a Coastal Submarine Spring
Rachel M. Schweers, James R. Garey*
University of South Florida, 4202 E. Fowler Ave, Tampa, FL, 33620, USA
[email protected]
*
corresponding author
Abstract
Limestone dissolution in karst environments is likely due to geochemistry of the water, the
actions of microbial communities, and the effect of water flow. We explored the rate of
limestone dissolution and will examine the microbial communities associated with the
limestone. A conduit within the brackish Double Keyhole coastal spring in central west
Florida was the site of the experiment. PVC pipes (5cm x 16cm) were filled with crushed
limestone that was screened to a 1.9cm – 2.54 cm size range. The limestone was dried for
three days at 75oC and weighed prior to deployment within the conduit on a rack with the
pipes parallel to the water flow. There were three treatments (5 replicates each): Control sealed autoclaved controls with limestone and conduit water, Low Flow – sealed at one end,
with a screen on the other so water contacts the limestone but cannot flow through, High Flow
– screen mesh at both ends to allow the flow of conduit water through the pipe. After 9
months, the samples were retrieved. The limestone was washed gently and dried for 3 days at
75oC and weighed. The Controls showed a loss of 0.33% ± 0.10 Low Flow samples showed a
loss of 1.63% ± 0.71 and High Flow samples lost 2.28% ±0.29. These results indicate that the
dissolution of limestone ranges from 0.3-2.25% in this system over the 9 month study period.
Other studies in freshwater conditions found an average weight loss of 2.25% over the same
time period under conditions similar to the High Flow sample in this experiment. Results thus
far suggest that limestone dissolution is significant in this system and is likely mediated by
microbial communities.
Keywords: carbonate, biogeochemistry, karst,
13
In: Lobel L.K. ed. Diving for Science 2015.
Proceedings of the American Academy of Underwater Sciences 34th Symposium.
Lionfish Invasion in Panama: Multiagency Collaboration Case Study
Andrew Sellers¹, Edgardo Ochoa²*, Yazmin Villareal³, Gabriel López Dupuis4
1
Smithsonian Tropical Research Institute, AP 0843-03092, Panama, Republic of Panama
Conservation International, 2011 Crystal Drive. Suite 500, Arlington VA. 22202 USA
[email protected]
3
Autoridad de los Recursos Acuáticos de Panamá, Departamento de Investigación, Dirección General de
Investigación y Desarrollo, Panama, Republic of Panama
4
Fundación Clear This Fish, Panama, Republic of Panama
*
presenting and corresponding author
2
Abstract
The invasion by the Indo-Pacific lionfish (Pterois volitans) in the Western Atlantic Ocean
represents a potentially serious ecological and economic threat to the region. Conservationists,
local communities, and researchers across the region have set out to study the ecology of this
invasion, and develop strategies to mitigate its potential impacts. Conservationists and local
coastal communities wrestling with the invasion have suggested that recreational and
commercial harvesting of the species for food may greatly reduce its abundance, at least at a
local scale. Researchers have also made important contributions to understanding the ecology
of this invader, including their impact and the ecological processes that determine the
lionfish's demographic success. In order to properly address the lionfish invasion, however,
countries across the affected region must integrate management and research initiatives. In
Panama, individuals and organizations have come together to develop creative ways to face
the problem. Such efforts have led to local reductions in lionfish populations, generated novel
insights into the ecology of the invasive lionfish, and created a source of food and revenue for
local communities. In this talk we will outline the efforts undertaken in Panama, and present
their results.
.
14
In: Lobel L.K. ed. Diving for Science 2015.
Proceedings of the American Academy of Underwater Sciences 34th Symposium.
Developing the Next Generation of Aquatic Stewards: The National
Association of Black SCUBA Divers Foundation Scientific Diving Program
Paul L. Washington Jr.1,*, Jay Haigler2
National Association of Black SCUBA Divers Foundation, 1605 Crittenden Street NE, Washington DC 20017
USA
1
[email protected]
2
[email protected]
*
presenting and corresponding author
Abstract
Founded in 2005 as the philanthropic arm of the National Association of Black SCUBA
Divers (NABS), the NABS Foundation has at its core the mission of promoting scuba diving,
water skills, environmental sciences, and archeology and conservation programs. In 2012, the
NABS Foundation became an Organizational Member of the American Academy of
Underwater Scientists, with goal of advancing marine and environmental sciences and
scientific diving within traditionally underserved and underrepresented communities. This
presentation discusses the approach taken by the NABS Foundation to develop and sustain a
scientific diving program that supports its goals as well as the larger goal of developing the
next generation of Aquatic Stewards.
Keywords: scientific diving, Aquatic Stewards, NABS, NABSF, AAUS
15
In: Lobel L.K. ed. Diving for Science 2015.
Proceedings of the American Academy of Underwater Sciences 34th Symposium.
Breaking Through Barriers for Marine Conservation
Liv Wheeler1*, Phil Dustan2*
1
Trees to Seas (501c3), 2646 Ipulei Place, Honolulu, HI 96816, USA
[email protected]
2
Department of Biology, College of Charleston, Charleston SC, 29424 USA
*
co-presenting authors
Abstract
We will begin with a brief history of the Aqualung and how it opened up the shallow seas for
sport, exploitation, and science exploration that ultimately lead to the formation of AAUS. In
the 60-70 years since, diving scientists have documented increased ecological degradation
correlated with local to global anthropogenic stressors, many of them resulting from or
intensified by climate change. We will show that scientists can no longer simply pursue pure
“loading dock” science because ocean degradation is accelerating. Our call to action is based
on the concept that people feel connected when they get involved in a cause they are
passionate about. We will describe three active coral reef conservation projects that blend
science and sociology through a fusion of scientific and sport diving. The transcending
simplicity of active participation, working together for a cause beyond an immediate goal,
empowers people to change the world.
Key Words: diveaware, Ed Rickets, marine conservation education, loading dock science
16
In: Lobel L.K. ed. Diving for Science 2015.
Proceedings of the American Academy of Underwater Sciences 34th Symposium.
Lost at Elbow Reef: Collaborative Research on Steamship Shipwrecks in
the Florida Keys National Marine Sanctuary
Jay V. Haigler1, 2*, Paul L. Washington Jr.1,2, Dr. Albert José Jones1,2
1
Diving With a Purpose, 3445 Massachusetts Avenue SE, Washington, DC 20019, USA
[email protected]
2
National Association of Black Scuba Divers Foundation, 1605 Crittenden Street NE, Washington, DC 20017,
USA
*
presenting and corresponding author
Abstract
Jutting into the Gulf Stream, Elbow Reef has claimed numerous vessels, particularly
steamships, over the last 150 years. Today, these shipwrecks attract hundreds of divers and
snorkelers visiting the National Oceanic and Atmospheric Administration’s Florida Keys
National Marine Sanctuary. Archaeologists have revealed the histories of several vessels, but
time has shrouded the identities of others until recently. Diving With a Purpose (DWP),
supported by scientific divers from the National Association of Black Scuba Divers
Foundation (NABSF) is partnering with the Office of National Marine Sanctuaries (ONMS)
to support renewed efforts to reveal the history of Elbow Reef. In 2012, volunteer avocational
archaeologists from DWP, joined ONMS archaeologists and resource managers to document
an unidentified shipwreck lost on Elbow Reef. Over several days the team archaeologically
documented a diagnostic portion of the shipwreck; known locally as “Mike’s Wreck” and
determined that it was the British steamship Hannah M. Bell lost in 1911. A much larger
team of DWP divers returned to the site in May 2014 and May 2015 to complete the site map
and reveal aspects of the historic salvage that took place on the site following its grounding.
Furthermore, the project began documenting another nearby steamship shipwreck and
determined its likely identity. The presenter will describe the collaborative efforts taken to
identify the Hannah M. Bell and other Elbow Reef shipwrecks, revealing the breadth of
human activities on that reef.
Keywords: Hannah M. Bell, Mike’s Wreck, National Oceanic and Atmospheric
Administration, Office of National Marine Sanctuaries, Diving With a Purpose, National
Association of Black Scuba Divers Foundation
Introduction
In Key Largo, Florida, there is an area called “Elbow Reef” that has been responsible for many
shipwrecks over the past 150 years. The City of Washington shipwreck is one of many ships that are
now favorite dive site destinations for hundred of recreational scuba divers per year.
While conducting a Nautical Archaeology Society (NAS) training session, NOAA maritime
archaeologist, Matthew Lawrence and Florida Keys National Marine Sanctuary Program Support
Specialist, Brenda Altmeier discovered a wreck that had been known locally as “Mike’s Wreck”,
which seemed to have a similar dimension and profile of another steamship.
This discovery provided an opportunity for NOAA’s Florida Keys National Marine Sanctuary to
collaborate with the Diving With a Purpose (DWP) organization to research and document this
shipwreck with the objective definitively identifying this ship.
17
Expeditions were conducted in September 2012; May 2014; and May 2015.
Methods
Research
The initial research indicated that the steamship Quoque was the ship that wrecked on Elbow Reef.
The Quoque was approximately the same size of the wreck. The wreck site is approximately 300 feet
long and a width of 40 feet. The construction was similar. The ship was built in Astoria, Oregon and
was lost in February 1920. The ship went down in 25 feet of water. The ship was reported to have
wrecked on top of the old wreck “Anna M. Bell”. Upon further research, it was discovered that the
Quoque was constructed with wood. The wreck that we were investigating was a steal steamship.
While continuing the investigation, we found that the measurements of the shipwreck and the records
a shipwreck called the “Hannah M. Bell” were an identical match. The ship was built by Ropner and
Son in Stockton-On-Tees, England on March 20, 1893 and named for the woman who christened it.
The length of the ship was 315 feet and the width was 41.5 feet (Figure 1). The Hannah M. Bell was
lost on April 4, 1911. The ship was loaded with coal bound for Vera Cruz, Mexico. Prior to its
demise, the ship made frequent transatlantic trips between European, the United States East and Gulf
coasts, and South American ports. Specific ports of call were: Hamburg, Liverpool, Rotterdam,
Havana, Boston, Norfolk and Galveston. The Hannah M. Bell transported a variety of bulk cargos
including fertilizer, hemp, naval stores, cotton and sugar.
Figure 1. Photo of the Hanna M. Bell Steamship. Courtesy of Harold Appleyard.
18
Mapping
Diver collected data was used to produce a site map of the wreckage. To document the site, the dive
teams used trilateration mapping. The baseline was established using iron stakes in a tripod
configuration as datums on the ocean floor. A tape measure was used for the baseline. The length of
the baseline was 300 feet.
The iron hull of the shipwreck was largely intact. The wreckage was centered on the keelson. Once
the wreck stabilized, hull of the ship opened with the keelson becoming the centerline of the
wreckage. The baseline was established along the keelson, from the bow to the stern of the wreck.
Because of the way in which the wreck stabilized, there were sections of the wreck site that were
elevated from the ocean floor.
Standard operating procedure is to document the wreck in planned view (in-situ). Because of the way
the ends of the ship were articulated on the ocean floor, the Principal Investigator felt that it was
important to document certain sections of the wreck from a side view perspective.
Trilateration data along with in-situ drawings were used to develop the site map. The site map was
initially drawn in the field by hand. The data was then used to develop a detailed map using
computer-assisted software (Auto-CADD), to produce a final product.
Dive Operations
Diving field expeditions were conducted in September, 2012; May, 2014 and May, 2015.
The September 2012 expedition consisted of a six person dive team. The May 2014 expedition
consisted of twenty-two divers and the May, 2015 expedition consisted of twenty-four divers. The
dive platform for the September 2012 was a small craft boat with a single outboard engine. The dive
platform for the May 2014 and 2015 expeditions was a Newton 46 with twin inboard engines.
The May, 2015 expedition diving corps consisted of twelve dive teams of two divers per team. The
Principal Investigator and Project Coordinator were a part of the diving corps. Each team had a
specified area of the baseline to take trilateration measurements and to do in-situ drawings. There was
one team of divers that was assigned to document the elevated sections of the wreck site. The wreck
site was photographed and videotaped extensively.
The dive plan was to have each team dive until their air supply necessitated returning to the boat. The
typical bottom time for a dive team was 90 minutes. Once the dive team was back onto the boat, they
would review their data and discuss a plan of action for the next dive. Each team would make 2 dives
per day. After the second dive, the boat would return to shore.
Visibility varied from 50 feet to 100 feet. The water temperature ranged from 78 to 84 degrees
Fahrenheit.
Each field expedition was typically six days long, which included one day of orientation and dive
planning, three days of diving and two days of drawing and mapping.
Results
A complete site map and in-situ drawing have been completed (Figure 2). The Hannah M. Bell was
315 feet long and 41.5 feet wide.
19
Figure 2. Site Map of Hannah M. Bell from May 2014 Field Expedition
The wreck site was 300 feet long and 40 feet wide. The wreck was open from the keelson and
exposed the interior of the ship’s hull. The steel members of the hull that reinforced the engineer were
largely intact, as well most of the ship’s hull (Figure 3).
Figure 3. Hanna M. Bell wreck. Overall view from keelson. Photo courtesy of Matthew Lawrence.
20
Sections of the wreck that were elevated from the ocean floor were documented (Figure 4). In certain
cases, sections were elevated as much as 15 feet from above the ocean floor. The maximum depth of
the wreck is 25 feet. The site map will be produced and available to the general diving community in
Key Largo.
Figure 4. Dive team document elevated section of the wreck. Photo courtesy of Matthew Lawrence.
Discussion
For years, the local Florida Keys community identified this wreck site as “Mike’s Wreck”, named
such after an employee of a local dive operator.
Confirming the exact name of a ship does more than give the dive site a name, it provides a history
and context with which divers can gain greater appreciation for our shared maritime heritage, on a
local, regional and national level.
Florida Keys National Marine Sanctuary historians have scoured historical archives and newspapers
for vessels lost at Elbow Reef and these historians will compare the characteristics of those ships
against what remains today. Sanctuary staff will use the information to establish a plan for future site
documentation and management, as well as possible nomination of the site to the National Register of
Historic Places.
Diving With a Purpose (DWP) is planning to develop a diver’s slate for use by the recreational diving
community to summarize the mapping information and site plan. The intent of the diver’s slate is to
inform the diving public about the heritage of the Hannah M. Bell and Elbow’s Reef.
Presentations to local communities in Key Largo, Florida as well as communities in locations of the
members of Diving with a Purpose (DWP) and the National Association of Black Scuba Divers
Foundation Scientific Diving Program are on going.
21
This mission is a model for collaborative efforts between government institutions and non-profit
organizations dedicated to protecting our oceans and preserving our heritage.
As a result of this collaboration and discovery, DWP along with its strategic partner, the Office of
National Marine Sanctuaries (ONMS) received the 2015 Chairman’s Award from the Advisory
Council of Historic Preservation.
Acknowledgements
The authors would like to thank Dr. James Delgado, Director of NOAA Maritime Heritage Program,
NOAA maritime archaeologist, Matthew Lawrence and Florida Keys National Marine Sanctuary
Program Support Specialist, Brenda Altmeier, Margo E. Jackson of the NOAA Maritime Heritage
Program for their dedication to the mission. We also will like to thank Ken Stewart, Co-Founder of
DWP for his commitment to the organization and Gayle Carter Patrick, DWP Cartographer for
developing and creating DWP site maps for all projects.
22
In: Lobel L.K. ed. Diving for Science 2015.
Proceedings of the American Academy of Underwater Sciences 34th Symposium.
Using Scientific Diving as a Tool to Tell the Story of Human History:
Bringing the São José Paquete de Africa Into Memory
Jay V. Haigler1, 2,3*, Paul L. Washington Jr.1,2,3, Kamau Sadiki1,2,3, Dr. Albert José Jones1,2,3
1
Diving With a Purpose, 3445 Massachusetts Avenue SE, Washington, DC 20019, USA
[email protected].
2
National Association of Black Scuba Divers Foundation, 1605 Crittenden Street NE, Washington, DC 20017,
USA
3
National Association of Black Scuba Divers, 1605 Crittenden Street, NE, Washington, DC 20017, USA
*
presenting and corresponding author
Abstract
Underwater archaeological scientific diving is a powerful tool that can be used to tell the story
of human history and past cultural behavior. On December 3, 1794, the São José Paquete de
Africa, a Portuguese ship transporting over 500 captured Africans, left Mozambique Island,
on the east coast of Africa, for what was to be a 7,000 mile voyage to Maranhao, Brazil and
the sugar plantations that awaited its human cargo. The ship was scheduled to deliver the
enslaved Africans in February 1795, some four months later. However, the journey lasted
only 24 days. Buffeted by strong winds, the ship rounded the treacherous Cape of Good Hope
and attempted to take shelter in Table Bay off the coast of Cape Town, South Africa. While
attempting to anchor in the bay, the ship came apart violently on rocks between two reefs not
far from what is known today as Clifton Beach. The São José Paquete de Africa represents
one of the earliest, “experimental voyages” from East Africa to the Americas that eventually
led to the shift that brought East Africa into the Transatlantic slave trade to an unprecedented
level. The Slave Wrecks Project (SWP) is a coalition of institutional partners that are
dedicated to documenting and preserving the São José Paquete de Africa. SWP is a
partnership between the Smithsonian Institute’s National Museum of African-American
History and Culture (NMAAHC), the George Washington University, the National Park
Service – Submerge Resource Center, Iziko Museums of South Africa and Diving With a
Purpose (DWP). Diving With a Purpose is supported by scientific divers from the National
Association of Black Scuba Divers Foundation. In 2013 and 2014, DWP supported the
scientific diving field mission to identify and document artifacts from the shipwreck. The
presenter will describe the collaborative efforts of the SWP partnership to identify and
document the São José Paquete de Africa shipwreck
Keywords: São José Paquete de Africa, Diving With a Purpose, Smithsonian Institute’s
National Museum of African-American History and Culture, The George Washington
University, National Park Service, Iziko Museums, Slave Wrecks Project, Transatlantic Slave
Trade.
Introduction
Diving is an integral part of underwater archaeology. Divers assist archaeologists, scientists and
researchers in their objectives of analyzing the physical remains of the past to acquire a broad and
comprehensive understanding of past human culture. Diving in Cape Town, South Africa has been a
critical component in assisting archaeologists, cultural anthropologists and researchers discover and
tell the story of the São José Paquete de Africa, a Portuguese ship transporting over 500 captured
Africans to Brazil, to be sold into slavery to work on the sugar plantations.
23
Documenting the São José Paquete de Africa shipwreck represents the first opportunity to fulfill a
goal of locating, documenting, and preserving the archaeological remains of ships that wrecked while
engaged in the international slave trade from Africa. The documentation of even one such ship would
represent an archaeological first, since not a single shipwreck of a vessel active in the slaving leg of
the trade has ever been documented. Over 600 slaving vessels known to have been lost in the
transatlantic trade alone, this mission could bring new archaeological perspective to bear on the
scholarly study of the Trans-Atlantic and Indian Ocean slave trades.
SWP field expeditions to the Sao Jose Paquete de Africa shipwreck site were conducted during
February in 2013 and 2014.
Diving safety is one of the primary objectives when searching, documenting and ultimately
excavating any portions of a shipwreck. Dive planning, equipment and water conditions are critical
aspects of a successful mission.
Methods
Mapping
To document the site, the dive team used trilateration mapping. Because of the surf and underwater
surge conditions, the baseline was established using steal nails as datums affixed to the hard-scape
ocean floor. Additional stainless steel nails were affixed to rocks on the ocean floor in equal
increments along a linear path between the two datums. The extremely dynamic environment of the
shipwreck prohibited the use of a tape measure as a baseline. The stainless steel nails in the linear
path served as the baseline. When an artifact was identified, a reference point was taken to the nearest
datum point. The distance from the artifact and the two nearest steal nails of the baseline were
measured. This gave the team sufficient data to determine the location of the artifact relative to the
baseline.
Dive Operations
The São José Paquete de Africa went down in 25 feet of water and pounding surf. The wreck site is
approximately 110 yards off the shore of an area called Clifton Beach. Thick kelp forest dominates
the wreck site with continuous underwater surges of up to 10 to 15 feet. Visibility varies from 5 feet
to 25 feet with kelp debris and sand continuously suspended in the water due to the underwater
surges. Because of the ocean conditions, the site is only accessible by boat (Figure 1). The site is very
dynamic with a constantly shifting sea floor. The water temperature ranges from 47 to 55 degrees
Fahrenheit.
The investigation of the São José Paquete de Africa was divided into two phases: 1) survey and
dredge the site to remove as much sand accumulation as possible, and 2) document any artifacts or
materials uncovered by developing in situ drawings. The field mission consisted of four dive teams of
two divers per dive team. The dive plan was to have each team dive for 45 minutes and be relieved by
the next team so that the work would be continuous.
To remove the sediment the dive teams used a surface water pump with a suction nozzle and flexible
hose to increase the team’s mobility on the wreck site (Figure 2). The dredge material was mostly
sand. Because of the significant surge conditions, sand would cover an area that was dredged almost
immediately. The dive teams engage in dredging activity until they uncover an artifact. Once a team
located an artifact, a photograph was taken before sand would re-cover the area. The teams dredge the
same area again to uncover an artifact to take measurements for the trilateration mapping.
24
Figure 1. Wreck site location, aerial view (L). Wreck site location, view from shore (R). The site
is located where rocks are breaking the surface. Photos provided by Kamau Sadiki.
Figure 2. Divers using induction dredge to increase mobility on the wreck site. Photos provided by Kamau
Sadiki.
The team located ship ballast bars, used to counter balance the ship. The research team determined
that these ballast bars were archaeologically significant. Lift bags were used to recover the ballasts
(Figure 3).
25
Figure 3. Diver preparing to recover of ballast (top). Diver recovering ballast (bottom). Photos
provided by Kamau Sadiki.
Results
The diving corps discovered the following items from the wreck site: (1) cannons and cannon balls;
(2) iron ballasts; (3) copper fasteners; (4) copper sheathing; (5) pulley block; and (6) iron shackles
(Figure 4). Through archival research in Mozambique and Portugal, the mission collaborators were
able to uncover documents that have revealed the ship’s owners, its cargo when it departed from
Mozambique and evidence of the sale of a slave by a local sheikh to the ship’s captain. The objects
recovered from the São José Paquete de Africa personalize the grand historical story and brutal nature
of the transoceanic slave trade.
26
Figure 4. Recovered ballast (Top left). Copper fasteners, in-situ (Middle left). Recovered pulley bock
(Bottom Left). X-ray of iron shackles (Top right). Example of iron shackles (Bottom right). Photos
provided by Kamau Sadiki.
As a result of discovered artifacts from the Sao Jose Paquete de Africa, the Smithsonian’s NMAAHC
and IZIKO Museums of South Africa have entered into a formal long-term agreement to loan the
artifacts for exhibition in Washington, DC at NMAAHC, which is scheduled to open in in Fall of
2016.
27
Acknowledgements
The authors would like to thank Dr. Stephen Lubkemann, International coordinator and creator of the
Slaves Wrecks Project. Dr. Lubkemann is also an Associate Professor of Anthropology &
International Affairs at The George Washington University. We would like to give special thanks to
Dr. Lonnie Bunch, Executive Director of the Smithsonian Institute for African-American History and
Culture Museum and Dr. Paul Gardullo, Curator of the Smithsonian Institute for African-American
History and Culture. Jaco Boshoff, Principal Investigator and Curator of the IZIKO – Museums of
Cape Town, South Africa was one the driving forces for the success of the São José Paquete de
Africa mission. Dr. Dave Conlin of the United States National Park Service – Submerged Resource
Unit and Mr. Jonathan Scharfman of the African Centre for Heritage Activities made significant
contributions to the mission.
28
In: Lobel L.K. ed. Diving for Science 2015.
Proceedings of the American Academy of Underwater Sciences 34th Symposium.
Diving for Cures: Mapping Microbial Genomics Underwater
Nasreen S. Haque1, 2*+, Bernie Chowdhury2*
1
New York Medical College, Valhalla, NY 10595, USA
[email protected]
2
Genomic Observatory Inc., 288 Portage Avenue, Staten Island, NY 10314, USA
*
Co-presenting authors
+
Corresponding author
Abstract
Resistant bacteria pose challenges to governments, healthcare systems, and drug development.
The study of unexplored, complex microbial ecosystems underwater offers avenues for the
much needed search for novel therapeutics. Scuba diving offers an invaluable resource for the
study of the underwater habitat(s) by facilitating sample collection and documentation of
environmental conditions. We have employed scuba diving techniques to obtain samples from
various depths at the now-defunct, flooded Tilly Foster Mine, Brewster, NY. Microbial
communities dominate the biosphere providing essential benefits to the environment and its
resident organisms. Many factors are involved in this interplay between the microbes and the
diverse ecological niches they occupy, however, most of these interactions that occur
underwater remain unknown. With rapid advances in technology and reduction in cost of
sequencing, the study of microbes is now possible at unprecedented levels. Targeting these
niches for the identification of novel metabolites may offer the next generation of
therapeutics. We used 16S/ metagenomics sequencing to compare and identify the antibiotic
resistance profile of the microbial communities in these environments. We have found that
Pseudomonades are prevalent and are responsible for most of the antibiotic resistant genes
found in this environment. This may be useful in identification of novel therapeutics.
Keywords: metagenomics, antibiotic resistance, sequencing, niche
Introduction
Bacterial resistance to antibiotics is a major cause of concern as it has become a critical healthcare
management issue worldwide (Ochman et al., 2000). Less than 1% bacteria found in the environment
can be cultured in the laboratory, which has negatively impacted our knowledge of microbial
dynamics that occurs in nature. However, with advances in sequencing technology, it is now possible
to identify the majority of uncultivable species leading to a clearer understanding of microbial
metabolic potentials and functional significance. This has also led to the realization that antibiotic
resistance genes are abundant in nature and present in diverse environments. Environments that
harbor antibiotic resistance include clinical samples such as human feces (Nesme et al., 2014) as well
nonclinical spaces such as soil (Allen et al., 2009), secluded caves (Bhullar et al., 2012), oceans
(Chen et al., 2013) and even permafrost (D’Costa et al., 2011; Martinez et al., 2009). As the
environmental antibiotic resistant genes are abundant reservoirs for potential transfer of resistances to
human pathogens (D'Costa et al., 2011) due to the widespread horizontal gene transfer, the selective
pressure that antibiotic pollution may exert on clinically important bacteria is of particular concern.
For example, human pathogens such as Escherichia coli and the enterococci are able to grow in
different environments (Topp et al., 2003, Moriarty et al., 2008). Thus, in the presence of
environmental concentrations of antibiotics, they may face a selective pressure leading to a gradual
increase in the prevalence of resistance. This raises the question about the mode of distribution of
microbial genes in human populations. In the present study, we asked whether the increase in
29
antibiotic resistance is a direct consequence of releasing large quantities of antibiotics into the
environment - via animal husbandry, sewage - or do other anthropogenic factors influence this
phenomenon. We hypothesize that understanding how microbes combat increasing resistances in
extreme environments may offer clues to the predominant mode of microbial function(s) in human
pathologies.
It has previously been shown that the biological and geochemical simplicity found in Acid mine
drainage (AMD) provides an ideal environment to study microbial community structure and function
(Baker and Banfield 2003; Denef et al., 2010). Therefore, we chose the privately-owned, nowdefunct, flooded Tilly Foster Mine, Brewster, NY as our site of investigation. Mining activities began
on this site in 1853 and it was dug to 600 feet deep by 1879. However, mining ceased in 1897, after
13 miners were killed in a rockslide (Dana, 1874). Subsequently, it was submerged by the Middle
Branch Reservoir and became a dump for household appliances, automobiles, vans, and trucks. New
York State Police have searched the Mine in 1999 and 2002 for the body of a murder victim
(www.doenetwork.org). The Mine was used in the past by military divers to test their equipment
(Various Personal Communication, Bernie Campoli, 2014), and in the 1980s was the site of a
commercial diving school (Various Personal Communication, Glenn Butler, 2014, 2015). In the
present study, we asked whether the increase in antibiotic resistance is a direct consequence of
releasing large quantities of antibiotics into the environment - via animal husbandry, sewage - or do
other anthropogenic factors influence this phenomenon. As there is no known direct input of
antibiotics into the mine compared to environment where direct sewage or household waste is
discarded, it provided us the ideal site for conducting our studies.
The most widely expressed mode of antibiotic resistant genes belonged to root nodulation cell
division family or RND efflux pumps, which are a common means of multidrug resistance. This
study highlights the importance of evolutionary pressures as a determinant of species specificity and
development of resistances. Thus, identifying the interactions that occur within specific niche(s) is an
essential first step towards understanding how microbial populations work and may offer clues to
combat antibiotic resistances in humans.
Methods
Sample collection:
Sediment and water samples were collected from the Tilly Foster Mine, Brewster, NY[Latitude &
Longitude (WGS84): 41° 24' 59'' North, 73° 38' 59'' West]. Sample collectors employed technical
diving techniques and used both open-circuit and rebreather scuba equipment to obtain samples from
different depths (65 ft and 165 ft). Breathing gases included trimix (oxygen – helium – nitrogen) for
greater mental clarity at deeper depths. Samples were collected in open water and in overhead
environments. The latter were tunnels created during the operation of the mine and the removal of ore
from which iron was extracted. Divers employed established cave diving principles in the overhead
environment. Surface water was also collected. Samples were either plated directly on Blood Agar
plates or stored at -20º C and transported to the lab and stored at -80º C till further use.
Water Quality Measurement:
Water was collected from various sites in the flooded mine and analyzed for water quality. The pH
and temperature were measured directly while concentrations (ppm) of dissolved oxygen, phosphates
and nitrates were tested using the standard water testing kit (Carolina laboratories, NC). Each assay
was performed in triplicate.
30
DNA Preparation and High-throughput Sequencing
DNA in the sediment samples was extracted using the Power soil kit from MO BIO (Carsbad, CA)
according to the manufacturer’s protocol. DNA was isolated from multiple samples and pooled to
eliminate heterogeneity in sediment samples and to avoid potential bias during the DNA extraction
process. The purity and yield of the DNA were determined using a Thermo Scientific NanoDrop 1000
Spectrophotometer and DNA from each sample were submitted to the New York Medical College
(NYMC, Valhalla, NY) Genomics core laboratory at NYMC. Sequence libraries of all samples were
prepared and sequencing performed on Illumina platform.
Bioinformatic Analysis
Raw reads containing low-quality reads, such as ambiguous nucleotides or with a quality value lower
than 20 were removed from each of the samples. The local BLASTX programs were employed to
align trimmed clean reads of each data set against an antibiotic resistance genes database (ARDB). A
read was annotated as an ARG-like sequence if the best BLAST hit (blastx) had a sequence identity
of higher than 90% and an alignment length of at least 25 amino acids.
Results
Water quality measurements
Samples collected from different sites/depths in the Tilly Foster Mine (Table 1) were subjected to
water quality testing. Nitrates were higher (5) at the surface compare to at depth (<5 ppm); while the
phosphates were inversely related [surface low (<4 ppm); depth high (2 ppm)]. However, the pH
levels were maintained within a small range (7.7-8) in all samples tested at different depths as well as
at the surface. As expected, dissolved oxygen content was much higher (4ppm) at surface as
compared to depth (0-2 ppm). Methanogens were found at those depths where dissolved oxygen
content was low or absent.
Table1. Water quality measurement at different depths in the Tilly Foster mine
Microbial diversity in the Tilly Foster Mine at different depths
Scuba diving was used to obtain samples from different depths in the flooded Mine. Sequencing
(16S) analysis showed that microbial diversity varied with depth. While Pseudomonas were the most
dominant species at all depths tested, Methanogens (Archaea) were found only at depths below 165 ft
and Shewanella were most abundant at the surface. While abundant microbial diversity was observed
at different sites in the mine it was clear that a very minor percent of bacteria could be encountered in
31
cultured conditions (Tables 2A, 2B). Samples obtained at the depth of 165 feet under culture
conditions showed a predominance of Pseudomonas species. Interestingly, an increase in species
diversity is seen in both Pseudomonas spp. (Table 2A) and Shewanella (Table 2B).
Table 2A. Pseudomonades are found at all sites examined and can be cultured from samples at the surface
(water) and at depth (sediment)
Table 2B. Shewanella are the most abundant species in culture conditions at the surface (water sample)
32
The direct culture of surface water sample (Figure 1A) yielded colonies, which were mostly
proteobacteria [Shewanella spp. (59%), Pseudomonas (7%) and Rahnenella aquatilus (2%)]. At 65 ft
water samples under cultured conditions (Figure 1B) was also dominated by proteobacteria with
Pseudomonas spp. (34%). However, when uncultured sediment samples were examined directly at
the same depth (Figure 1C), actinobacteria (5%) were also observed along with proteobacteria which
included Pseudomonas spp. (34%) Enterobacteriaceae bacterium (3%), Myxococcales spp. (4%) and
Bradyrhizobiaceae spp. (3%). In uncultured sediment samples at 165 ft (Figure 1D), proteobacteria
were further reduced, whereas actinobacteria were increased. Proteobacteria included Pseudomonas
spp. (7%), Burkholderiales (5%), Candidatus spp. (3%), and Syntrophobacterales (3%). Among the
actinobacteria, 3% Clostridium spp. were identified. These results show that the differences in
resistance gene expression may be taxa specific or a result of the differing microbial assemblages by
depth and/or matrix.
.
Figure 1A. Shewanella spp. were the dominant species in cultured surface water.
It was evident that samples that underwent direct metagenomics analysis provided a better assessment
of microbial diversity in any community (Figures 1C, 1D). Sediment samples collected at 65 feet
accounted for 84.6% bacteria, which were enriched for proteobacteria and actinobacteria and
Dickeya phage (13.7%). The bacterial species that dominated this space included enterobacteria,
Kleibessia pneumoniacae (47%), Shewanella spp. (5%), Pseudomonas (26%) and Oceanspirillates
(18%).
33
Figure 1B. Water samples at depth (65 ft) is dominated by proteobacteria, Pseudomonas spp. under culture
conditions.
Figure 1C. Sediment samples at depth (65 ft) shows actinobacteria in addition to proteobacteria.
Figure 1D. In uncultured sediment samples at 165 ft (Figure 2D), proteobacteria were further reduced, whereas
actinobacteria were increased
34
Archea - Euryarchaeota identified only in sediment samples at deeper depths
At the depth of 165 feet (sample #23) Archaea, which accounted for up to 14.4 % of the total species,
started appearing. Euryarchaeota belong to Archaea (Figure 2). This group includes the methanogens,
which produce methane and are often found in intestines, the halobacteria, which survive extreme
concentrations of salt, and some extremely thermophilic aerobes and anaerobes. They are separated
from the other archaeans based mainly on rRNA sequences. We found that both methanogens and
halobacteria were present at this site. Natronoccoccus occulitus (50%) and Natrimena pellirubrum
(50%) accounted for the Halobacteriaceae present in this environment. The Methanoccaceae
comprised of Methanothermoccocus okinavenus (50%) and Methanoccocus vitae (50%). Abundant
bacteria (65%) which included firmicutes, Actinobacter and proteobacteria were also present.
Notably, no Shewanella spp. were found at this depth. However, the number of virus increased at this
site.
Figure 2. Archeal species are found as depth increases in sediment samples
Antibiotic resistance genes are abundant in sediment samples at all sites examined
Metagenomic profiling demonstrated that widespread antibiotic resistant genes were present in this
environment which increased with depth. The antibiotic resistant genes expressed between samples at
depths of 65 ft and 165 ft were compared and bioinformatics analysis was performed by using the
ARDB-Antibiotic Resistance Genes Database. The results indicate an increase in AR genes as depth
increases indicating that organisms that need to survive under such extreme conditions are under
constant selective pressure (Table 3). The predominant mechanism of resistance seems to by the
Root–nodulation–cell division (RND) family efflux pumps, which are a common means of multidrug
resistance. There was an increase of 29.3 % increase in the RND family of genes at 165 ft (532 hits)
compared to 65 ft (156 hits). Similarly, an increase (41%) in tetracycline (105 hits at 165 ft; 43 hits at
65 ft) and streptomycin (62 hits at 165 ft; 4 hits at 65 ft) resistant genes was observed.
35
Table 3. RND family efflux pumps are the most abundant mode of antibiotic resistance
Discussion
This study provides the first glimpse into the microbial dynamics of a mine which has been impacted
by both natural conditions as well as human activity. Environmental levels of antibiotics were not
verified in the present study. However, the presence of contaminants in this environment suggests that
it might impact the evolution of microbial resistance genes. For example, the automobiles and
household appliances routinely dumped into this mine release numerous contaminants. Automobiles
release oil, antifreeze, grease, metals and tires which settle in the water. It is important to note that
appliances manufactured prior to 1979 may contain PCB capacitors and mercury-containing
components (i.e., switches and relays). PCBs are a probable carcinogen. Mercury in products does not
pose a threat until it is released which acts as a neurotoxin and interferes with the brain and nervous
system in humans. Refrigerants deplete the ozone, causing several human and environmental
problems, such as global warming and increased skin cancer risk. Used oil, if improperly disposed,
can result in groundwater contamination, and skin, eye and respiratory irritation. In the long term, it
can cause cancer and damage internal organs (Iowa Department of Natural Resources, 2012).
Key findings in this study are that Pseudomonades species are found at all depths examined and are
responsible for most of the antibiotic resistant genes found in this environment. Interestingly, while
Pseudomonades could be isolated under cultured conditions at both surface and at depth, and are
found at all sites examined, Shewanella were the most abundant (72%) species in culture conditions
at the surface but not at depth. Notably, Shewanella levels decrease at 65 ft (5%) and is completely
eliminated at depths over 165 ft. The abundance of the easily cultivable Shewanella as compared to a
reduction of Pseudomonades at the oil/water interphase at the surface may change the dynamics of
microbial interactions and raises the likelihood of a self–sustaining environmental bioremediation
system, which may also have implications in clinical environments. Soil or sediment bacteria are
known to contain antibiotic resistance genes responsible for different mechanisms that permit them to
overcome the natural antibiotics present in the environment. These genetic elements can be mobilized
into the microbial community that affects humans because of widespread horizontal gene transfer
among microbial populations. Evidence for this transference has been suggested or demonstrated with
newly identified widespread genes in multidrug-resistant bacteria (Canteón, 2009.).
Antibiotic resistance is a common characteristic of environmental bacteria (Walsh, 2003; Baron et al.,
2007). This is due to the fact that several vital cell functions are targeted by resistant organisms. In
36
this study the most abundant mode of antibiotic resistance genes belong to the Root–nodulation–cell
division (RND) family efflux pumps. Efflux pumps are transport proteins involved in the extrusion of
toxic substrates from within cells into the external environment (Webber and Piddock, 2003).
Essentially, this includes all classes of clinically relevant antibiotics. These efflux pumps are a
common means of multidrug resistance, and induction of their expression can explain the observed
cross-resistance found between antibiotics. Pseudomonas aeruginosa, which has been identified in
this mine, is a gram-negative rod that is ubiquitous in nature and an opportunistic pathogen, causing a
wide variety of infections in compromised hosts. For example, P. aeruginosa is the most significant
pathogen in Cystic Fibrosis (CF) in which chronic airway infection is the most important cause of
morbidity and mortality (Burns et al., 1998, 2001; Cystic Fibrosis Foundation, 1994; Saiman, 2004).
In addition to resistant chromosomal β-lactamase, and mutations of antibiotic target molecules,
upregulated efflux pumps seem to play a major role in CF pathogenesis (Høiby et al., 2015). Efflux
systems that have been described in P. aeruginosa include MexAB-OprM, MexCD-OprJ, MexEFOprN, and MexXY-OprM which efflux fluoroquinolones and the RND pumps (CmeB, AcrB, and the
Mex pumps) that also export multiple antibiotics (Webber and Piddock, 2003). It has been shown that
concomitant overexpression of some Mex systems, which are found in abundance at our examined
site, superimpose their antimicrobial drug efflux capabilities, contributing to the multidrug resistance
phenotype in the P. aeruginosa in non-CF clinical isolates (Poonsuk et al., 2014). Our finding that
RND efflux pumps in conjunction with Mex systems are activated with the abundance of P.
aeruginosa suggests that selective pressures incurred in this extreme environment may have parallel
repercussions in clinical environments.
In contrast to other pathogenic bacteria P. aeruginosa from diverse environments do not show
particular genomic differences and thus genetic variability is extremely low (Grosso-Becerra et al.,
2014). However, they are phenotypically diverse with respect to production of virulence and motility
factors even though the genomes have high degrees of similarity (Finnan, 2004). Therefore,
understanding the mechanisms of P. aeruginosa derived RND efflux pumps in extreme environments,
such as the Mine, may be correlated to what occurs in clinical environments which may be developed
for novel therapeutics.
Apart from the bacterial species the virus, Dickeya phage is also found in this environment. In
addition, we have identified Archaea, namely, the euryarchaeota which comprise the strict anaerobic
methanogens and the extreme halophiles, at increased depths, which shows that even after more than
a century of cessation of mining activities, the bio-mineralization of ores continues at this site. This is
of particular concern as methanogens process substrates and then releases methane back into the
global carbon cycle. This may have climate implications. Moreover, it is interesting to find
methanogens and halobacteria in such close proximity. The chance of any two strains of a single
archaeal species at any site should be evolutionary closer than a pair of bacterial strains from the same
site. This may be because archaeal dispersal is more difficult due to the lack of cell wall, leading to
less phylogenetic diversity than that of coexisting bacteria, which would disperse more easily. As
opportunities for dispersal of Mine-adapted microorganisms will be limited, bacterial and archaeal
populations should be more related; this has been observed in the present study.
In conclusion, antibiotic resistance is a major concern because of the widespread resistance both in
hospitals and in the environment. Microbial diversity is an indicator of the functioning of any
ecosystem. Therefore, targeting this diversity and identifying the characteristic niche of an
environment such as the Tilly Foster Mine will provide useful insights which may be implemented
for future criteria that may be used in environmental remediation programs as well as in clinical
environments.
37
Acknowledgments
We would like to thank the following: J. Dan Wright and John Eells for obtaining samples from the
Tilly Foster Mine; William Ahrens and Bill Carver for surface support during operations at the Mine;
Maurice and David Simon for access to this site; Dr. John Fallon III, and Dr Weihua Huang,
Genomics Core Facility at New York Medical College, Valhalla, NY for metagenomics sequence
analysis; special thanks to students and volunteers for their engagement at various stages of this
study; support from the Rouse-Berman Memorial Fund. This project is sponsored by Genomic
Observatory, Inc., Staten Island, NY.
Literature Cited
Allen, H.K., L.A. Moe, J. Rodbumrer, A. Gaarder, and J. Handelsman. 2009. Functional Metagenomics Reveals
Diverse Beta-lactamases in a Remote Alaskan Soil. ISME J., 3, 243–251.
Baker, B.J., and J.F. Banfield. 2003. Microbial Communities in Acid Mine Drainage. FEMS Microbiol. Ecol.,
44: 139–152.
Baron, C., and B. Coombes. 2007. Targeting Bacterial Secretion Systems: Benefits of Disarmament in the
Microcosm. Infect. Disord. Drug Targets, 7:19–27.
Bhullar, K., N.Waglechner, A.Pawlowski, K. Koteva, , E.D. Banks, M.D. Johnston, H.A. Barton, and G.D.
Wright. 2012. Antibiotic resistance is prevalent in an isolated cave microbiome. PLoS ONE, 7(4): e34953.
Burns, J.L., J. Emerson, J.R. Stapp, D.L. Yim, J. Krzewinski, L. Louden, B.W. Ramsey, and C.R. Clausen.
1998. Microbiology of Sputum from patients at Cystic Fibrosis Centers in the United States. Clin. Infect. Dis.,
27(1):158-63.
Burns, J.L., R.L. Gibson, S. McNamara, D. Yim, J. Emerson, M. Rosenfeld. 2001. Longitudinal Assessment of
Pseudomonas aeruginosa in Young Children with Cystic Fibrosis. J. Infect. Dis., 83:444-452.
Chen, B., Y. Yang, L. Ximei, K.Y. Liang, Z. Tong and X. Li. 2013. Metagenomic Profiles of Antibiotic
Resistance Genes (ARGs) between Human Impacted Estuary and Deep Ocean Sediments. Environmental
Science & Technology, 47:22.
Cystic Fibrosis Foundation. 1994. Microbiology and Infectious Disease in Cystic Fibrosis. Bethesda, MD:
Cystic Fibrosis Foundation, Consensus Conference: Concepts in Care, 5(1).
Dana, E.S. 1874. On Serpentine Pseudomorphs and other Kinds from the Tilly Foster Iron Mine, Putnam
County, New York. American Journal of Science, 3 (8): 371-81.
D’Costa, V.M., C.E.King, L.Kalan, M.Morar, W.W.L Sung, C. Schwarz, D. Froese, G. Zazulaa, F. Calmels,
and R. Debruyne. 2011. Antibiotic Resistance is Ancient. Nature, 477: 457–461.
Denef, V.J., R.S. Mueller, J.F. Banfield. 2010. AMD Biofilms: Using Model Communities to Study Microbial
Evolution and Ecological Complexity in Nature. ISME J., 4: 599–610.
Finnan, S. Genome diversity of Pseudomonas aeruginosa Isolates from Cystic Fibrosis Patients and the
Hospital Environment. 2004. J. Clin. Microbiol., 42: 5783–5792.
Grosso-Becerra, M.V., C. Santos-Medellín, A. González-Valdez, J.L. Méndez, G. Delgado, R.M. Espinosa, L.
Servín-González, L.D. Alcaraz and G. Soberón-Chávez. 2014. Pseudomonas aeruginosa Clinical and
Environmental Isolates Constitute a Single Population with High Phenotypic Diversity. BMC Genomics,
15:318.
38
Høiby, N., C. Oana, and B. Thomas. 2015. Pseudomonas aeruginosa Biofilms in Cystic Fibrosis. Future
Microbiology, 5(11): 1663-1674.
Iowa Department of Natural Resources. 2012. Appliance Fact Sheet. Appliance disposal, (1) 1-2.
Martinez, J.L., A. Fajardo, L. Garmendia, A. Hernandez, J.F. Linares, L. Martínez-Solano, and M.B. Sánchez.
2009. A Global View of Antibiotic Resistance. FEMS Microbiol. Rev., 33: 44–65.
Moriarty, E., F. Nourozi, B. Robson, D. Wood, and B. Gilpin. 2008. Evidence for Growth on Enterococci in
Municipal Oxidation Ponds Obtained Using Antibiotic Resistance Analysis. Appl. Environ. Microbiol.,
74:7204–7210.
Nesme, J., S. Cécillon, T.O. Delmont, J.M. Monier, T.M. Vogel, and P. Simonet. 2014. Large-Scale
Metagenomic-Based Study of Antibiotic Resistance in the Environment. Current Biology, 24:10: 1096–1100.
Ochman, H., J.G. Lawrence, and E.A, Groisman. 2000. Lateral Gene Transfer and the Nature of Bacterial
Innovation. Nature, 405: 299–304.
Poonsuk, K., T.C. Tribuddharat, and R. Chuanchuen. 2014. Simultaneous Overexpression of Multidrug Efflux
Pumps in Pseudomonas aeruginosa Non-cystic Fibrosis Clinical Isolates. Canadian Journal of Microbiology,
60(7): 437-443.
Saiman, L. 2004. Microbiology of Early CF Lung Disease. Paediatr. Respir. Rev., 5:367-369.
Topp, E., M. Welsh, Y.C. Tien, A. Dang, G. Lazarovits, and K. Conn. 2003. Strain-dependent Variability in
Growth and Survival of Escherichia coli in Agricultural Soil. FEMS Microbiol. Letters, 44:303–308.
Walsh, C. 2003. Where Will New Antibiotics Come From? Nat. Rev. Microbiol., 1:65–70.
Webber, M.A. and L.J.V. Piddock. 2003. The Importance of Efflux Pumps in Bacterial Antibiotic Resistance.
J. Antimicrobial Chemotherapy, 51 (1): 9-11.
Various Personal Communication
Bernie Campoli, 2014.
Glenn Butler, 2014, 2015.
Website Cited
www.doenetwork.org/cases/518DFNY accessed July 15 2015
39
In: Lobel L.K. ed. Diving for Science 2015.
Proceedings of the American Academy of Underwater Sciences 34th Symposium.
Using Divers and 3D Sonar Technology to Study Historic Shipwrecks in
Lake Michigan
Kira E. Kaufmann
Commonwealth Cultural Resources Group, Inc., 8669 N. Deerwood Drive, Milwaukee, WI 53209, USA
[email protected]
Abstract
Sonar acoustic imaging technology was employed through mobile and diver-deployed
applications to develop two different kinds of three-dimensional models of historic
shipwrecks in Indiana’s territorial waters of Lake Michigan in the United States. Important for
the scientific applications of diving, deployment of sonar equipment by divers was integral to
the accuracy and efficiency of data collection. However, divers did encounter challenges that
were addressed with intensive pre-planning, coordination, and safety measures. AAUS
standards provided a framework to conduct diving activities that assured meeting OSHA
standards. These guidelines were crucial not only to the success of the current project, but to
maintaining a standardization that can be replicated for future projects. These projects were
funded with Section 309 financial assistance to the Indiana Lake Michigan Coastal Program
provided by the Coastal Zone Management Act of 1972, as amended, administered by the
Office of Ocean and Coastal Resource Management, National Oceanic and Atmospheric
Administration, and other sources.
Keywords: acoustic imaging, nautical archaeology, maritime cultural resources
Introduction
In 2013 and 2015, newer applications of remote sensing technology were employed to better define
four archaeological shipwreck sites within Indiana’s territorial waters of Lake Michigan. For the first
time in the Great Lakes region, a mobile three-dimensional (3D) sonar survey was conducted at four
shipwreck sites. Additionally, a diver-deployed 3D sonar survey was conducted at two of these same
shipwrecks. Using diver-deployed techniques provided for increased accuracy in data acquisition.
Further, using diver deployment instead of machine deployment allowed for the discernment of sonar
equipment placement in order to maximize data acquisition while minimizing time conducting
survey. Diver deployment of sonar equipment is one way that scientific diving is advancing the
science of nautical archaeology.
Previous archaeological applications of tripod and mobile sonar technology have employed hoist
systems or remotely operated vehicles (ROV’s) to deploy the sonar equipment at stationary locations
(Dive Training, 2015; National Oceanic and Atmospheric Administration (NOAA), 2015; Van Dover
and Ball, 2015). In 2013, an initial diver-deployed 3D sonar survey was conducted at the site of the
Muskegon shipwreck, the first Indiana shipwreck to be listed in the National Register of Historic
Places (NRHP) (Kaufmann, 2013, 2015). The 2015 sonar surveys included one diver-deployed 3D
sonar survey and four mobile surveys. Because of the dynamic nature of the southern Lake Michigan
basin, and in an effort to obtain more data, most of the 2015 sonar surveys were based from a
completely mobile platform – a moving vessel – in a manner similar to towed side-scan surveys.
However, the sonar head was not towed. Instead, the equipment was mounted directly to the survey
vessel.
40
The goals of these remote sensing surveys were to obtain detailed measurements, gather more
information about site changes, and obtain more detail about the characteristics. Acoustic imaging
with sonar was employed because previous visual survey and digital photography did not effectively
record site features in the low visibility environment. Other challenges of the environment involved
working underwater in very unpredictable waves, extreme cold water temperatures, and potential
entanglement conditions. Safety considerations were a priority because some of the research involved
venturing into interior parts of a historic shipwreck to obtain sonar data. Overall, risk management
was prioritized during the archaeological remote sensing data collection.
Methods
Remote sensing investigations using mobile sonar were conducted at four archaeological shipwreck
sites in Indiana’s territorial waters of Lake Michigan: the Material Service, Car Ferry No. 2, J. D.
Marshall, and the Muskegon (aka Peerless). Additionally, the Muskegon had been surveyed with
diver-deployed remote sensing sonar in 2013 and the Material Service was further surveyed in 2015
using diver-deployed remote sensing sonar. This work contributed to ongoing management of the
sites by collecting information about each site’s current condition (Kaufmann, 2012).
Two different types of 3D sonar survey were conducted. The first was a mobile platform-based sonar
survey from a moving vessel and the second was a diver-deployed sonar survey. Both approaches
utilized a Teledyne BlueView BV5000 high definition, multibeam, 3D scanning sonar operating at
1350 kHz. Prior to scanning, the Teledyne Odom Hydrographic Digibar Pro sound velocity probe was
used to identify the sounding values at the four sites. Consequently, sonar equipment settings were
adjusted to account for site-specific conditions.
The three-dimensional sonar data allow archaeologists to visualize shipwreck features as a point
cloud model which has millions of datum points. Each point in the model has its own unique set of x,
y, and z coordinates. The resulting point cloud data (XYZ) can be depicted either as a twodimensional or a three-dimensional spherical image to produce plan and cross section views of each
shipwreck site. The resulting models also allow for the measurement of site characteristics, as well as
a more accurate assessment of size and configuration of each ship structure, the site, and other bottom
landscape features including debris fields.
Mobile Sonar Survey
Mobile sonar survey was conducted at all four archaeological sites in 2015. During the mobile sonar
survey, an onboard computer navigation and data integration system was interfaced with a
Differential Global Positioning System (DGPS) to maintain locational accuracy. The DGPS system
employed a base station on shore that was connected to the vessel sonar equipment through high
frequency antennas (Figure 1). Additionally, HYPACK® hydrographic survey software was used as a
navigation system to guide the survey vessel along manually determined survey lines spaced
approximately 15 feet (ft) (4.6 meters [m]) apart. During mobile survey, the maximum range of the
BV5000 is generally 100 ft (30.5 m) and the average effective range is 70 to 80 ft (21.3 to 24.4 m)
(Hartzell and Forsyth, 2015). However, for these surveys, the effective range was set to 60 ft (18.3
m). A total of 134 mobile sonar transects were conducted for the four sites.
41
Figure 1. Crew members set up a base station with frequency antennas close to shore, prior to mobile sonar
survey, to establish locational accuracy (Used with permission, Indiana Department of Natural Resources).
Initial (2013) Diver-Deployed Sonar Survey
Initial diver-deployed sonar survey was conducted at the site of the Muskegon in the spring of 2013
(Kaufmann, 2013a). The sonar was equipped with pan and tilt assembly that was mounted on a tripod.
The tripod and sonar assembly were initially deployed to the lakebed from a small vessel, but then
subsequently moved manually by divers to each scan location. The sonar survey was conducted so
that survey cones (or paths of the sonar signal) were overlapped, providing 100 percent coverage of
the main portion of the shipwreck structure and immediately adjacent debris field. The sonar unit
itself was placed at regular intervals around the entire exterior of the mainframe of the Muskegon
shipwreck. Each scan location was measured using a tape measure and ranged from 15 to 25 ft (4.6 to
7.6 m) apart for comprehensive sonar coverage. The sector scan unit was placed at the bottom of the
lakebed in water depths from 22 to 29 ft (6.7 to 8.8 m). During the initial diver-deployed survey, 19
sonar placements were made. Two divers conducted a total of 21 dives to secure the survey vessel
and conduct sonar placement.
2015 Diver-Deployed Sonar Survey
Diver-deployed sonar survey was conducted at the Material Service in the spring of 2015. During
these recent investigations, the survey vessel was secured to a single location. Direct diver-deployed
sector scan sonar survey was conducted using a tripod-mounted sonar with umbilical cables that
connected topside to the survey vessel. Two divers moved the BlueView sonar tripod to depth from
the surface with the assistance of the topside crew. While at depth, the dive team manipulated the
equipment between placements by lifting the unit manually and with a small lift bag. This diver-
42
deployed sonar survey was more complex because of the necessity to penetrate the interior of the
shipwreck to deploy the equipment. The sonar unit was manually placed at the bottom of the lakebed
in water depths from 31 to 37 ft (9.5 to 11.3 m) along 40 ft (12.2 m) intervals around a portion of the
exterior of the mainframe of the Material Service shipwreck. Additionally, the sonar equipment was
manually placed at regular intervals within the interior of the cargo hold at 30 ft (9.1 m) intervals.
Because the sonar equipment was manually placed and moved, diver observations confirmed correct
placement of the unit. During the diver-deployed survey, 20 placements were made based on the
results of the previous mobile sonar survey. Three divers conducted a total of 24 dives to secure the
survey vessel and conduct sonar placement.
Pre-Planning
Pre-planning addressed diver competency and survey procedures. Diving techniques focused on the
capacity of divers to manage their own buoyancy as well as managing cumbersome equipment while
underwater. In addition to buoyancy control, entanglement was a concern because the sonar
equipment was connected by cables to a surface support station. Therefore, prior to diving activities, a
draft site plan developed from the mobile sonar survey was used to plan manual sonar placement by
divers (Figure 2).
Figure 2. Draft mobile sonar survey results that were used to establish the plan for diver-deployed survey.
Coordination
Coordination included ensuring that there was always surface support for divers entering and exiting
the water. Coordinating sonar movement, sonar placement, and sonar cable placement ensured that
there were no issues with equipment such as inadvertent damage or issues with divers, such as
entanglement. Communication (verbal and hand signals) prior and during diving activities facilitated
the coordination during survey work.
43
Safety Measures
General categories of potential issues for scientific divers include: Water quality (visibility, currents,
surge, temperature); biological hazards (hydroids stings, mammal or fish encounters/bites); site
conditions (sharp structural edges, collapsing decking, entanglements); equipment issues (both for the
diver and the sonar equipment - malfunction); and diving schedule limitations (time in water, depth of
water). Safety measures instituted included safety/standby diver preparedness and safety training.
The most important water quality hazard for this project was extreme cold water temperatures
because these could affect diver stamina and efficiency. Guaranteeing that divers dressed with
sufficient thermal protection for cold water diving was an important consideration for diver safety.
When severe weather or rough waves were experienced, diving operations were postponed.
Biological hazards for scientific divers during this project included the potential of cuts by
zebra/quagga mussels. Site hazards for scientific divers during this project included the potential for
abrasion or puncture wounds from jagged and broken ship structure. Other site hazards were
addressed by using an additional safety line to ensure diver location when visibility underwater
diminished or when divers were near potential entanglements that could hinder divers and potentially
damage equipment during the manual placement of the sonar equipment (Figure 3). Potential
equipment issues were addressed by providing standby/safety divers, testing all equipment prior to all
diving activities, having spare equipment, conducting safety checks, and ensuring diving staff was
prepared with equipment that had redundant air support. All divers and boat crew members were
previously trained in First Aid, CPR, AED, and emergency oxygen use through reputable training
agencies. Diving schedule limitations were addressed by providing multiple means for air, time and
depth management during diving activities, by using both analog and computer gauges, and by diver
check-in procedures.
Figure 3. A diver stabilizes sonar equipment after placement during the diver-deployed survey (Used with
permission, Indiana Department of Natural Resources).
44
Results
Following established scientific diving guidelines provided a framework for small private research to
work effectively. Ultimately, the scientific diving facilitated the efficient collection of data that was
then used to develop two different kinds of three-dimensional computer modeling platforms for the
historic shipwrecks: sonar-generated point clouds and animated web-based 3D computer models.
Both types of sonar data (from mobile and diver-deployed survey) reveal additional detail about the
shipwreck sites, but the diver-deployed survey provided the opportunity to acquire much more detail
than was possible through just the mobile survey. For example, the diver-deployed survey revealed
the accurate orientation of the shipwreck the Muskegon and where along the structure of the ship an
invasive, modern pipe was located. Diver-deployed survey at the Material Service revealed damage
that had occurred at the time of sinking and when the wheelhouse was removed, unrecorded details of
the interior, and the intricacy of the debris scatter on top of the stern deck (Figure 4).
Figure 4. The point cloud model of the Material Service depicts previously unrecognized ship structure and
features in the debris field (Used with permission, Indiana Department of Natural Resources).
The diver-deployed sonar survey provided the detailed data that supplemented the creation of webbased animated computer models. The web-based shipwreck computer models (Figure 5) can be
accessed through: http: www.indianashipwrecks.org. The resulting compilation of remote sensing
technology and computer modeling provides new information about previously unrecognized site
limits, site conditions and existing artifacts. These new perspectives allow for better assessment of the
sites as part of a regular management program.
45
Figure 5. The web-animated computer model of the Material Service provides non-divers and members of the
public the opportunity to virtually visit the shipwreck
(Used with permission, Indiana Department of Natural Resources).
In conclusion, the diving techniques used for this diver-deployed sonar survey were successful
because of the implementation of AAUS diving guidelines in pre-planning, coordination and safety
measures that were adhered to throughout each diver-deployed sonar survey. The scientific
contribution of diver-deployed survey has been the ability to acquire detail of shipwreck features that
is not possible through mobile sonar survey or other means.
Discussion
In the private sector, project and time constraints dictate which kinds of staff are available for diving
activities. For example, contract projects that occur during active academic sessions cannot have their
schedules altered in order to employ students or faculty who are AAUS certified scientific divers.
Thus, private employers have relied on nationally recognized diver training agencies for staff.
Although AAUS training has expanded, become more recognized, and more individuals have become
AAUS certified scientific divers, the reliance on nationally recognized diver training agencies has
continued. However, AAUS standards are frequently used by small archaeological consulting
companies to provide a framework for conducting diving activities under exemption from OSHA
commercial-diving regulations, but assuring OSHA standards. These standards are crucial not only to
the success of a project, but to maintaining a standardization that can be replicated for future projects.
Supplementing adherence to AAUS guidelines, this archaeological project identified potential
planning, coordination, and safety issues for scientific diving personnel prior to in-water activities.
46
Impact of Employing Scientific Diving and AAUS Guidelines in the Private Sector
The AAUS guidelines provided a baseline from which to evaluate divers and their competency to
collect data in a safe and efficient manner (American Academy of Underwater Sciences [AAUS]
2006, revised 2011). Also, the guidelines are a framework, helpful in preparing divers for specific
tasks. The pre-planning stage was necessary to develop effective survey procedures that would
maintain the safety of the divers collecting the data. Assuring that there was always surface support
was crucial to divers entering and exiting the water with equipment. Additionally, coordinating sonar
movement between divers and the topside survey vessel ensured smooth transitions as the data was
collected. Instituting safety measures such as these contributed to effective risk management.
Acknowledgments
The author acknowledges the professional support of Michael Molnar, Program Manager of the
Indiana Department of Natural Resources, Lake Michigan Coastal Management Program, Cathy
Draeger-Williams, Archaeologist, Indiana Department of Natural Resources Division of Historic
Preservation and Archaeology, Chris Hartzell, of Collins Engineering, Michael Haynes and John
Shuder of the Underwater Connection.
Literature Cited
American Academy of Underwater Sciences. 2006 (revised 2011). Standards for Scientific Diving Certification.
Dauphin Island, Alabama.
Dive Training. 2015. 50 Years after Sinking, Aircraft Carrier ‘Amazingly Intact’. Dive Training, June 2015, pp.
18.
Hartzell, C., and R. Forsyth. 2015. Multibeam Procedures. Collins Engineering, Inc., Milwaukee, Wisconsin.
Kaufmann, K.E. 2012. Management Plan for Submerged Cultural Resources within Indiana’s Territorial
Waters of Lake Michigan. R-0986. Commonwealth Cultural Resources Group, Inc., Jackson, Michigan.
Kaufmann, K.E. 2013. Draft Stabilization Plan for the Muskegon Shipwreck (12LE0381) Archaeological Site
within Indiana’s Territorial Waters of Lake Michigan. WR-0743. Commonwealth Cultural Resources Group,
Inc., Milwaukee, Wisconsin.
Kaufmann, K.E. 2015. The Muskegon Shipwreck in Lake Michigan: Modeling Three-Dimensional Sonar Sector
Scan Data for Archaeological Applications Including Identification, Analysis, and In Situ Management.
Advisory Council on Underwater Archaeology (ACUA) 2014 Underwater Archaeology Proceedings, 2014:383389.
National Oceanic and Atmospheric Administration (NOAA). 2015. USS Independence (CVL 22). Electronic
document, http://sanctuaries.noaa.gov/shipwrecks/independence/independence_fact_sheet.pdf. accessed July
2015.
Van Dover, C.L., and B. Ball. 2015. Centuries-old Shipwreck Discovered off North Carolina Coast. Electronic
document, https://nicholas.duke.edu/news/centuries-old-shipwreck-discovered-north-carolina. accessed July
47
In: Lobel L.K. ed. Diving for Science 2015.
Proceedings of the American Academy of Underwater Sciences 34th Symposium.
Choosing Organisms for Monitoring Contaminant Exposure on Coral
Reefs: Case Studies from Johnston Atoll, Central Pacific Ocean
Lisa K. Lobel1*, Phillip S. Lobel2
1
Wheelock College, Department of Math & Science, 200 Riverway, Boston, MA 02215, USA
[email protected]
2
Boston University, Department of Biology, 5 Cummington Mall, Boston, MA 02215, USA
*
presenting and corresponding author
Abstract
The most crucial decision when designing a sampling plan for determining contaminant or
toxin accumulation in fishes is the correct selection of species. Choice of species based on
trophic guild alone can produce dramatically different uptake results due to variation in
feeding modes and digestive morphology. For example, differences in herbivorous fish gut
morphology, types of algae ingested, and whether food is ingested with sand or not, can
determine levels of accumulation or transformation of toxic compounds. Continued
quantification of anthropogenic contamination and toxin accumulation in coral reef
environments is a key step in linking exposure to measured ecological impacts. Our
experience is based upon 20 years of research and sampling surveys of metal, organic and
radionuclide contamination in both sediments and biota at Johnston Atoll, Central Pacific
Ocean. Using these environmental investigations as case studies, we outline important factors
to consider when choosing organisms in terms of understanding potential exposure and
ultimately effects. These factors range from contaminant class and exposure pathways to
having a solid understanding of the target organism’s ecology including abundance, trophic
level, type of herbivory, age vs. size and territoriality. This paper will define a suite of
biological factors to consider when assessing fishes that might serve as indicators for toxin
and contaminant uptake and impacts on reefs.
Keywords: bioaccumulation, metal contamination, organic contamination, radionuclides, reef
fish, indicator organisms, coral reef contamination, reef health
Introduction
Pollution is one of the many stressors impacting the health of coral reefs (Burke et al., 2011; Halpern
et al., 2008). While there are entire programs (e.g. NOAA National Status and Trends) dedicated to
measuring distribution and trends in contamination, the primary interest is aimed at determining at
what concentration or threshold these contaminants have a distinct negative impact; resulting in
biological or ecological responses linked to the chemical contaminants (GESAMP, 1995; Wu et al.,
2008). Due to the expense of chemical analyses and the increase in the production and use of
thousands of new chemicals released into the environment, researchers seek quicker and simpler
methods to assess anthropogenic stressors through the use of biological indicator organisms. These
indicator organisms (or functional groups) integrate exposure spatially and temporally (the “dose”),
while a biological or ecological change is measured as the “response”, thus “indicating” what
contaminants or other stressors are available and impacting the organisms. The interest is in using
these indicators to determine if contaminants are posing a risk to ecological and/or human health
(Bartell, 2006; Green and Bellwood 2009; Linton and Warner, 2003).
48
Terms such as biomarkers and bioindicators, as well as contamination and pollution are often used
interchangeably leading to some confusion. The occurrence of contaminants in the environment does
not represent pollution unless some level of adverse biological change is documented as a result of
the contamination. Additionally, biomarkers are often defined as a measure of exposure at the suborganismal level, while indicators indicate exposure and impacts at higher levels of organization
(Bartell, 2006). As such, biomarkers and bioindicators are assessing the biologically available portion
of environmental chemicals, also integrating exposure to complex chemical mixtures and natural
environmental stressors. In order for these indicators to be used as proxies for organismal and
ecological well being, the indicators should be biologically, methodologically and socially relevant
but most importantly require scientific testing of the relationship between the stressor and the change
in the indicator (Bartell, 2006; Goodsell et al., 2009).
Necessary criteria for organisms to serve as indicators of contaminant impacts are not often met,
including 1) strong and consistent correlation between biological/ecological changes and levels of
environmental stressors, spatially and temporally, 2) the correlation must be tested to determine the
causal relationship between the biological parameter and stressor, and 3) the organism responds
directly and predictably to the change in the environmental stressors (Goodsell et al., 2009). Many
indicators fail at the first criterion, due to poor correlation. The difficulty in providing the necessary
links between contamination and biological effects is most often due to high levels of variability
resulting in these weak and inconsistent correlations between the stressor and the effect (Goodsell et
al., 2009). The purpose here is to not propose yet another indicator or suite of indicators but to
highlight biological factors that may help increase variability in contaminant concentrations thereby
causing difficulty in linking contaminant concentrations to measured biological effects. Consideration
of these factors during planning phases and incorporating these variables as co-variates would
improve correlations between contaminant levels and measured effects.
In addition, the utility of a particular indicator species depends on the determination of appropriate
baseline and effect levels to allow comparison as well as determination of predicted no effect
concentration for the development of environmental quality guidelines specific to tropical reef
ecosystems. Each new study seems to propose a new indicator. Consistent, appropriately replicated
data on the same or functionally similar species, through time, at differing locations are needed to
build a database required to determine predicted no effects concentrations (e.g. Long et al., 1998). In
other words, it would be beneficial for all reef studies to sample the same (or functionally equivalent)
species across a wide range of investigations so that large-scale patterns and processes could be
elucidated. Recommendations for sampling fish species representing organisms with the highest
potential for exposure are given based on work for an ecological risk assessment conducted at
Johnston Atoll.
Case Study: Johnston Atoll, Central Pacific Ocean
The following will describe several biological factors taken into consideration when we selected
species to sample for the exposure and risk characterizations for an ecological risk assessment at
Johnston Atoll. The focal organisms chosen for sampling were fishes and based upon their sensitivity
to water quality and their potential for use as widespread “indicators”. Additionally, contaminants
measured in fishes can often serve the dual role of being used for both ecological and human risk
assessment. In this case, in addition to ecological risk, there was concern over risk to humans who
may consume contaminated fishes.
Johnston Atoll (160 43.6’ N, 1690 31.5’W) is located in the Central Pacific approximately 1,287 km
(800 miles) southwest of Honolulu, Hawaii and 1,440 km (900 miles) north of the Line Islands of
Kiribati (Figure 1). The nearest landfall is French Frigate Shoals, 804 km (500 miles) north. Johnston
Atoll was under military control for approximately 70 years, ending in 2003. During those years the
49
Atoll was used extensively as a refueling site, atmospheric nuclear testing, master LORAN station for
the Pacific, storage site for unused herbicide orange (“agent orange”), chemical weapons storage, and
the prototype incineration facility for the destruction of chemical weapons in the Johnston Atoll
Chemical Ammunition Disposal System (JACADS) (Lobel 2003, Lobel and Lobel 2008).
Many of these activities as well as infrastructure needed to support a military and civilian workforce
of up to 2000 people contributed to soil and sediment contamination within the atoll (Lobel and Kerr
2002). Polycyclic aromatic hydrocarbon, petroleum hydrocarbon and metal contamination was
associated with refuse burning, fire training operations and fuel storage. Organochlorine
contamination due to leakage from discarded electrical equipment, transformers, polychlorinated
biphenyl (PCB) contaminated fuel and herbicide orange (HO) were the main contaminants of
potential concern (COPC) due to accumulation in top predators and potential toxicity. Herbicide
orange contains two active ingredients, the n butyl ester of 2,4- dichlorophenoxyacetic acid (2,4- D)
and 2,4,5-trichlorophenoxyacetic acid (2,4,5-T), and 2,3,7,8- tetrachlorodibenzo-p-dioxin (TCDD) as
a contaminant in the mixture. Polychlorinated biphenyls were found mainly in two areas of the
lagoon, the west end of Sand Island and in the former Navy Pier (tank 49 lagoon) area on Johnston
Island. Polychlorinated dibenzo-p-dioxin and dibenzofuran (PCDD/PCDF) contamination in soil and
nearshore sediments of the northwest corner of Johnston Island were due to leaks from corroded
storage drums containing herbicide orange (Lobel and Kerr, 2000). Most of this contamination
occurred before modern day environmental regulations were developed.
Figure 1. Aerial view of Johnston Atoll. Photo © P. Lobel
Of the nuclear tests that occurred on Johnston, four were aborted and two of these would have
contributed to the dispersal of radionuclides into the lagoon. Debris and residual plutonium from the
STARFISH event that aborted at 30,000 feet, landed in the water surrounding Johnston Island (JI) and
on adjacent Sand Island. The BLUEGILL PRIME event scattered radioactive material primarily
downwind of the launch emplacement on Johnston Island. The residuals were, the five isotopes of
plutonium (238, 239, 240, 241, and 242) found in Weapons Grade Plutonium (WGP) as well as
americium-241 (Johnson et al., 1997; Kerr Lobel and Lobel, 2009).
Contaminants of Concern
Contamination of marine sediments by organic and metal compounds resulted from soil transport
(wind or rain erosion runoff) into the nearshore marine environment, marine disposal of used
50
equipment (batteries, transformers), leakage from fuel storage tanks, and fallout in the case of the
radionuclides resulting from the aborted tests (Lobel and Kerr, 1995).
Identification of Ecological Receptors
Understanding the species present and their biology is critical in designing an effective study.
Potential aquatic receptors were identified from studies and lists of known species within the atoll
(Irons et al., 1985; Randall et al., 1985). Since the contaminants of concern (organochlorines, metals,
radionuclides) were associated with sediments, the most likely receptors included organisms that live
in, come in contact with, ingest sediments or that feed upon other organisms that are direct receptors.
Fishes were the chosen as the focal organisms because they are abundant and easily observed on the
reef. While not specific to coral reef fishes in general, fishes accumulate contaminants and they have
been found to be extremely sensitive, especially to dioxin and dioxin “like” compounds (Peterson et
al., 1993).
Exposure Pathways
A complete exposure pathway was defined as having the following factors: 1) a source and
mechanism of chemical release into the environment; 2) a chemical transport medium or mechanism
(soil or sediment movement); 3) a point of contact; and 4) an uptake mechanism, i.e. ingestion,
dermal contact (Lobel et al., 1997).
In the near shore marine environment within the atoll, it is assumed that hydrophobic compounds
such as PCBS, dioxins and furans are introduced by soil transport or runoff. These compounds are
bound to particulate matter and sink rapidly. Once integrated into the sediments, particle bound
contaminants can be consumed by detritivores and other organisms feeding on organic material.
These organisms are secondarily consumed by reef invertebrates and fishes that can accumulate high
concentrations of the contaminants within their tissues. Certain organisms are believed to be at a
higher risk based on spatial and temporal scales of residence at the contaminated site. Marine animals,
which are most likely to have the greatest exposure to chemical contamination, have the following
characteristics:
•
•
•
•
•
Feed directly on algae or sediments or is a predator on other animals that consume these foods.
Resides for its lifetime in a limited territory or home range that can be delineated relative
to a specific zone of exposure or non-exposure.
Have a population containing an abundant number of individuals so that collecting itself
does not adversely impact the species.
Test organisms should be of sufficient biomass for chemical analysis.
The biology of the organism should be reasonably known for a proper interpretation of
results.
Some background information on reef fishes organized by trophic level follows, with specific
examples of species that would make ideal choices for measuring contaminant exposure in reef
environments when considering other factors such as territoriality, exposure potential abundance and
fish size.
Herbivorous Fishes
The bulk of the animal biomass on coral reefs is composed of herbivorous species. Thus, most edible
algae are rare and constantly cropped to a growth of low micro-turf algal stubble (Ogden and Lobel,
1978). Coral reef fish faunas typical include all the types of herbivorous fishes (e.g. parrotfish,
Scaridae; surgeonfish, Acanthuridae; blennies Bleniidae; damselfishes, Pomacentridae; mullets.
Mugilidae; rabbitfishes Kyphosidae, etc.). Herbivores most likely to be directly exposed to
51
contaminants in marine sediments are “grazer” herbivores that also consume sand or dead coral
skeletons with its plant material diet (Lobel, 1980). In contrast, browser herbivores consume
primarily algae. These different herbivore types differ in their gut morphologies and how food is
digested potentially impacting contaminant uptake (Figure 2). Browsers have thin walled stomachs
and use acid lysis to digest their algal diets (Horn, 1989; Lobel, 1981). Grazers have thick walled,
gizzard like stomachs with a neutral pH. Grinding of stomach contents with ingested sediments in
fishes with thick-walled stomachs has been hypothesized to aid in the digestion process (Horn, 1989;
Lobel, 1981). Parrotfishes (Scaridae) lack stomachs, grinding their food in their pharyngeal mills
(Horn, 1989; Lobel, 1981). Finally, rabbitfishes (Kyphosidae) may ferment their algal food in their
hindgut (Horn, 1989). Furthermore, differences in these species have been recorded in regard to
toxicity from the ciguatoxin produced by the benthic dinoflagellate, Gambierdiscus toxicus
(Anderson and Lobel, 1987; Figure 3). The ciguatera dinoflagellate was distributed throughout the
Johnston Atoll lagoon (Richlin and Lobel, 2011). Ingestion and defecation of plants on reefs by
herbivorous fishes also contribute to the production of the chemical, dimethysulfide on reefs (Darcey
et al., 1994) but how this may react to other chemicals in their gut is unknown.
Figure 2. The different gut morphologies in herbivorous fishes. Modified from Horn 1989.
52
Figure 3. Differences in toxicity due to ciguatoxin in herbivores with different alimentary morphology. Top.
The browser, Acanthurus triostegus has a thin-walled, acidic stomach, long intestine and low toxicity from
ciguatoxin. Middle. The grazer, Ctenochaetus strigosis has a thick-walled, gizzard-like stomach, long intestine
and is highly toxic from ciguatoxin being converted into maitotoxin. Bottom. The grazer, Scarus sordidus has a
pharyngeal mill, no stomach, a moderately long intestine and is highly toxic from ciguatoxin being converted
into scaritoxin. Photos © P. Lobel.
Browsers, or herbivores feeding solely on fleshy algae are expected to be at risk of contaminant
exposure through ingestion of marine algae only when that alga specifically accumulates
contaminants. Because organic and metal contaminants are associated with sediments, grazer fish are
more likely exposed through the processing of contaminated sediments as well as potentially
contaminated algae. The browser surgeonfish, Acanthurus triostegus feeds on filamentous algae while
the grazer, Ctenochaetus strigosus feeds on organic detritus, sediments and microalgal filaments
(Figure 4). Both of these species have the ability to accumulate contaminants and have had organic
and radionuclide contamination measured within their tissues (Lobel and Lobel, 2009). Other grazers
at Johnston Atoll are species of parrotfishes (Scaridae; Figure 5).
53
Within Johnston Atoll, the surgeonfish Ctenochaetus strigosis and the parrotfish, Scarus sordidus are
the first and second most abundant and numerous of all species (Irons et al., 1989). Thus, these fishes
are the best species for assessing contamination since both are benthic feeders that graze microalgae
while also ingesting quantities of benthic material with their food and are abundant enough for
sampling at specific sites and over a wide geographic range. Functional equivalents of these species
can also be found in other regions (see Figure 4).
Figure 4. Herbivorous fishes with differing feeding modes and gut morphologies. A and B are found in the
Pacific with their functional equivalents C and D, in the Caribbean. A. Acanthurus triostegus, a browser
with a thin walled, acidic stomach, feeds on filamentous algae. B. Ctenochaetus strigosis. a grazer with a
thick walled, gizzard like stomach, feeds on microalgae mixed with fine grain sand particles, also
ingesting sediment along with its food. C. Acanthurus bahaianus, a browser with a thin walled, acidic
stomach, feeds on filamentous algae. D. Acanthurus chirurgus, a grazer with a thick walled, gizzard like
stomach, feeds on microalgae mixed with fine grain sand particles, also ingesting sediment along with its
food. (Photos © P. Lobel).
Figure 5. The bullethead parrotfish, Scarus sordidus. Photo © P. Lobel.
54
Planktivores
Planktivores would be expected to have a low risk of exposure since they are feeding on plankton
suspended in the water column. It may be possible that bioaccumulation can occur if plankton feed on
suspended contaminated organic carbon or from contaminated particles from the sea surface
microlayer. But given dispersal in ocean currents and widely variable flow patterns, exposure is
unlikely to be site specific. Some planktivorous damselfishes are highly site specific and are also
benthic spawners (Figure 6). This level of site specificity may increase exposure to some
contaminants and benthic eggs may also be exposed through contact with the substrate.
Figure 6. Top. Abudefduf abdominalis is a planktivorous damselfish that roams the reef during the day and
shelters in the reef at night. Bottom. Dascyllus albisella is a highly territorial and site-specific damselfish that
can live within the same coral head for its entire life. Both species spawn benthic eggs on dead coral surfaces.
Photos © P. Lobel.
Omnivores
Omnivorous fishes are basically carnivorous but include plant and other material in the diet, often
obtained incidental to consuming some small animal prey. Omnivores vary feeding among a variety
55
of reef surfaces and even on plankton in the water column. Some omnivorous fishes feed on
microinvertebrates living in marine sediments.
Omnivorous damselfishes such as the Pacific species, Abudefduf sordidus have high potential for
accumulating contaminants (Figure 7). This large, territorial species feeds on both algae and benthic
invertebrates, consuming sediments along with its prey. Fishes that are territorial, remaining in one
patch reef for their entire lives and that feed on algae and invertebrates are likely to be accumulators
of contaminants that occur in sediments and are mixed with algae. This species often chooses
artificial substrates for spawning, and is frequently found spawning on piers and other debris
associated with contamination, which could increase exposure for this species (Lobel and Lobel,
2013).
Figure 7. Top. Abudefduf sordidus, a damselfish from the Pacific that is a benthic omnivore and also ingests
sediments with its food. Photo © P. Lobel. Bottom. Abudeduf taurus, the functional equivalent of A. sordidus in
the Caribbean. Photo by J.E. Randall from FishBase (http://www.fishbase.org).
Carnivores
Carnivores, of course, consume primarily other animals. On coral reefs, carnivorous fishes may either
eat invertebrates only, fishes only, or a combination of invertebrates and fishes. Among the types of
fishes most likely to be directly exposed to contaminants present in marine sediments are those
species that feed on the invertebrate infauna. Fishes such as goatfishes (Mullidae) feed by gulping
mouthfuls of sand containing resident microinvertebrate infauna, which are filtered out by the gill
rakers and swallowed (Figure 8). These fishes feed exclusively on benthic invertebrates and are likely
to accumulate contaminants. They are at high risk if sediments are contaminated. However, their
56
abundance can vary, with different species occurring in different microhabitats. Goatfishes have been
shown to accumulate heavy metals and have been suggested as indicators of contamination elsewhere
(Hernandez et al., 1992).
The squirrelfishes, family Holocentridae. These fishes are nocturnal predators that feed on small
crustaceans, worms and, occasionally, small fishes. At Johnston Atoll, a squirrelfish, Sargocentron
diadema, contained the highest dioxin concentration measured in a fish during the early sampling. A
related (same family) species, Myripristis berndti, is a prized food fish. Unfortunately, these species
are not as abundant as some of the herbivores; therefore few holocentrids could be sampled at specific
reef sites.
Higher-level carnivores are of interest for understanding accumulation at the top of the food web, but
consideration of the home ranges of these species is necessary. For example, transitory species visit
many areas of the atoll during the course of their life. As roving predators, species such as a jack
(Carangidae) may only experience momentary exposure as it swims through a contaminated area
(Figure 9). They are at low risk of exposure to contaminant bioaccumulation through the food chain
due to their feeding in multiple and wide-spread locations. Intermediate ranging species are likely to
stay within 2 km of a given home area with bottom features such as channels acting as boundaries to
their range.
Figure 8. Some examples of carnivorous Pacific goatfishes, A. Parupeneus bifasciatus, B. Parupeneus
multifasciatus, C. Mulloidichthys flavolineatus, D. Mulloidichthys vanicolensis. Photos © P. Lobel.
Triggerfishes are territorial, demersal spawners and benthic carnivores feeding on infaunal
invertebrates (Figure 10). While these characteristics make some species of triggerfishes ideal
candidates for monitoring contaminant uptake, these species are not as abundant on the reef.
Demersal or substrate spawners, like triggerfishes, that lay their eggs in the sediment, expose their
embryos directly and these embryos are suspected to be the most affected by exposure to
contaminated sediments. The embryos of broadcast spawning species would be much less susceptible
57
to contaminant exposure than those of demersal spawners since their eggs are broadcast into the
plankton where they drift in water currents. However, the embryos from broadcast spawning species
are at greater risk to those chemicals that form a surface film and which are concentrated in the ocean
surface microlayer.
Site attached species are bottom-dwellers that settle from the plankton, the stay within an approximate
area of 10 m2. Fishes such as gobies (Gobiidae) and the herbivorous blennies (Blenniidae) are site
attached and often live in direct contact with and nest in sediments where they can receive chronic
doses of contaminants (Figure 11). Their potential exposure is high. However, the small size of these
fishes does not provide enough material for contaminants analysis and would require pooling of
multiple individual fishes per sample.
Figure 9. A large roving predator, the jack, Caranx melampygus. Photo © P. Lobel.
Figure 10. An infaunal carnivore, that also lays eggs in a benthic nest on sediments. The triggerfish,
Rhinecanthus aculeatus. Photo © P. Lobel.
58
Figure 11. The site-specific goby, Gnatholepis cauerensis, lives in direct contact with and spawns in the
sediment. Johnston Atoll. Photo © P. Lobel.
Coralivores
Coralivores represent an extreme trophic specialization of a carnivore (Figure 12). Feeding on living
corals requires a specialized cranial and alimentary morphology. Butteflyfish abundance has been
proposed as indicator of change on coral reefs (Crosby and Reese, 1996). However, butterflyfish are
targets of aquarium fish collectors and respond indirectly to stressors since they respond to changes in
coral cover, not necessarily the stressor itself. While contaminants have been found in coral tissue,
these organisms are not expected to accumulate levels of contaminants as high as species feeding in
the sediment (Guzman and Garcia, 2002; Haynes and Johnson, 2000).
Figure 12. A coralivorous butterflyfish, Chaetodon citronellus. Photo © P. Lobel.
59
Additional Consideration of Exposure Duration and Age
In some tropical coral reefs fishes, particularly in the surgeonfishes (Acanthuridae), fish size is not a
good predictor of age (Choat and Robertson, 2002). These species exhibit rapid early growth,
reaching adult size and then somatic growth stops. For schooling surgeonfish, this could result in
multiple age classes of the same size living together. Surgeonfishes are also relatively long lived.
Estimates of maximum life spans for Ctenochaetus striatus are from 28-36 years. Acanthurus lineatus
is estimated to live for 42 years and the longest-lived species Naso hexacanthus and N. vlamingii
achieving ages of 44 and 45 years respectively (Choat and Robertson, 2002). The longer-lived species
in the snapper genus Lutjanus have similar growth patterns to surgeonfishes, completing most of their
growth within the first 15% of their life span (Choat and Robertson, 2002). In contrast, parrotfishes
(Scaridae) and groupers in the genus Plectropomus have shorter life spans with size being a better
predictor of age (Choat and Robertson, 2002).
As exposure time increases with age, this could have significant impacts in the interpretations of
contaminant data measured in these fishes. Exposure and contaminant uptake in fishes living in
contaminated areas aged two years as compared to 20 years of age will vary dramatically. Therefore
consideration of the relationship between size and age in the species being monitored is an important
factor when interpreting contaminant data. Having age data for fishes sampled from contaminated
locations could help explain high levels of variation by incorporating exposure time into the analyses.
However, field studies of contamination in fishes rarely determine the age of the fish sampled.
In one study of three co-occurring mullet species, PCB concentration increased with age in one
species but not the other two, suggesting that different species were located in different habitats, or
spent more time in contaminated habitats during their juvenile stages (Baptista et al., 2013).
Otoliths were removed from all fishes sampled at Johnston Atoll. However the analysis of otoliths is
time consuming and particularly difficult for tropical species. Age analysis was only completed. so
far, for a limited sample of the damselfish, A. sordidus, and there was no relationship between PCB
contamination and age (Kerr et al., 1997). While the overall sample size was small (N = 19), and even
smaller from the contaminated site (N = 5), the age distribution was narrow (ages 6-9 years) and the
fish tissue concentrations highly variable. Regardless, other factors such as territoriality, and sex need
to be considered in future studies with much larger sample sizes.
Impacts
The ultimate goal of the study was to provide data for the ecological risk assessment and therefore
provide an estimate of ecological risk due to the contaminants measured in sediment and biota around
the atoll. As was the case for other tropical environments, contaminant data were compared to the
best environmental quality guidelines available at the time, the ERL and ERMs developed by Long et
al. (1988) based mostly on data from temperate organisms with high levels of uncertainty (NOAA,
1999a, b). These screening guidelines are intended to be used as informal tools to determine the
potential for toxicity in the environment (Long and MacDonald, 1992).
Discussion
Recommended fish species for monitoring contaminant uptake on coral reefs include those with direct
exposure through the consumption of contaminated sediments such as the abundant, herbivorous
grazing species such as Ctenochaetus strigosis in the Pacific and Acanthurus chirurgus in the
Caribbean. Species in the goatfish family (Mullidae) are recommended due to their consumption of
invertebrate infauna species and relatively small home ranges. Omnivorous damselfishes, are large
bodied damselfish, are territorial and therefore have small home-ranges, are benthic spawners, ingest
60
sediment and often prefer artificial substrates that may be associated with contamination (Lobel and
Lobel, 2013). In the Pacific, the recommended damselfishes are Abudefduf sordidus or A.
septemfasciatus with A. taurus in the Caribbean. Functional equivalents of these species can be found
in other regions. Size must be taken into account in terms of the sample mass required for analysis but
care must also be taken with those species where size is not a good indicator of age.
Contamination of reef habitats also results from global transport and deposition, ocean based sources,
runoff due to coastal development and deforestation, in addition to direct local inputs from sewage,
agricultural and industrial activities. While it is important to continue to characterize contaminant
levels in reef environments and organisms, linkages between specific contaminants and biological
effects, producing environmental quality benchmarks specific to tropical marine environments are
still needed.
Assessing potential impacts of chemical contaminants in coral reef environments has been difficult
due to a lack of baseline monitoring criteria as well as appropriate benchmarks for risk assessment
(Jameson et al., 1998). It is not known whether tropical organisms respond to xenobiotics in a similar
manner or at similar concentrations as temperate organisms (Johannes and Betzer, 1975). While there
are many, extensive, coral reef monitoring programs most have quantified ecological responses such
as trends in coral cover and diversity but do not quantify specific stressors (Peters et al., 1997).
Therefore, knowledge of concentrations in the field at which adverse effects are observed is limited
(Peters et al., 1997; Whitall et al., 2014). Continued quantification of contaminants in a consistent
suite of organisms simultaneous with measured biological responses is required to establish strong
and consistent correlations between the response and the contaminant. With experimental validation
of a direct, causal relationship, these taxa could be used as reliable indicators of environmental
impacts (Goodsell et al., 2009; Underwood and Peterson, 1988).
Acknowledgments
This work was supported by funding from the USAF Pacific Command as part of the Former
Herbicide Orange Storage Site Environmental Restoration Program, by the US Army Chemical
Demilitarization activity as part of the JACADS marine ecological monitoring program and by the
US Coast Guard for the Sand Island study. Funding administration provided by the Office of Naval
Research (Grant numbers N00014-19-J1519, N00014-92-J-1969 and N00014-95-1-1324) and the
Army Research Office (Grant number DAAG55-98-1-0304). Significant conceptual contributions to
the sampling plan were made by representatives of the USAF (Mark Ingoglia), NOAA (Denise
Klimas), EPA (Steve Linder) and USFWS (Roger DiRosa and Don Palawski). We also thank our
consistent dive buddies and collaborators; Gary McCloskey, Dave Shogren, Steve Oliver, Jason
Phillebotte, Anne Cohen, Mindy Richlin, David Mann, Brandon Casper, Don Anderson, Aaron Rice,
Janelle Morano, and David Portnoy.
Literature Cited
Anderson, D. M., and P.S. Lobel. 1987. The Continuing Enigma of Ciguatera. Biological Bulletin, 172:89-107.
Baptista, J., P. Pato, S. Tavares, A.C. Duarte, M. A Pardal. 2013. PCB Bioaccumulation in Three Mullet
Species—A Comparison Study. Ecotoxicology and Environmental Safety, 94:147-152.
Bartell, S.M. 2006. Biomarkers, Bioindicators, and Ecological Risk Assessment - A Brief Review and
Evaluation. Environmental Bioindicators, 1:60-73.
61
Burke, L., K. Reytar, and M. Spalding, A. Perry. 2011. Reefs at Risk Revisited. World Resources Institute,
Washington, DC. 130 pp.
Choat, J.H., and D.R. Robertson. 2002. Age Based Studies. In: Sale P.F. ed. Coral Reef Fishes: Dynamics and
Diversity in a Complex Ecosystem. Academic press. London. Pp. 57-80.
Crosby, M.P. and E.S. Reese. 1996. A Manual for Monitoring Coral Reefs With Indicator Species:
Butterflyfishes as Indicators of Change on Indo Pacific Reefs. Office of Ocean and Coastal Resource
Management, National Oceanic and Atmospheric Administration, Silver Spring, MD. 45 pp.
Dacey, J.W., G. King, and P.S. Lobel. 1994. Herbivory by Reef Fishes and the Production of Dimethysulfide.
Marine Ecological Progress Series, 112:67-74.
GESAMP, 1990. Joint Group of Experts on the Scientific Aspects of Marine Pollution. The State of the Marine
Environment . Rep. GESAMP No. 39, London, 111pp.
Goodsell, P.J., A.J. Underwood, and M. G. Chapman. 2009. Evidence Necessary for Taxa to be Reliable
Indicators of Environmental Conditions or Impacts. Marine Pollution Bulletin, 58:323-331.
Green, A.L., and D.R. Bellwood. 2009. Monitoring Functional Groups of Herbivorous Reef Fishes as Indicators
of Coral Reef Resilience – A Practical Guide for Coral Reef Managers in the Asia Pacific region. IUCN
working group on Climate Change and Coral Reefs. IUCN, Gland, Switzerland. 70 pages.
Guzman, H.M., and E.M. Garcia. 2002. Mercury Levels in Coral Reefs Along the Caribbean Coast of Central
America. Marine Pollution Bulletin, 44:1415–1420.
Hardy, J.T., S. Kiesser, L. Antrim, A. Stubin, R. Kocan, and J. Strand. 1987. The Sea-surface Microlayer of
Puget Sound: Part I. Toxic Effects on Fish Eggs and Larvae. Marine Environmental Research, 23: 227-249.
Halpern, B.S., S. Walbridge, K.A. Selkoe, C.V. Kappel, F. Micheli, C. D’Agrosa, J.F. Bruno, K.S. Casey, C.
Ebert, H.E. Fox, R. Fujita, D. Heinemann, H.S. Lenihan, E.M.P. Madin, M.T. Perry, E.R. Selig, M. Spalding, R.
Steneck, and R. Watson. 2008. A Global Map of Human Impact on Marine Ecosystems. Science, 319:948-952.
Haynes, D., and J.E. Johnson. 2000. Organochlorine, Heavy Metal and Polyaromatic Hydrocarbon Pollutant
Concentrations in the Great Barrier Reef (Australia) Environment: a Review. Marine Pollution Bulletin,
41:267-278.
Hernandez, F., A. Pastor, M.L. Gisbert, J. Ansuategui, and R. Serrano. 1992. Biomonitoring of Heavy Metal
Distribution in the Western Mediterranean Area of Spain. Marine Pollution Bulletin, 24: 512-515.
Horn, M.H. 1989. Biology of Herbivorous Fishes. Oceanography and Marine Biology Annual Reviews, 27:
167-272.
Hourigan, T.F., T.C. Tricas, and E.R. Reese. 1988. Coral Reef Fishes as Indicators of Environmental Stress in
Coral Reefs. In Marine organisms as indicators, ed. D. F. Soule and G. S. Kleppel. 107-135. New York:
Springer-Verlag.
Hughes, T.P., M.J. Rodrigues, D.R. Bellwood, D. Ceccarelli, O. Hoegh-Guldberg, L.McCook, N.
Moltschaniwskyj, M.S. Pratchett, R.S. Steneck, B. Willis. 2007 Phase Shifts, Herbivory, and the Resilience of
Coral Reefs to Climate Change. Current Biology, 17: 1-6.
Irons, D.K., J.D. Anderson, and J.D. Parrish. 1985. Johnston Atoll Resource Survey. Hawaii Cooperative
Fishery Research Unit. University of Hawaii, Honolulu HI. Submitted to the Department of the Army, U.S.
Army Engineer District, Honolulu, Fort Shafter, Hawaii.
62
Jameson, S., M. Erdmann, G. Gibson, and K. Potts. 1998. Development of biological criteria for coral reef
ecosystem assessment. Atoll Res. Bull. 450.
Johannes, R.E., and S.B. Betzer. 1975. Introduction: marine communities respond differently to pollution in the
tropics than at higher latitudes. In: Ferguson Wood, E.J. and R.E. Johannes eds. Tropical Marine Pollution, New
York: Elsevier Scientific Publishing Company. pp1-11.
Johnson O., D. Osborne, C. Wildgoose, W. Worstell, and P. Lobel. 1997. Development and Testing of a LargeArea Underwater Survey Device. IEEE Transactions on Nuclear Science, 44(3):792-798.
Kerr L.M., K.L. Lang, and P.S. Lobel. 1997. PCB Contamination Relative to Age for a Pacific Damselfish,
Abudefduf sordidus (Pomacentridae) Biological Bulletin 193:279-281.
Kerr Lobel, L., and P.S. Lobel. 2009. Contaminants in fishes from Johnston Atoll. Proceedings of the 11th
International Coral Reef Symposium. pp. 1123-1128.
Linton, D. M., G.F. and Warner. 2003. Biological Indicators in the Caribbean Coastal Zone and Their Role in
Integrated Coastal Management. Ocean and Coastal Management 46:261-276.
Lobel L.K., and P.S. Lobel. 2013. Junkyard Damselfishes: Spawning Behavior and Nest Site Selection. In:
Lang M., Sayer M. eds. Diving for Science. Proceedings of the American Academy of Underwater Sciences /
European Scientific Diving Panel Joint International Scientific Diving Symposium. Curaçao, Netherlands
Antilles: AAUS; 2013.
Lobel, P. S. 1981. Trophic Biology of Herbivorous Reef Fishes: Alimentary pH and Digestive
Strategies. Journal of Fish Biology, 19:365-397.
Lobel, P. S. 2003. Marine Life of Johnston Atoll, Central Pacific Ocean. Natural World Press, OR, 128pp.
Lobel, P.S., G. Tomasky, and L. M. Kerr. 1997. Johnston Atoll Phase II Marine Sediment Sampling Field
Report. Johnston Atoll Ocean Science Study. Technical Report to the U.S. Army, U.S. Air Force, U.S. Coast
Guard, U.S. Fish and Wildlife Service and the U.S. Environmental Protection Agency.
Lobel, P.S., and L.M. Kerr. 1995. Johnston Atoll Phase I Marine Sediment Sampling Field Report. Johnston
Atoll Ocean Science Study. Technical Report to the U.S. Army, U.S. Air Force, U.S. Coast Guard, U.S. Fish
and Wildlife Service and the U.S. Environmental Protection Agency.
Lobel P.S., and L. Kerr Lobel. 2008. Aspects of the Biology and Geology of Johnston and Wake Atolls,
Pacific Ocean. Chapter 17 In: Coral Reefs of the USA, Series: Coral Reefs of the World, Vol. 1 Riegl, B.M.
and R.E. Dodge (Eds.). 806pp.
Lobel, P.S., G. Tomasky, and L. M. Kerr. 1997. Johnston Atoll Phase II Marine Sediment Sampling Field
Report. Johnston Atoll Ocean Science Study. Technical Report to the U.S. Army, U.S. Air Force, U.S. Coast
Guard, U.S. Fish and Wildlife Service and the U.S. Environmental Protection Agency.
Lobel P.S., and L.M. Kerr. 2000. Status of contaminants in Johnston Atoll lagoon sediments after 70
years of US military activity. Proceedings of the 9th International Coral Reef Symposium. Bali,
Indonesia 23-27 October 2000. Vol 2. pp. 861-866.
Long, E.R., and D.D. MacDonald. 1992. National Status and Trends Program approach. In: Sediment
classification methods compendium. USEPA. Office of Water. EPA 823-R-92-006.
Long, E.R., L.J. Field, and D.D. MacDonald. 1998. Predicting Toxicity in Marine Sediment with Numerical
Sediment Quality Guidelines. Environmental Toxicology and Chemistry 17:714–727.
63
McManus, J., and J.F. Polsenberg. 2004 Coral-algal Phase Shifts on Coral Reefs: Ecological and Environmental
Aspects. Progress in Oceanography 60: 263-279.
Morrison, R.J., G.R.W. Denton, U. Bale Tamata, and J. Grignon 2013. Anthropogenic Biogeochemical Impacts
on Coral Reefs in the Pacific Islands—An Overview. Deep-sea Research II 96:5–12.
Mumby, P.J., C.P. Dahlgren, A.R. Harborne, C.V. Kappel, F. Micheli, D.R. Brumbaugh, K.E. Holmes, J.M.
Mendes, K. Broad, J.N. Sanchirico, K. Buch, S. Box, R.W. Stoffle, A.B. Gill. 2006. Fishing, Trophic Cascades,
and the Process of Grazing on Coral Reefs. Science 311; 98-101.
NOAA, 1999a. Sediment Quality Guidelines developed for the National Status and Trends Program.
http://ccma.nos.noaa.gov/publications/sqg.pdf
NOAA. 1999b. Screening Quick Reference Tables. http://response.restoration.noaa.gov/environmentalrestoration/environmental-assessment-tools/squirt-cards.html
Peters, E., N. Gassman, J. Firman, R. Richmonds and E. Power. 1997. Ecotoxicology of Tropical Marine
Ecosystems. Environmental Toxicolology and Chemistry, 16: 12-40.
Peterson, R.E., H.M. Theobald, and G.L. Kimmel. 1993. Developmental and Reproductive Toxicity of Dioxins
and Related Compounds: Cross Species Comparisons. Critical Reviews in Toxicology 23: 283-335.
Randall, J.E., P.S. Lobel, and E.H. Chave. 1985. Annotated Checklist of the Fishes of Johnston Island. Pacific
Science. 39:24-80.
Richlin, M. L., and P.S. Lobel. 2001. Effect of Depth, Habitat and Water Motion on the Abundance and
Distribution of Ciguatera Dinoflagellates at Johnston Atoll, Pacific Ocean. Marine Ecology Progress Series,
421: 51–66.
Underwood, A.J., and C.H. Peterson. 1988. Towards an ecological framework for investigating pollution.
Marine Ecology Progress Series, 46.1:227-234.
Whitall, D., A. Mason, A. Pait, L. Brune, M. Fulton, E. Wirth, and L. Vandiver. 2014. Organic and metal
contamination in marine surface sediments of Guánica Bay, Puerto Rico. Marine Pollution Bulletin, 80: 293–
301.
Wu, R.S.S., A.K.Y. Chan, B.J. Richardson, D.W.T. Au, J.K.H. Fang, P.K.S. Lam, and J.P. Giesey. 2008.
Measuring and Monitoring Persistent Organic Pollutants in the Context of Risk Assessment. Marine Pollution
Bulletin, 57:236-244.
64
In: Lobel L.K. ed. Diving for Science 2015.
Proceedings of the American Academy of Underwater Sciences 34th Symposium.
Milestones in Underwater Ichthyology: The First Scientific Divers in
America
Phillip Lobel1* and Lisa Lobel2
1
Boston University, Department of Biology, 5 Cummington Mall, Boston, MA 02215, USA
[email protected]
2
Wheelock College, Department of Math & Science, 200 Riverway, Boston, MA 02215 USA
*
presenting and corresponding author
Abstract
The science of underwater observation of fish behavior and ecological studies begins with a
botanist, Dr. William H. Longley (1881 – 1937). Longley served as the second director of the
Carnegie-Mellon Marine Laboratory on the Dry Tortugas Island (1922- 1937), which was the
first tropical marine lab in the western hemisphere. Longley’s underwater studies began while
working at the Dry Tortugas lab early in the 1900s, first diving at the lab in 1910. Longley’s
general research objective was to test Darwin’s concept of evolution. Using a first generation
Miller-Dunn shallow water diving helmet, he developed the first underwater slate for note taking
and a specialized underwater camera system to document fish color patterns and behavior. His
work with National Geographic photographer Charles Martin resulted in the first underwater
color photographs published in the National Geographic Magazine in 1927. As a direct result of
his diving with a helmet, Longley discovered 29 new species of fishes, the behavior of the
cleaner goby, the symbiosis of goby and shrimp sharing a burrow, the sand diving behavior of the
razor wrasse and many more notable “firsts”. His early scientific diving led the way for the next
generation scientific diving research and classes at the University of Miami in the 1930s. We will
review the diving technology that Longley used, highlight his scientific discoveries and show his
lasting influence on scientific diving and coral reef ecology.
Keywords: fish behavior, Miller-Dunn diving helmet, reef ecology, underwater photography,
William Longley,
Introduction
The history of Ichthyology in the United States is a legacy of great thinkers and adventurers who also
had the physical stamina for fieldwork plus natural abilities as hunters for collecting wildlife. They
were also technically savvy. These great men (sad to say women did not enter this field until after the
1930s, see below) were totally constrained to collecting fishes by hook, nets, poisons and explosives.
The color patterns of fishes were mainly known from freshly dead specimens. Artists working with
these Ichthyologists documented the color patterns of these specimens by detailed hand drawn
paintings, which were reproduced in limited editions of the early books (all of which are now highly
collectable). Among the most famous of these, were the works of David Starr Jordan (1851-1931) and
Barton W. Evermann (1853-1932), two examples are Evermann and Marsh 1899 and Jordan and
Evermann 1905.
The problem in the 1800s was that at the time, in the absence of observations of the live fishes, the
taxonomy was often confused by the diversity of colors and patterns that occurred within a single
species (e.g. sexual dimorphism and changes in ontogeny: juvenile vs. adult colorations). As a result,
what we know now as a single species was often classified back then as different species based upon
these different colors. This taxonomic problem would not be resolved until scientists were able to
65
dive underwater and directly observe fishes engage in their natural behavior in their native habitat.
The beginnings of underwater scientific diving is the topic of this paper, but the inspiration,
motivation and justification for this endeavor was based upon the earlier work of the great
Ichthyologists who were constrained to remain topside or ashore. For a history of Ichthyology before
diving see Hubbs (1964) and Pietsch (1995).
American technology was being developed during the industrial revolution of the late 1800s, which
would eventually lead to the development of the diving apparatus. Science was also undergoing a
revolution stimulated by C. Darwin and his theory of evolution.
This was the background to the underwater scientific research conducted by W.H. Longley (1881 –
1937), Professor for Biology at Goucher College and the second head of the Tortugas Marine
Laboratory of the Carnegie Institution of Washington in the Gulf of Mexico. He earned his Ph.D.
from Yale in 1910. Longley was intent on testing Darwin’s hypothesis of evolution (Davis, 1932)
with a focus on marine life, just as Darwin had done. The advantage that Longley had in the early
1900s that Darwin lacked in the 1830s, was the “Diving Hood”. It was in this context that Longley
became one of the earliest diving scientists in America (perhaps the first). William H. Longley (who
was actually trained as a botanist) started diving before 1916 using the Dunn shallow water helmet at
the first tropical marine laboratory in the western hemisphere, the Carnegie Marine Laboratory in the
Dry Tortugas, Florida. By contrast, the famous William Beebe made his first helmet dive in 1925. For
a history of the early days at the Carnegie laboratory, see Colin (1980).
Our interest in the studies by Longley developed from research that the senior author had done in
collaboration with J.E. Randall. Randall and P. Lobel had worked on two studies concerning goby
behavior and ecology. While reviewing the literature, they found that Longley reported these
behaviors for first time. One study was on the symbiosis of goby and shrimps in burrows (Randall et
al., 2005) and the other was on the systematics and behavior of cleaning gobies (Elacatinus spp.) in
the Caribbean (Randall and Lobel, 2009). Whenever anyone initiates a study of Caribbean fish
ecology and behavior, they are likely to find the earliest reference being Longley and Hildebrand
(1941), more on this publication below.
History
Early use of the Dive helmet
The history of the early coral reef explorations while using a “diving hood” was chronicled by the
Ichthyologist, Dr. E. Gudger (1866-1956). He came from North Carolina, earned his Ph.D. at Johns
Hopkins University in 1905, and began working at the American Museum of Natural History, New
York in 1919. His first trip to the Carnegie Marine Laboratory in Dry Tortugus, Florida was in 1907.
It was Gudger who first wrote about the use of the diving helmet in his paper titled “ On the use of the
diving helmet in submarine biological work” published in 1917. Prior to this publication, the first
report of using the “diving hood” for research underwater was mentioned incidentally in a brief paper
by A.G. Mayer (1916), the marine lab’s first director. Mayer included what is probably the first
photograph of a diver using the Miller-Dunn Diving Hood Style 1 (Figure 1). Interestingly, this photo
was taken by the Submarine Photo Company, Miami, FL and was, most likely, the work of George
Williamson, who developed the “submarine tube” (Figure 2). It was this submarine tube that was used
for the filming of the first underwater movie “20,000 Leagues under the Sea” in 1916.
In terms of the very first diving by a scientist, the earliest use of a diving helmet and suit was
probably by M. Milne-Edwards off Italy in 1844-1845. This was in the full diving rig adapted from
the fire-fighting outfit of the day. A. Siebe developed the earliest diving helmet and suit in 1819 (see
the exhibits at the History of Diving Museum, Marathon, FL). It was not until the Dunn diving hood
66
was developed and which only required a simple helmet and no suit that diving by scientists became
possible and easy (Gudger, 1917). For the best historical review of hard-hat diving see Bauer and
Bauer (1988) and visit the History of Diving Museum, Marathon, FL.
Figure 1. “The Dunn Diving Hood in
use” from Mayer 1916. Officially,
this helmet was introduced to the
commercial market in 1916 but it was
in use at the Tortugas lab before 1915
and probably earlier.
Figure 2. The “submarine tube” was used in the filming of the 1916 version of 20,000 Leagues Under the Sea.
Picture from the website
http://www.miamisci.org/blog/the-curious-vault-003-mr-williamsons-submarine-tube/
67
Mayer’s article briefly describes Longley’s research using the diving hood, which was invented by
Mr. Dunn. In this 1916 article, Mayer refers to Longley’s “years of patient study” on the meaning of
the coloration of reef fishes: thus, implying by the time of Mayer’s report in 1916, that Longley had
been diving for years. Mayer apparently inaugurated the widespread use of the diving helmet by
visiting scientists at the lab in 1915 (Gudger, 1917), a year before the Miller-Dunn Helmet was
officially available commercially. This enabled other scientists, including Gudger, to dive on the
reefs. According to Gudger, the helmet was in frequent use during the summers of 1915 and 1916.
Overall, it is confusing from these different accounts to pin-point exactly when Longley started his
underwater research using the helmet.
Gudger (1917) reported how “the diver is free to move about to a depth of twenty or thirty feet and to
sit or recline in any position his work demands”. He showed Figures 3 and 4 to illustrate this point.
Gudger himself is shown diving with the helmet in Figure 5.
Figure 3. “Becoming a marine animal for
study of unexplored tropical seas”
(from Gudger 1917).
Figure 4. Diver with hood removed to
show ease of operation.
(from Gudger 1917).
Professor William Longley
Longley conducted most of his underwater research at the Tortugas Marine Laboratory, Florida. He
spent every summer between 1910 and 1936 missing only 1912 at the Tortugas station (Colin, 1980).
He also made observations in Hawaii in 1916 where he experimented with color photography and
discovered the problem of needing color correction when submerged due to the attenuation of colors
underwater (Longley, 1918).
The remarkable accomplishment by William Longley was that he conducted his underwater research
while diving solo (but with surface support for pumping the air) and during a time before the
68
behaviors of fishes and other reef creatures were known. He detailed his in-situ observations using a
wax-covered slate, which were later transcribed on paper. His use of this slate for ‘underwater note
taking’ is the first reference to such a device being used, as far as we could find in the literature.
Figure 5. This photo shows E. Gudger beginning a dive
in Miller-Dunn Style 1 helmet. About 80 lbs of weight
was needed. Gudger wrote “So valuable has been it been
found in submarine biological work at Tortugas that it
has been made a part of the permanent equipment of the
station there” (from Gudger, 1917).
One of Longley’s earliest papers based on his observations while diving was published in 1916
“Observations upon tropical fishes and inferences from their adaptive coloration”. In this paper, he
presented a critical evaluation of Darwin’s hypothesis of evolution. He was being swayed by
Darwin’s hypothesis of evolution by natural selection but he was not entirely convinced at this time
because of the variability in the coloration of fishes. He speculated this could include aspects of the
inheritance of acquired characteristics as the “immediate cause of adaptation”.
Longley documented his observations of fish behavior and coloration using a camera in a “specially
devised water-tight metallic box (Gudger, 1917). Longley described his camera (Figure 6) in his 1918
paper.
Longley’s 1918 paper contained his first published photographs in black and white to illustrate the
color changes and behavior of reef fishes. He described the camera design as well: “The mirror
projecting in the rear view from the top of the focusing hood enables one to without bending over to
see the doubly reflected image of objects within the field of the camera”. The key here is that this
camera was specifically made so a diver in the Diving-hood could use it such that the diver would not
loose air by tipping the helmet! He went on to describe: “The rods with the milled heads are for
focusing and for release of the shutter”. The cubical body of the camera box was eight inches on a
side and it weighed about fifty pounds.
69
Figure 6. Longley’s camera 1916 – 1930
from his 1918 paper on the “Haunts and
habits of tropical fishes”.
Longley is most famous for taking the first underwater color photographs in collaboration with
Charles Martin for National Geographic Magazine in 1926 (published in National Geographic
Magazine, January 1927). In order to obtain good color rendition, they developed the first flash
system for underwater photography. This was described and illustrated in their National Geographic
article. They built a pontoon float (Figure 7) and equipped it with one pound of “flash-light
(magnesium) powder” and an electric battery, which was activated by the diver when he was ready to
take the photograph. (http://photography.nationalgeographic.com/photography/photographers/firstunderwater-article.html).
Figure 7. Showing the pontoon boat with explosives (left) and the FLASH when detonated (right).
From the January 1927 issue of National Geographic Magazine.
70
Longley published only a few papers during his lifetime, but he kept extensive notes and photographs
of all of his observations. When he died, the scientific community assigned the task of collating,
editing and publishing these notes to another ichthyologist, Samuel Hildebrand, from the Smithsonian
Institution. This monumental study titled: "Systematic catalogue of the fishes of Tortugas, Florida
with observations on color, habits and local distribution" was published in 1941 after Longley’s death
in 1937. This book was based on Longley's observations of over 25 years of diving using a shallowwater helmet and includes dozens of underwater photographs. It was the first underwater study of fish
behavior and set the stage for the generations of diving ichthyologists who followed. His obituary was
published in Science (Cleland 1937). A photo of William Longley was published by Colin (1980) and
is reproduced here as Figure 8.
Figure 8. W. H. Longley fishing from the back of
the boat on his way to Tortugas, summer 1930. He
was dressed for town having just departed Key West
(photo extracted from figure 1 in Colin 1980 and
was a photo provided by Longley’s son, W. H.
Longley Jr.)
Summary
Every coral reef biologist should read Longley and Hildebrand 1941 for insight and history.
The discoveries made by Longley while diving with the shallow-water helmet include:
•
•
•
•
•
•
•
•
•
•
Synonymy of about 20% of the known fish species at the time that occurred in the Florida Keys.
Description of 29 new reef fish species
Recognition of the larval transformation of a leptocephalus larva into the juvenile bonefish,
Albula vulpes.
First descriptions of the symbiosis relationship of cleaner fishes and host fishes. He was the first
to describe the cleaning behavior of the goby, Elacatinus oceanops, juvenile porkfish,
Anisotremus virginicus, and the juvenile bluehead wrasse, Thalassoma bifasciatum.
First observations of the nocturnal habits of fishes including color changes.
Color changes with behavior of the hogfish, Lachnolaimus maximus.
First observations of the spawning behavior of several fishes, most notably the damselfishes
(Pomacentridae).
First observations of the sand diving behavior of the razor wrasse, Xyrichthys spp.
First observations of the burrowing behavior of the yellowhead jawfish, Opistognathus aurifrons.
First observations of the symbiotic burrow sharing behavior of the goby, Nes longus and the
alpheid shrimp, Alpheus floridanus.
71
Developments in the Miller-Dunn Diving-Hood
There were three styles of Miller-Dunn diving helmets (Figure 9, 10 and 11) and several styles of
hand-pump, one is shown in Figure 12.
Figure 9. A Miller-Dunn Diving Helmet
Style 1. It was introduced in 1916. Photo
by the authors of a helmet on display at
the History of Diving Museum
Figure 11. A Miller-Dunn Diving
Helmet Style 3 ca 1940. Photo by the
authors of a helmet in their personal
collection.
Figure 10. A Miller-Dunn Diving Helmet Style 2.
This became the US Navy’s first official diving
rig, ca 1927. Photo by the authors of a helmet on
display at the History of Diving Museum
Figure 12. A Miller-Dunn Hand Pump
Model No. 1A. The air-hose is not shown.
Photo by the authors of a pump in their
personal collection.
72
Discussion
William Beebe began diving with a shallow-water dive helmet in 1925 and wrote about his
experiences in the National Geographic Magazine in Dec 1932 in an article titled "A Wonderer Under
Sea". In a newspaper interview published 15 March 1928, Dr. Beebe said his work was only possible
due to the Miller-Dunn helmets (Miami Daily News). After a lecture, Beebe is quoted as saying, “talk
to Mr. Miller. He and Mr Dunn, both Miamians, have made possible the finest work in studying
marine life, they have opened up a new world to science with their diving hoods and equipment”.
Beebe went on to say, “We simply take the equipment provided by Miller and Dunn” he explained
“and wearing only a pair of trunks and tennis slippers, go down in the sea to discover a new realm of
life. Why worry about Mars and Venus, when another world may be so reached so easily by anyone?
Experience or training isn’t necessary”. (italic emphasis added, well, we know now that Beebe’s last
statement was naïve and dangerous).
By the time the Miller-Dunn Style 3 helmet made its debut, helmets were in widespread use by the
Navy and the scientific community. The University of Miami began organized scientific diving
courses in the 1930s. In 1935-1937, Dr. J.W. Pearson was leading field trips to the Bahamas and
using the diving hood with students to explore the reefs. By this time, these trips involved both men
and women students! They dove from shore and from boats. Figures 13, 14, 15 and 16 show some
scenes from these early scientific diving classes.
Figure 13. 1930s University of Miami divers using various styles of Miller-Dunn helmets, also
showing the pumps and air-hoses. Photo from University of Miami Archives.
73
Figure 14. 1930s University of Miami divers using various styles of Miller-Dunn helmets. Notice the
handling of the hoses and the support teams. Photo from University of Miami Archives.
Figure 15. 1930s University of Miami divers in the Miller-Dunn Style 3 helmet with both men and
women underwater. Photo from University of Miami Archives.
74
Figure 16. 1930s University of Miami divers using various styles of Miller-Dunn helmets from a
diving barge. Photo from University of Miami Archives.
Other scientists were also eager to explore the ocean bottom first-hand. Encouraged by William
Beebe, the science writer and US Fish and Wildlife Biologist, Rachel Carson joined a University of
Miami expedition (1949) and used the Miller-Dunn Helmet Style 3 to observe the reefs for herself
(Figure 17). The weather was rough and she only spent a few minutes underwater on the ladder, but
the experience was transformative for her.
Figure 17. Rachel Carson enroute to a dive, 1949.
Photo by Shirley A. Briggs,
Rachel Carson Council Archives,
from the website,
https://blogs.ntu.edu.sg/hp331-2014-47/?page_id=39
75
In many ways, the subsequent discoveries by modern marine biologists were built upon the scientific
approach that Longley established. For example, John E. Randall also used photography and
developed a new technique for photographing fishes in trays in order to accurately document their
color patterns so he could best describe new species (Randall, 1961). To obtain the best-looking
specimens with minimal damage, Randall invented the multi-prong mini-spear (Randall, 1963).
Randall's many discoveries were largely based upon being a skilled scuba diver who understood what
he was observing. He readily recognized new species and was often the first ichthyologist to dive
many remote locations worldwide. His photographs both using his photo-tray and underwater were a
key part of his scientific method.
Today, scientists can dive longer and deeper using nitrox and rebreathers. Scientists using rebreathers
are now going to where open circuit scuba divers have not been able to collect before and are
discovering new fishes at deeper depths (e.g., Pyle, 1996). Previously unknown behaviors such as the
sounds made by fishes during mating are also being discovered using the silent rebreathers and
innovative recording technology (e.g. Lobel, 2002; Pyle et al., 2015).
We can see a simple progression in our diving history. The core element of advancement being based
on the diving technology and associated gear used to explore the undersea. The importance of the
underwater breathing technology to making advancements in our science is obvious. Underwater
photography/video is also an essential tool. We need to imagine what are the next technological
innovations needed that will enable new discoveries in the future.
Acknowledgments
We sincerely thank Sally Bauer and the late Joe Bauer for many years of great conversations about
the history of diving (Joe and Sally took Phil on his first ocean dives in the Florida Keys in 1968). We
also thank John E. “Jack” Randall for decades of mentorship (Phil first dove with Jack in 1971 in
Hawaii, and the three of us have done many dives together since) and many hours of intriguing
discussion about the history of ichthyology and much more. We also thank Rick Gomez, Univ. Miami
for providing the historical photos from the University of Miami Archives in Figures 13, 14, 15 and
16.
Literature Cited
Bauer J.A. and S.E. Bauer. 1988. The Hard Hat Diving Helmet. In: Bachrach A.J., B.M. Desiderati and M.M.t
Matzen (eds) A Pictorial History of Diving. Best Publishing Company, San Pedro, California, USA. 149pp.
Cleland, R.E. 1937. William Harding Longley: Obituary. Science, 85 no. 2208:400-401.
Colin P.L. 1980. A Brief History of the Tortugas Marine Laboratory and the Department of Marine Biology,
Carnegie Institution of Washington. In: Sears, M. and D. Merriman (eds), Oceanography: The Past. pp 138147. Springer Verlag
Davis, W. 1932. In Confirmation of Darwin. Current History, Feb 1932, pp 690-692.
Evermann, B.W., and M.C. Marsh. 1900. The Fishes of Puerto Rico. pages 51 – 350 in Investigations of the
Aquatic Resources and Fisheries of Puerto Rico, U.S. Fish Commission for 1900. Government Printing Office
Washington. pp 35.
76
Gudger, E.W. 1917. On the Use of the Diving Helmet in Submarine Biological Work. American Museum
Journal, Feb. 1, 1917: 135-138.
Hubbs, C.L. 1964. History of Ichthyology in the United States after 1850. Copeia, Vol. 1964, No. 1: 42-60.
Jordan, D.S. and B.W. Evermann. 1905. The Shore Fishes, the Aquatic Resources and Fisheries of the Hawaiian
Islands. Bulletin of the U.S. Fish Commmission. Government Printing Office Washington.
Longley, W. H. 1917. Observations Upon Tropical Fishes and Inferences from their Adaptive Coloration.
Proceedings of the National Academy of Sciences, 2 (12):733-737
Longley, W.H. 1917. Habits and Coloration of Hawaiian Brachyura and Fishes with Notes on the Possibility of
Submarine Color-Photography. Year Book no 16, 1917 Carnegie Institution of Washington (distributed Feb
1918).
Longley, W.H. 1918. Haunts and Habits of Tropical Fishes: Observations of an Explorer Equipped with a
Diving-Hood in the Unknown World of Coral Labryinths at the Bottom of the Sea. The American Museum
Journal, 18(2):79-88.
Longley, W.H. 1922. Habits and Local Distribution of Tortugas Fishes. Carnegie Institution of Washington year
book no. 20. pp 204-205.
Longley, W.H. 1927. Life on a Coral Reef. National Geographic Magazine. 51(1).
Longley, W.H., and S. Hildebrand. 1941. Systematic Catalogue of the Fishes of Tortugas, Florida with
Observations on Color, Habits and Local Distribution. Carnegie Institute of Washington Publication 535,
Washington DC, 1941; 331pp + 34 plates.
Lobel, P. S. 2002. Diversity of Fish Spawning Sounds and the Application of Passive Acoustic Monitoring.
Bioacoustics, 12: 286-9.
Mayer, A.G. 1916. Studies of Reef Fishes. (New York) Zoological Society Bulletin, March 1916:1335-1336.
Pietsch, T.W. (ed) 1995. Historical Portrait of the Progress of Ichthyology, From its Origins to Our Own Time
by G. Cuvier. The Johns Hopkins Press, Baltimore. 366 pp.
Pyle, R.L. 1996. How Much Coral Reef Biodiversity are We Missing? Global Biodiversity. 6(1): 3-7.
Pyle, R.L., P.S. Lobel, and J.A. Tomoleoni. 2015. The Value of Closed-Circuit Rebreathers for Biological
Research. In: Pollock N.W., S.H. Sellers, J.M Godfrey, eds. Rebreathers and Scientific Diving. Workshop
proceedings. NPS/NOAA/DAN/AAUS: Durham, NC. in press.
Randall, J.E. 1961. A Technique for Fish Photography. Copeia. 1961; 2: 241-2.
Randall, J.E. 1963. Methods of Collecting Small Fishes. Underwater Naturalist. 1963; 1(2): 6 -11, 32-6.
Randall, J.E., and P.S. Lobel. 2009. A Literature Review of the Sponge-dwelling Gobiid Fishes of the Genus
Elacatinus from the Western Atlantic, with Description of Two New Caribbean species. Zootaxa, 2133: 1-19.
Randall, J.E., P.S. Lobel, and C.W. Kennedy. 2005. Comparative Ecology of the Gobies Nes longus and
Ctenogobius saepepallens, Both Symbiotic with the Snapping Shrimp Alpheus floridanus. Environmental
Biology of Fishes, 74(2): 119-27.
77
In: Lobel L.K. ed. Diving for Science 2015.
Proceedings of the American Academy of Underwater Sciences 34th Symposium.
Octopus rubescens’ Prey Handling Procedures are Influenced by Bivalve
Shell Thickness and Adductor Muscle Strength
Jillian Perron1, 2*, Alan Verde1#
1
Corning School of Ocean Studies, Maine Maritime Academy, 1 Pleasant Street, Castine, ME, USA
[email protected], [email protected]
2
St. George’s University, School of Veterinary Medicine, St. Georges, Grenada, West Indies
[email protected]
*
presenting author
#
corresponding author
Abstract
Most generalist predators are faced with an assortment of preparation and handling decisions to
make prior to consuming their prey. Octopuses commonly preying on mollusk and gastropod
species that are protected by a calcified exoskeleton (shell), attempt to pull the shells apart or drill
into the shell. This study was conducted to determine which feature of bivalve shells, shell
thickness or adductor muscle strength, influenced the red octopus’ penetration techniques the
most. Red octopuses (Octopus rubescens) were fed a single species of clam once a day over the
course of 11 days and the handling time of each feeding trial was measured. Octopus rubescens
presented with thin shelled (Nuttalia obscurata) vs. thick shelled (Venerupis philippinarum)
bivalves, utilized different mechanisms for processing them. Octopuses used their tentacles and
suckers to pull apart the thin shelled bivalves, but thick shelled bivalves, with nearly three times
the pulling resistance of thin shelled bivalves, were more commonly drilled, presumably to inject
paralyzing venom. Consequently, octopuses that drilled bivalve shells took 6.8 times longer to
consume their prey than those that physically pulled the shells apart. Regardless of shell
thickness, bivalve handling times continually decreased from day 1 to day 11 which suggests that
O. rubescens uses a sophisticated working memory to learn and adjust their bivalve prey
handling behavior. By using the “ideal” method for opening different types of bivalves, O.
rubescens may be utilizing optimal foraging strategies when manipulating and processing bivalve
prey.
Keywords: Octopus rubescens, shell penetration, handling time, working memory
Introduction
Generalist predators, or more commonly known as opportunists, are faced with many decisions
regarding prey detection, capture, penetration, and consumption (Lavoie, 1956; Anderson et al., 2008;
Onthank and Cowles, 2011) because of the variety of organisms they consume. In contrast, specialist
predators are well suited to feed on a restricted variety of prey and therefore the majority of their
energy expenditure is spent on searching for and detecting prey rather than consumption. Generalists
have a wide variety of prey species and these can differ greatly in physiology, camouflage, defense
mechanisms, and nutritional value (Iribarne et al., 1991; Mather et al., 2012). The feeding habits and
strategies of generalists are heavily dependent on the abundance of prey and they are more likely to
feed on the most profuse prey species available. This reduces searching time but forces the predator to
select a handling mechanism to maximize energy acquisition (Smith, 2003; Onthank and Cowles,
2011). Such a process decreases time spent on searching for and detecting prey but increases energy
spent on prey consumption. This principle is known as the optimal foraging theory and it drives the
feeding habits of all predators (Lai et al., 2011) and highlights the selection pressure of predators to
spend minimal time handling its prey in return for maximum energy acquisition.
78
According to optimal foraging theory, predators (such as the octopus) must take prey size into
consideration (Iribarne et al., 1991; Smith, 2003; Ebisawa et al., 2011; Mather et al., 2012). Werner
and Hall (1974) suggest this size selectivity is associated with the optimal allocation of time and
energy expended searching for and handling prey. For example, a small octopus species would not be
expected to prey on a relatively large mollusk or gastropod. The increased handling time to process
such a large prey item would reduce the fitness of the predator since the energy expended to forage
and handle a large prey item may be greater than the energy acquired from the tissue of the prey itself
(Pyke et al., 1977) therefore, in general, smaller octopuses prey on predominantly smaller animal
species (Smale and Buchan, 1981, McQuaid, 1994; Steer and Semmens, 2003). Some benthic
octopuses are notorious for using a variety of prey preparation and handling methods depending on
the morphology and size of the targeted prey (Runham et al., 1997; Anderson and Mather, 2007;
Anderson et al., 2008).
Predators often have “tools” to handle and penetrate prey, which may include claws, talons, chelae,
teeth, bills, and beaks such that preparation and penetration techniques vary by predator species.
However, handling techniques used by the predator may vary according to the prey species as well.
For example crabs utilize their chelae to chip away at the shells edges of the Saxidomus giganteus
clam but when preying on the Protothaca staminea clam, the crab attempts to use brute force to
puncture the shell (Boulding, 1984). Western gulls use their bills to peck open smaller species of
bivalves, including Macoma secta; however when presented with Saxidomus, the bivalve was carried
to a significant height and dropped onto a hard substrate in an attempt to crack the shell (Maron,
1982). Octopus dierythraeus employs selective drilling with its radula depending on the species of
mollusk (Steer and Semmens, 2003) allowing this octopus to target certain locations on gastropod
shells depending on the morphology of the shell. The location of the drill hole is a trade-off between
the simplest places to drill and the optimal regions to inject paralyzing venom into the prey’s muscle
by Eledone cirrhosa (Runham et al., 1997) and Octopus dierythraeus (Steer and Semmens, 2003).
According to Harper (2002), octopuses have been drilling holes in scallops since the mid-Pliocene
(3.5-3.3 mya) Epoch so this drilling behavior is a common occurrence within the octopods.
Octopuses are opportunistic benthic foragers that feed upon a wide variety of shelled gastropods,
mollusks, crustaceans, fishes, and even other octopuses (Wodinsky, 1969). Ebisawa et al. (2011)
recorded Octopus vulgaris regularly feeding on 38 different animal species with each species being
detected, attacked, prepared, handled and consumed in a different manner. Octopuses utilize both
chemotactile and visual mechanisms to detect their prey (Mather, 2006; Huffard, 2007; Leite et al.,
2009). Depending on the environment and the topography of the substrate, octopuses apply three
forage strategies: cruise, saltatory, and ambush (Leite et al., 2009). Crawling, poking, groping, and
web-over (pounce and engulf prey under the buccal web) behaviors are characteristic of a “cruise”
searcher. Heavy dependence on the chemotactile and exploratory features of the tentacle appendages
is characteristic of a “saltatory” searcher, which is commonly known as the “stop-and-go” pattern.
Byrne et al. (2006) suggests that octopuses have preferred tentacles for certain tasks including
exploring, grasping, handling prey, and locomotion. For instance, Octopus vulgaris have the ability to
elongate their tentacles twice their original length, which can be beneficial when reaching for prey
taking refuge in small crevices or within rock pilings (Mazzolai et al., 2013). Leite et al. (2009)
described the third strategy as an “ambush” searcher, which is highly reliant on eyesight and motion
cues. Octopuses have the ability to detect and differentiate small movements and shadows on both the
oceans bottom and in the water (Iribarne et al., 1991; Byrne et al., 2006).
Among the preferred prey items of the benthic octopuses are crustaceans and bivalves, which have
tough calcified exoskeletons or shells, respectively (Iribarne et al., 1991; Cortez et al., 1998;
Anderson et al., 2008). Three mechanisms by which octopuses handle prey include pulling the
exoskeleton or shell apart with its tentacles and suckers (Kier and Smith, 2002; Mather, 2006;
79
Huffard, 2007), chipping away at the exoskeleton or shell gape with its beak (Mather, 2006; Huffard,
2007), or hole drilling into the exoskeleton or shell with the aid of a dissolving saliva lubricant and
injecting a paralyzing venom (Arnold and Arnold, 1969; Wodinsky, 1978; Mather, 2006; Huffard,
2007). All three mechanisms require a different energy cost (Onthank and Cowles, 2011) and take
differing amounts of time to accomplish (Anderson and Mather, 2007) which can be a costly trade-off
in regard to predation, egg investment, and/or foraging for more easily consumed prey (Ebisawa et
al., 2011).
Octopuses are the only invertebrates that have the ability to use their active working memory to
strategize foraging routes, manipulate prey, and escape predation (Mather, 1991a; 1991b; 2006).
According to Baddeley (1992), working memory is defined as a brain system that provides temporary
storage and manipulation of the information necessary for such complex cognitive tasks as language
comprehension, learning, and reasoning. Although octopuses may not necessarily use their working
memory for language comprehension, they may require it for learning and reasoning although the
length of time an octopus’s temporary information storage lasts remains unknown. Mather (1991b)
directly observed octopuses taking refuge in a central den, leave to hunt, and return multiple times
throughout the day; however each time the octopus left the den, it did not return to an area it had
previously searched which suggests that octopuses retain a working memory of landmarks and spatial
cues. Selection pressure for such a memory system may account for why octopuses have developed
the highly sophisticated visual and tactile-based memory system described by Mather (1995; 2006).
Octopus learning is almost entirely environmentally dependent, rather than socially dependent, since
they live solitary lives, unless taking part in reproductive behavior (Mather, 2006; Leite et al., 2009).
Consequently any learning that takes place is a result of interactions the octopus has with its prey,
predators, and natural habitat.
This research investigated the handling time and penetration techniques the red octopus (Octopus
rubescens) utilizes when offered a thin shelled clam (Nuttalia obscurata) or a thick shelled clam
(Venerupis philippinarum). Clam characteristics such as size, weight, adductor muscle strength, and
shell thickness were measured to determine what parameters the octopuses take into account when
utilizing a given handling mechanism to penetrate a bivalve. We also investigated the capabilities of
the red octopus to complete a novel task, which entailed rotating a plastic cap from a glass jar
containing a food reward within. This research explored the physical features of bivalves, which may
influence predator penetration tactic and how experience with a specific prey item influences the
handling time; consequently, we asked the following questions:
Is the handling time of the thick shelled clams greater than that of the thin shelled clams?
Do octopuses possess the ability to decrease handling time of the bivalves with experience?
Can octopuses learn how to successfully open a lidded glass jar containing a food reward?
Methods
Octopus Collection
Nine red octopuses (Octopus rubescens), regardless of sex, were collected via SCUBA at Admiralty
Bay on Whidbey Island, Washington (48°09’47.81”N 122°38’14.81’W) every 21 days over the
course of 2 months from June 29th to August 21st 2014 for a total sample size of 27 octopuses. A
pebble beach bordered the shore line and as the beach sloped into the bay the steep bank reached
approximately 20 m before it flattened out. Glass bottles settle to the sea floor at this location where
the octopuses find refuge; the octopuses were confined to locations only where these glass bottles
were found.
80
Bottles were retrieved and any barnacle and algal growth was scraped off with a shell to determine
whether or not a red octopus inhabited the bottle. If so, the bottle was collected, placed in a 3.8 L
Ziploc® bag, sealed, and placed in a mesh collection bag. Once on shore, each bottle was inspected
for strings of eggs laid on the interior portion of the bottle. If the bottle contained eggs, the octopus
and the bottle were subsequently returned to the ocean floor. However, if no eggs were present, the
octopus was removed from the glass bottle, transferred to a red 1 L Nalgene® bottle, sealed with
plastic window screen and an elastic band, placed in an aerated cooler, and transported to Rosario
Beach Marine Laboratory (RBML), Anacortes, Washington ~48 km from the collection site. All 9
octopuses were individually housed in enclosed containers (50 cm x 30 cm x 50 cm) with constant
flowing ambient seawater via a manifold system (Chase and Verde, 2011); the enclosed containers
were maintained in seawater raceways (240 cm x 60 cm x 50 cm) to maintain a constant temperature
of 12 °C.
Each octopus was given a minimum of 48 h to acclimatize to the free flowing sea water system and
fed purple shore crabs (Hemigrapsus nudus) while acclimating to the containers. It was not until each
octopus readily consumed crabs that a 24 h starvation period was initiated prior to experimentation.
Clam Treatments
Eighteen octopuses were randomly assigned, with the aid of a random numbers table, to be fed either
a thin shelled savory clam (Nuttalia obscurata) or thick shelled Manila clam (Venerupis
philippinarum) for 11 consecutive days. Red octopus middens within the Admiralty Bay region have
recorded both N. obscurata and V. philippinarum shells, which indicate both are appropriate, prey test
subjects. Bivalves were selectively chosen between 30 and 45 mm in length to be used as the prey
offered to each octopus. The savory clams were purchased from the local supermarket and the Manila
clams were generously donated by Penn Cove Shellfish (Coupeville, Washington). Before each
feeding sequence, the morphometric characteristics of each bivalve were noted including bivalve
weight (g), length (mm) and width (mm). Each octopus was placed in an observation tank (80 cm x
60 cm x 50 cm; Figure 1) equipped with three Logitech C615 cameras mounted in custom made
underwater Lexan housings which provided submerged and overhead views of the octopuses feeding
behaviors. An H1a Hydrophone (Aquarian Audio), connected to an iRigPRE preamplifier, was
submerged to acoustically record any bivalve drilling activity under the octopus tentacles.
The octopus was allotted three minutes to acclimate to the tank before the clam was placed within
reaching distance of the octopus. At this time both video (Eyeline Video System) and sound software
(Wavepad Sound) began recording the octopuses behavior. If the octopus made no advances on the
clam within the first 15 minutes of recording, the clam was moved within 8 cm of the octopus. The
trial was deemed unsuccessful after 60 minutes if the octopus made no advances on or was
unsuccessful in opening the bivalve. This process continued with each octopus for 11 consecutive
days. On the 12th experimentation day, octopuses that were regularly fed a thin shelled clam were
provided a thick shelled clam and vice versa. This was done to observe changes in handling behavior
of the octopuses to a different bivalve prey item.
Handling time was measured from the time the octopus took the clam beneath its buccal web to the
moment it released the opened clam from its tentacles. If the octopus successfully pulled apart or
drilled the clam, the handling time was recorded. If neither of these conditions were met, observations
continued and the handling time was restarted at the next instance the octopus took the clam under its
buccal web.
81
Overhead Webcams
Seawater Hose
Drain
Webcam Cables
Hydrophone Cable
Figure 1. The octopus observation tank equipped with wooden frame, seawater hose, drain, overhead webcams
and submerged webcam, and hydrophone.
Octopus Learning Curve
Prior to testing, the octopus was placed in the observation tank three minutes prior to the jar
containing a live food reward, a purple shore crab (Hemigrapsus nudus). Initially, the capped jar with
a single crab was placed inside the observation tank with the octopus and its behavior was noted.
However, there was zero success rate of the octopuses retrieving the crab from the capped jar.
Therefore, after the first trial the jar was presented to the octopus without the cap. Once the octopus
was able to retrieve the crab four consecutive times, the cap was placed on top of the jar without
being screwed on. After the octopus displaced the lid to the jar and retrieved the crab four consecutive
instances the cap was turned slightly. This means that the physical turning of the cap in the
counterclockwise direction would be the only way to retrieve the food reward. After completing this
task four consecutive times, the cap was tightened 0.25 of a full turn after successful retrieval of the
crab. Handling time was measured from the instance the octopus made contact with the jar to the
moment a single tentacle made contact with the crab within the jar.
Adductor Muscle Strength
Methods from Anderson and Mather (2007; see Figure 2) were employed to calculate pulling force of
the adductor muscle of each species of clam. A Jennings Ultra Sport V2-30 scale was mounted on a 5
x 15 cm wooden frame which was utilized to measure the force necessary to open the shells of each
82
species of clam (N. obscurata n = 36; V. philippinarum n = 34) by 3 mm. Clams were selectively
chosen varying in shell length from 30 to 60 mm, dried, weighed, and suction cups were superglued
onto the center of each shell. The clams were air dried for 30 min (to allow the adhesive to cure)
before they were fastened to both sides of the frame. The stainless steel bolt was tightened until the
clam was taught, the scale was zeroed, and the shells were pulled until a 3 mm gape was visible
between the clam shells. Once the force was recorded the shells were immediately separated
completely and all soft tissue was removed and weighed (wet weight).
Figure 2. Schematic drawing of typical clam shell (Venerupis philippinarum) displaying the five possible
regions where Octopus rubescens may drill holes. Image from: naturalhistory.museumwales.ac.uk/.
Shell Features
Penetrated bivalve shells were separated according to the presence or absence of a drill hole. Drill
hole location was determined on either the left or right shell and categorized into one of five positions
on the shell’s surface: posterior, anterior, ventral, umbo or center (Figure 2). Whether or not the hole
punctured the anterior or posterior adductor muscle was recorded as well. Surface area of each drilled
shell was calculated via a plastic transparency sheet that was molded to the inside of each drilled
shell, cut out, and weighed and the same method was used to measure the surface area of both the
anterior and posterior adductor muscle scar. The mass of each cut out (shell and adductor muscle
scars) was compared to a transparency sheet standard curve (mass (g) vs surface area (mm)) to best
estimate the surface area of the drilled shell and both the anterior and posterior adductor muscle
(Figure 2).
Data Analysis
Data from this study was analyzed using IBM SPSS Statistics Data Editor Version 21 software to
perform linear regression, Student’s T-test, and Mann-Whitney U-test. Student’s T-test was used to
83
analyze data (prey handling time) that met the assumptions of normal distribution or equal variance.
Mann-Whitney U Test was conducted on data (shell thickness and adductor muscle strength) that
were not normally distributed or showed unequal variance.
Results
Handling Times
When octopuses were fed bivalves of differing species, they exhibited different prey processing times
and behaviors. The mean handling time of octopuses fed thick shelled bivalves (V. philippinarum)
was 1.8 ± 1.5 hrs (for both drilled and pulled thick shelled prey items consumed) (Figure 3a) whereas
the mean handling time of octopuses fed thin shelled bivalves (N. obscurata) was 0.4 ± 0.2 hrs
(Figure 3b). Therefore, it took approximately 4.5 times longer to penetrate a much thicker shelled
bivalve than a thin shelled bivalve (Students T-test, p < 0.001, F = 112.1, n thick = 48, n thin = 84). The
average time required to drill a bivalve (2.7 ± 0.4 hrs) was significantly greater than the time required
to pull a bivalve apart (1.2 ± 0.2 hrs) (Student’s T-test, p < 0.001, F = 162.5, ndrilled = 34, npulled = 98).
The octopuses displayed a decrease in average handling times over the course of the 11 trial days and
the octopuses fed V. philippinarum displayed stronger negative correlation over time (greater slope)
than the octopuses fed N. obscurata (Figure 3c). When octopuses were presented with a bivalve of a
thicker shell thickness than they were normally fed, the handling time increased by ~5 times.
Likewise, when the octopuses were presented with a bivalve of a thinner shell thickness the handling
time decreased by ~5 times (Figure 4).
Shell Thickness and Muscle Strength
The mean shell thickness of V. philippinarum (n = 48) was 1.21 ± 0.20 mm which is ~20% thicker
than the shell thickness of N. obscurata (n = 84) which was 1.02 ± 0.26 mm (Mann-Whitney U Test,
p < 0.001, Z = 4.138, n = 130). Mean muscle tissue strength (Figure 5) of the thick shelled bivalve
(1054.3 ± 314.7 g force . g -1 wet weight, n = 34) was significantly greater (Student’s T-test, p <
0.001, F = 111.6) than that of the thin shelled bivalve (356.7 ± 147.8 g force . g -1 wet weight, n = 36).
Shell Penetration Techniques
Penetration techniques of the octopuses varied between the prey species. Only 1.2% (1 of 84) of the
opened thin shelled bivalves was drilled whereas 69.4% (34 of 49) of the thick shelled bivalves were
drilled (Figure 6). Of those shells (regardless of shell thickness) that were drilled, 56% of the bored
holes were located within the anterior region of the bivalve shell (Table 1) and every drilled hole in
the anterior region of the shell was located within the anterior adductor muscle scar. The surface area
anterior adductor muscle scar is significantly smaller than the posterior adductor muscle scar (MannWhitney U Test, p = 0.001, Z = 3.352, n = 76). Nearly half (53.8%) of the total thick shelled bivalves
provided to the octopuses were unsuccessfully penetrated and 20.8% of the total thin shelled bivalves
were unsuccessfully penetrated.
84
Figure 3. Average time for octopuses (Octopus rubescens) to penetrate (a) thick shelled bivalves (1.8 ± 1.5 hrs)
versus (b) thin shelled bivalves (0.4 ± 0.2 hrs). Penetration time of thick shelled bivalves (n = 48) was
significantly greater (Students T-test, p < 0.001, F = 112.1) than thin shelled bivalves (n = 84). The
decreasing slope of the trend line (c) indicates decreasing handling time over the 11 day trial;
octopuses feeding on the thick shelled bivalves display a stronger inverse correlation than the
octopuses feeding on the thin shelled bivalves.
85
Figure 4. The bivalve handling time of Octopus rubescens when their prey items were reversed between thick
and thin shelled bivalves (and vice versa) on day 12 (n = 18). When thin shelled bivalves were fed to
octopuses for the first 11 days of the trial (0.4 ± 0.2 hrs), the handling time increased ~5 times when
presented with a thicker shelled bivalve (2.2 ± 1.6 hrs). When thick shelled bivalves were fed to
octopuses for the first 11 days of the trial (1.8 ± 1.5 hrs) the handling time decreased to ~0.2 of the
normal handling time (0.3 ± 0.2 hrs) when presented with a thinner shelled bivalve. Data are mean ±
SE.
Figure 5. Mean pulling force of (Venerupis philippinarum, n = 34) and thin shelled (Nuttalia obscurata, n = 36)
bivalves as a function of increasing shell size. Pulling force of thick shelled bivalves (1054.3 ± 314.7
g force . g-1 wet weight) was significantly greater (Students T-test, p < 0.001, F = 111.6) than of thin
shelled bivalves (356.7 ± 147.8 g force . g-1 wet weight). Methods of measuring bivalve pulling
strength were referenced from Anderson and Mather (2007).
86
Figure 6. Frequency of Octopus rubescens drilling into or pulling thick shelled (Venerupis philippinarum,
n = 48) and thin shelled (Nuttalia obscurata, n = 84) bivalves over the 11 day period.
Table 1. Frequencies and percentages of drill hole locations found in five different regions of thick (Venerupis
philippinarum, n = 35) and thin (Nuttalia obscurata, n = 1) shelled bivalves after predation by Octopus
rubescens.
Anterior
Posterior
Umbo
Center
Ventral
Within
Muscle Scar
Sample Size
19
7
7
3
0
23
Percentage (%)
53
19
19
8
0
64
87
Figure 7. Mean time for Octopus rubescens to retrieve the food reward within the glass jar on each
consecutively successful trial day. Octopuses were presented with (a) no lid (n = 3), (b) lid placed on
(n = 2), (c) lid slightly latched (n = 2). Individual octopus did not proceed to the next treatment until
the given task was completed on four consecutive days; the average time of each consecutive
successful trial is reported. Data are mean ± SE.
88
Discussion
The octopuses handling behavior of the two different bivalve species was strongly influenced by both
shell thickness and adductor muscle strength. The thicker shelled and stronger V. philippinarum were
primarily drilled while the thinner shelled and weaker N. obscurata were predominately pulled apart.
Venerupis philippinarum were mostly drilled because the greater strength of the adductor muscles
prevented the octopus from physically pulling apart the shells. Consequently, the octopus resorted to
drilling into the shell with its radula, injecting a paralyzing venom (cephalotoxin) into the soft tissue
of the clam from the extendible salivary papilla, and opening the clam by successfully pulling the
shells apart due to the paralyzed and weakened adductor muscles (Mather and Anderson, 2000). In
contrast, N. obscurata displayed much lower adductor muscle strength resulting in higher incidences
of being physically pulled apart to produce a gape between the shells and could allow the octopus to
inject venom directly into this gape to further paralyze the bivalve’s muscles (Runham et al., 1997;
Anderson and Mather, 2007). The difference in adductor muscle strength between bivalve species
may be due to the ecological location of these two bivalves. Venerupis philippinarum has a much
shorter siphon and only burrows about 10 cm or less beneath the surface of the sediment whereas N.
obscurata, which has a longer siphon, burrows up to 30 cm within the sediment (Dudas et al., 2005).
Consequently, adductor muscle strength of V. philippinarum may be greater to compensate for its
higher vulnerability in the shallower sediment to predators such as crabs, octopuses or starfish.
Octopuses are tactile foragers meaning they use their tentacles to grope the sea floor for prey and
‘pounce’ by engulfing it within its buccal web (Huffard, 2007). If V. philippinarum are commonly
found closer to the surface of the substrate, they are more likely to be detected by a predator including
the red octopus; however since N. obscurata are buried deeper within the sediment, they may not be
as easily preyed upon in the natural environment. Pulling bivalve shells apart takes less time than
drilling, however, the energetic cost per minute of handling prey while prying is 1.29 times greater
than when drilling (McQuaid, 1994). The greater the amount of energy expenditure allocated to prey
consumption leaves less time to invest in reproduction, foraging for more easily penetrable prey,
guarding the den, or any other activity that may increase fitness.
This study revealed that adductor muscle strength has a greater influence on the octopuses’
penetration method than the physical thickness of the bivalve shell; however, the thickness of the
bivalve shell does have a substantial influence on handling time. Since the red octopuses took nearly
4.5 times longer to penetrate the thick shelled bivalves than the thin shelled bivalves in laboratory
conditions, the thickness of the shell would have a greater influence on the octopuses’ penetration
method if bivalve shell drilling was the initial penetration method.
The red octopus displayed the ability to reduce handling time over the course of the 11 day
investigation although there was a large variation in mean handling times from day to day; both V.
philippinarum and N. obscurata treatments experienced a general decrease in handling times over the
course of 11 days. The octopuses fed V. philippinarum displayed an average of 121 min (65%)
decrease in handling time between day 1 and day 11 of experimentation and the octopuses fed N.
obscurata displayed an average of 9 min (30%) decrease. Octopuses are arguably the most intelligent
invertebrates because they have the ability to retain short term working memory, establish prey
preferences, strategize foraging patterns (Mather, 1991b) and make adjustments to problem solving
(Finn et al., 2009). Consequently, this decrease in prey handling time would not be possible without a
working memory. With respect to this investigation, since bivalve prey were only provided every 24
hrs, a minimum of a 24 hrs working memory may be necessary to recollect which penetration method
successfully breached the bivalve shells and which were not. According to Boal et al. (2000), O.
bimaculoides acquire spatial knowledge within a 24 hr time period and have the ability to retain such
working memory as exploratory awareness for up to a week. Octopuses first attempt to pull apart the
89
bivalve shells with their tentacles (Fiorito and Gherardi, 1999; Steer and Semmens, 2003) and if
unsuccessful, they resort to drilling into the surface of the bivalve shell with their radula or simply
give up (McQuaid, 1994; Fiorito and Gherardi, 1999; Mather, 2006; Hufford, 2007). The time with
which the octopuses made the transition from pulling to drilling, on the V. philippinarum bivalves,
decreased drastically over the course of the 11 day trial suggesting that O. rubescens has the innate
ability to learn and associate a specific species of bivalve with a particular handling mechanism
(Mather, 2008).
The octopuses were fed a bivalve species with a specific shell thickness on the first 11 days of each
trial and upon the 12th day they were presented with the reciprocal shelled bivalve. When O.
rubescens (fed thin shelled bivalves for the first 11 days) was presented with a thicker shelled bivalve
on day 12, they took an average of 114.3% longer than the average of the octopuses that were fed the
thick shelled clam on a regular basis for all 11 days. This increase in time may be due to more
extensive investigation of the specimen and greater preliminary pulling with the tentacles in an
extended attempt to pull the shells apart. Octopuses gave up on the thicker shelled organisms on three
(out of a total of 9) different accounts suggesting that the energy required to penetrate the clam was
much greater than the energy content of the prey organism itself (if it were digested). Likewise, when
the octopuses were presented with a thinner shelled organism on day 12, the handling time decreased
by an average of 80.2% from the average of the octopuses that were fed the thin shelled clams on a
regular basis. This decrease may be a result of a greater initial test pulling strategy the octopuses
adopted over the past 11 days when fed a much thicker organism.
The data suggest that O. rubescens presented with N. obscurata processed these thin shelled bivalves
by pulling them apart (98.8%). In contrast, O. rubescens exposed to V. philippinarum (thick-shelled)
bivalves drilled for 69.4% and pulled for 30.6%; this higher incidence of pulling is due to three (out
of a total of seven octopuses that penetrated thick-shelled bivalves) larger octopuses that were
provided relatively smaller-sized clams which were most likely easier to pull apart. Handling times
and penetration techniques would have been more comparable if bivalves were chosen based on the
relative size of the octopus; this would control for the strength variation of both the bivalves and
octopuses that is often correlated with size (Mather and Anderson, 2000) since octopus used for the
bivalve experiments varied in size from 92.0 to 276.8 g.
Octopus rubescens selected locations of the shell to drill which increased shell penetration efficiency
(Anderson et al., 2007). In this investigation, on average, the octopuses exhibited a preference (53%)
to drill within the anterior region of the shell rather than the other four regions (posterior, ventral,
umbo or center). If O. rubescens were drilling at random locations on the 5 regions of the shell, this
percentage of drilled holes within each region would be expected to be evenly distributed at
approximately 20% among all five regions of the bivalve shell. The majority (64%) of the drilled
shells had drill holes within either the anterior or posterior adductor muscle scars. These numbers
corroborate the work conducted by Anderson et al. (2008) who reported 52% of drilled shells were
bored in the anterior region of the shell and 64% of the drilled shells had holes within an adductor
muscle scar. The area of the anterior adductor muscle occupies 4.2% of the total surface area of the
bivalve shell and the probability of drilling a hole within this specific area of the shell is relatively
small. The preference to drill into the anterior region may be due to the anterior adductor muscle
being significantly smaller than the posterior adductor muscle, and therefore is weaker. This muscle
could be the “Achilles heel” of the bivalve and would be the ideal location for the octopus to inject its
venom in order to paralyze the muscle and make it easier to pull the bivalve shells apart. It is
important to note that some individual octopuses randomly drilled holes in a variety of locations on
the shell which may be due to relatively “young” octopuses learning the most efficient locations on
the shell to drill. Outer shell morphological features that could provide information to the octopus as
to where the anterior adductor muscle is located remain unknown.
90
When octopuses were introduced to a novel object to navigate and penetrate to retrieve a food reward,
they had difficulty with the task as it involved rotating the cap off; the octopuses were unable to
unscrew the plastic cap from the glass jar to retrieve the food reward. In the first few days they
experienced no success, giving up at a much faster rate as trials continued (unpublished data), and
eventually ceased advances on the jar. However, when they were offered the task in smaller,
manageable stages (first: jar without lid, second: jar with lid placed on top, third: jar with lid slightly
latched, lastly: jar with lid rotated 0.25 turn) the success rate increased. Again, this is may be
attributed to their short term working memory.
When the octopuses were required to remove the food reward from the jar without a cap, the time it
took for the octopus to advance to the jar and remove the prey decreased each time they were required
to complete the task. This trend is easily noticed in both the no lid and lid slightly latched treatments.
This decrease in time with increased familiarity parallels the work conducted by Fiorito et al. (1990)
who presented O. vulgaris with glass jars closed with plastic plugs containing live crabs as a food
reward. Fiorito et al. (1998) considered the decrease in handling time with increased familiarity as an
indicator of invertebrate learning. In the present study, four consecutive completions of each task
were required of each octopus and this suggests that they are learning the given task and subsequently
reducing processing time. This decrease in handling time with increased experience would not be the
case if the red octopus had no working short term memory and advances on the prey were random.
Mather (2008) suggests that octopuses also have the ability to retain working memory of foraging
areas from the recent past. For instance, Mather (2008) found that O. rubescens have the ability to
actively forage in areas surrounding their central dens. Throughout the course of a given day, a single
octopus does not navigate the same foraging pattern twice and suggests that octopuses possess the
ability to be “conscious” (Mather, 2008) of their environment within a comprehensive workspace by
storing memory inputs.
In this study once the cap was introduced, the octopuses were more determined to remove it because
they had the ability to recall the memory of previously familiarizing themselves with the object and
were able to penetrate the jar. This may explain the decrease in mean handling time from the no lid
treatment to the treatment where the lid was first introduced. The variety in handling times between
days 1 and 2 versus 3 and 4 when the lid was first introduced may be explained by increased interest
in the novel lid by the octopus. Octopuses were often observed removing the lid from the jar,
engulfing it within the buccal web and rotating it with its tentacles multiple times to investigate or
“play” with the novel, plastic lid which they had never been introduced to before further investigating
the newly opened jar.
Much remains to be studied of the prey handling procedures, especially the boring mechanism
exhibited by octopus, because it is a very effective predatory mechanism and it remains an interesting
behavior involving many areas of biological interest. How octopuses target the adductor muscle from
the exterior of the bivalve needs to be further investigated as well. Signs of where the adductor
muscle is located may be indicated by any of the following bivalve characteristics: color, chemical
cues, and external shell morphometries. Alternatively, a possible knocking mechanism utilized by the
octopuses’ beak upon the bivalve shell to detect the presence of the adductor muscles may be used but
this remains to be investigated.
91
Additional questions that remain to be answered on how octopuses prey on bivalves include:
Are individual octopuses specialized or generalist predators in the natural environment?
How long do octopuses’ working memory lasts and how does it affect predatory and feeding
procedures or mechanisms?
What is the energy cost of pulling versus drilling bivalve prey items?
What mechanisms do octopuses utilize to determine where the adductor muscle is located?
Is drilling onto the adductor muscle a learned behavior or an innate behavior?
Acknowledgements
We would like to thank Kirk Onthank for his Octopus rubescens expertise and extensive knowledge
about octopus, Philip Hortin of PM Solutions Down Under (Australia) for providing us with the
blueprints for the underwater webcam housings, and William Tefft and Timothy Allen for
constructing the housing for the cameras. We also thank Tim Jones of Penn Cove Shellfish for
donating the Manila clams and Jim Nestler and divers of Rosario Beach Marine Laboratory for
laboratory and logistical support. We are grateful to Lisa Lobel for her editorial comments and
suggestions that made this manuscript much better. Financial support was provided by Maine
Maritime Academy.
Literature Cited
Anderson, R.C., and J.A. Mather. 2007. The Packaging Problem: Bivalve Prey Selection and Prey Entry
Technique of the Octopus Enteroctopus dofleini. Journal of Comparative Psychology, 121:300-305.
Anderson, R.C., D.L. Sinn, and J. A. Mather. 2008. Drilling Localization on Bivalve Prey by Octopus
rubescens Berry, 1953 (Cephalopoda: Octopodidae). The Veliger, 50:326-328.
Arnold, J.M., and K.O. Arnold. 1969. Some Aspects of Hole-Boring Predation by Octopus vulgaris. American
Zoologist, 9:991-996.
Baddeley, A. 1992. Working Memory. Science, 255:556-559.
Boal, J.G., A.W. Dunham, K.T. Williams. 2000. Experimental evidence for spatial learning in octopuses
(Octopus bimaculoides). Journal of Comparative Psychology, 114:246-252.
Boulding, E.G. 1984. Crab-resistant Features of Shells of Burrowing Bivalves: Decreasing Vulnerability by
Increasing Handling Time. Journal of Experimental Marine Biology and Ecology, 76:201-223.
Byrne, R.A., M.J. Kuba, D.V. Meisel, U. Griebel, and J.A. Mather. 2006. Does Octopus vulgaris have Preferred
Arms? Journal of Comparative Psychology, 120:198-204.
Chase, E.R., and A. Verde. 2011. Population Density and Choice of Den and Food Made by Octopus rubescens
Collected from Admiralty Bay, Washington, in July 2011. Proceedings of the American Academy of
Underwater Sciences, 30:110-116.
Cortez, T., B.G. Castro, and A. Guerra. 1998. Drilling Behavior of Octopus mimus Gould. Journal of
Experimental Marine Biology and Ecology, 224:193-203.
Dudas, S.E., I.J. McGaw, and J.F. Dower. 2005. Selective Crab Predation on Native and Introduced Bivalves in
British Columbia. Journal of Experimental Marine Biology and Ecology, 325:8-17.
92
Ebisawa, S., K. Tsuchiya, and S. Segawa. 2011. Feeding Behavior and Oxygen Consumption of Octopus
ocellatus Preying on the Short Neck Clam Ruditapes philippinarum. Journal of Experimental Marine Biology
and Ecology, 403:1-8.
Finn, K.F., T. Tregenza, and M.D. Norman. 2009. Defensive Tool Use in a Coconut-Carrying Octopus. Current
Biology, 19:R1069-R1070.
Fiorito, G., G.B. Biederman, V.A. Davey, and F. Gherardi. 1998. The Role of Stimulus Pre-exposure in
Problem Solving by Octopus vulgaris. Animal Cognition, 1:107-112.
Fiorito, G., and F. Gherardi. 1999. Prey-Handling Behavior of Octopus vulgaris (Mollusca, Cephalopoda) on
Bivalve Preys. Behavioral Processes, 46:75-88.
Fiorito, G., C. Planta, and P. Scotto. 1990. Problem Solving Ability of Octopus vulgaris Lamarck (Mollusca,
Cehpalopoda). Behavioral and Neural Biology, 53:217-230.
Harper, E.M. 2002. Plio-Pleistocene Octopod Drilling Behavior in Scallops from Florida. Palaios, 17:292-296.
Huffard, C.L. 2007. Ethogram of Abdopus aculeatus (D’Orbigny, 1834) (Cephalopoda: Octopodidae):
Can Behavioral Characters Inform Octopodid Taxonomy and Systematics? Journal of Molluscan Studies,
73:185-193.
Iribarne, O.O., M.E. Fernandez, and H. Zucchini. 1991. Prey Selection by the Small Pantagonian Octopus
Octopus tehuelchus d’Orbigny. Journal of Experimental Marine Biology and Ecology, 148:271-281.
Kier, W.M., and A.M. Smith. 2002. The Structure and Adhesive Mechanism of Octopus Suckers. Integrative
and Comparative Biology, 42:1146-1153.
Lai, Y., J. Chen, and L. Lee. 2011. Prey Selection of a Shell-Invading Leech as Predicted by Optimal Foraging
Theory with Consumption Success Incorporated into Estimation of Prey Profitability. Functional Ecology,
25:147-157.
Lavoie, M.E. 1956. How Sea Stars Open Bivalves. The Biological Bulletin, 111:114-122.
Leite, T.S., M. Haimovici, and J.A. Mather. 2009. Octopus insularis (Octopididae), Evidences of a Specialized
Predator and a Time Minimizing Hunter. Marine Biology, 156:2355-2367.
Maron, J.L. 1982. Shell Dropping Behavior of Western Gulls (Larus occidentalis). The Auk, 99:565-569.
Mather, J.A. 1991a. Foraging, Feeding, and Prey Remains in Middens of Juvenile Octopus vulgaris (Mollusca,
Cephalopoda). Journal of Zoology, 224:27-39.
Mather, J.A. 1991b. Navigation by Spatial Memory and Use of Visual Landmarks in Octopuses. Journal of
Comparative Physiology, 168:491-497.
Mather, J.A. 1995. Cognition in Cephalopods. Advances in the Study of Behavior, 24:316-353.
Mather, J.A. 2006. Behaviour Development: A Cephalopod Perspective. International Journal of Comparative
Psychology, 19:98-115.
Mather, J.A. 2008. Cephalopod Consciousness: Behavioral Evidence. Consciousness and Cognition, 17:37-48.
Mather, J.A., and R.C. Anderson. 2000. Octopuses are Smart Suckers. The Cephalopod Page. Retrieved June 15
(2014).
93
Mather, J.A., T.S. Leite, and A.T. Batista. 2012. Individual Prey Choices of Octopuses: Are they Generalist or
Specialist? Current Zoology, 4:597-603.
Mazzolai, B., L. Margheri, P. Dario, and C. Laschi. 2013. Measurements of Octopus Arm Elongation: Evidence
of Differences by Body Size and Gender. Journal of Experimental Marine Biology and Ecology, 447:160-164.
McQuaid, C.D. 1994. Feeding Behavior and Selection of Bivalve Prey by Octopus vulgaris Cuvier. Journal of
Experimental Marine Biology and Ecology, 177:187-202.
Onthank, K.L., and D.L. Cowles. 2011. Prey Selection in Octopus rubescens: Possible Roles of Energy
Budgeting and Prey Nutritional Composition. Marine Biology, 15:2795-2804.
Pyke, G.H., H.R. Pullman, and E.L. Charnov. 1977. Optimal Foraging: Selective Review of Theory and Tests.
The Quarterly Review of Biology, 52:137-154.
Runham, R.W., C.J. Bailey, M. Carr, C.A. Evans, and S. Malham. 1997. Hole Drilling in Crab and Gastropod
Shells by Eledone cirrhosa (Lamarck, 1798). Ecology of Marine Molluscs, 61:67-76.
Smale, M.J., and P.R. Buchan. 1981. Biology of Octopus vulgaris off the East Coast of South Africa. Marine
Biology, 65:1-12.
Smith, C.D. 2003. Diet of Octopus vulgaris in False Bay, South Africa. Marine Biology, 143:1127-1133.
Steer, M.A., and J.M. Semmens. 2003. Pulling or Drilling, Does Size or Species Matter? An Experimental
Study of Prey Handling in Octopus dierythraeus (Norman, 1992). Journal of Experimental Marine Biology and
Ecology, 290:165-178.
Werner, E.E., and D.J. Hall. 1974. Optimal Foraging and the Size Selection of Prey by the Bluegill Sunfish
(Lepomis macrochirus). Ecology, 55:1042-1052.
Wodinsky, J. 1969. Penetration of the Shell and Feeding on Gastropods by Octopus. American Zoologist, 9:9971010.
Wodinsky, J. 1978. Feeding Behaviour of Broody Female Octopus vulgaris. Animal Behaviour, 26:803-813.
94
In: Lobel L.K. ed. Diving for Science 2015.
Proceedings of the American Academy of Underwater Sciences 34th Symposium.
Heavy breathing: how much gas is consumed in a diving emergency?
Martin D.J. Sayer1*, Nick Bailey2
1
UK National Facility for Scientific Diving, Scottish Association for Marine Science, Oban, Scotland
[email protected]
2
UK Health and Safety Laboratory, Buxton, United Kingdom
* presenting and corresponding author
Abstract
The UK Diving at Work Regulations (1997) state that occupational divers must be provided
with a fully independent breathing supply with access to a gas volume that is capable of
supporting an ascent to the surface or safety in the event of a failure of the primary breathing
system. The Regulations do not, at present, provide any guidance as to what breathing rates
should be employed when computing or implementing bail-out options. The UK Health and
Safety Executive (HSE) have recently conducted a review of published emergency breathing
rates in an attempt to provide new guidance on what levels should be considered in the
planning process. A wide variety of breathing rates was identified during the review but the
conclusions were that a general breathing rate of between 50 or 75 l.min-1 might be
appropriate. The decision on the actual breathing rate employed when calculating bail out
requirements would need to be derived from the risk assessment for the dive being
undertaken. The implications of such breathing rates are placed into context of currently
available diving equipment including the use of cylinders that are compressible to pressures
greater than 232bar; 3-litre pony cylinders may not be adequate independent bail-out options
for dives deeper than 30msw. Dive computer downloads, where the computer is integrated
with the divers’ cylinder pressure, provide the opportunity to calculate breathing rates that
actually occur during diving emergencies; examples of such downloads are given. There are a
number of procedures that need to be employed when converting raw dive cylinder pressure
records into estimates of actual breathing rates; these are outlined.
Keywords: emergencies, breathing rates, dive computers
Introduction
Scientific diving operations in UK waters must adhere to the 1997 UK Diving at Work Regulations
(DWR97), which is a Statutory Instrument of the 1974 Health and Safety at Work etc., Act.
Guidance on how to comply with DWR97 is contained within industry sector-specific approved codes
of practice (ACoPs). The ACoP specific to scientific diving (the Scientific and Archaeological
Approved Code of Practice, 2014) was revised recently and, along with generic statements within
DWR97, contains the following guidance related to breathing gas supplies:
• whatever type of breathing apparatus is in use, each diver must carry an independent reserve
supply of breathing gas that can be quickly switched to the breathing circuit in an emergency;
• an alternative breathing gas source or secondary life support system should be provided for
emergency use; and
• the alternative system should have sufficient capacity to allow the diver to reach a place of
safety.
However, there was no guidance provided as to what was “sufficient capacity”.
95
This present study reviews the current literature on breathing rates and attempts to identify those that
are typical for normal diving work and those which would be expected in an emergency. A review is
also conducted of present industry guidance for breathing rates to be used when calculating planned
gas needs for normal work and emergencies. The overall objective is to produce guidance on how
commonly employed alternative breathing gas supplies may last in a diving emergency. In support of
the consultation process conducted during the review, cases of dive computer downloads from diving
incidents that included out of air situations were considered; two are presented here.
Methods
Initially a literature search was undertaken for scientific papers from 1970 to present, for gas
consumption rates of divers. Alongside the search for diving papers, a search was carried out for
studies using different types of subjects, from the general population to elite athletes. The search was
initially internet based for published papers. A further literature search was then carried out into the
measurement methods of human physiological testing. This gave clarification of how the volume of
oxygen consumed per minute (VO2) and minute expired ventilation (VE) are interrelated. The search
also looked at calculation methods to substantiate the findings. Alongside this, further physiological
texts, including diving medical textbooks, were sourced and reference-checked. To allow for accurate
comparison of gas consumption levels all data were corrected, where needed, to 1.013 body
temperature and pressure, saturated (BTPS; 1 bar).
Scientific papers
Papers were sourced through the “Rubicon Foundation research repository”, which is a specialist
library for underwater science papers. These papers cited further papers which were sourced through
general internet search engines and, if full text versions were unavailable, were requested through the
UK Health and Safety Executive Knowledge Centre. References to papers in diving text books were
also sourced.
Industry documentation and guidance
Other searches were made into current guidance provided by industry. This was followed up with emails to specific personnel from industry sectors where guidance was not immediately available.
From these searches, a list of organisations that provide guidance was produced as shown below:
•
•
•
•
•
•
•
•
The Association of Diving Contractors (ADC)
International Maritime Contractors Association (IMCA)
International Association of Oil and Gas Producers (OGP)
Royal Navy
US Navy
National Oceanic and Atmospheric Agency (NOAA)
British Sub Aqua Club (BSAC)
Professional Association of Diving Instructors (PADI)
Dive computer data
Data from two dive computer downloads were obtained in accordance with the methodologies
described by Sayer and Azzopardi (2014). Breathing rates were derived from cylinder pressure
readings where this was integrated with the dive computer. Changes in pressure readings were
converted to surface breathing rates (l.min-1) through employing known cylinder volumes, an
integration of the time/pressure dive profile, and correction to BTPS values (Sayer and Azzopardi,
96
2014). All calculations employed a one-minute rolling average to even out the effects of sporadic
cylinder pressure changes.
Results
Hyperbaric research breathing rates
Three papers examined exercise tolerance, submerged exercise at depth and maximal physical work
capacities at depth, under hyperbaric research conditions (Anthonisen et al., 1976; Dwyer et al., 1977;
Thalman et al., 1979); consumption rates of between 84 and 134 l.min-1 were calculated.
Breathing rates from commercial diving industry guidance
The International Marine Contractors Association (IMCA) provides guidance of surface consumption
rates of 35 l.min-1 under normal working conditions, and 40 l.min-1 in emergencies (IMCA, 2002).
The International Association of Oil and Gas Producers (IAOGP) suggest a bail-out gas consumption
rate 45 l.min-1 (OGP, 2008), whereas the Association of Diving Contractors (ADC) recommend
normal working values of 40 l.min-1 and values for emergency events of 50 l.min-1 (ADC, 2012)
Breathing rates from military and government agencies
The UK Royal Navy recommends six surface consumption rates: 9 l.min-1 at rest; 18 l.min-1 for light
work; 30 l.min-1 for moderate work; 40 l.min-1 for heavy work; and 60 l.min-1 for severe work. A rate
of 50 l.min-1 was recommended for generic gas volume calculation (RN, 2013). The US Navy
recommended 40 l.min-1 for normal demand valve diving, 50 l.min-1 for heavy work, and 60 l.min-1
for severe work (USN, 2008). Guidance from the National Oceanic and Atmospheric Administration
(NOAA, 2013) is supposedly based on the US Navy rates but estimates lower values: 12-16 l.min-1
for light work, 20-30 l.min-1 for moderate work, 35 l.min-1 for heavy work and 53 l.min-1 for severe
work.
Breathing rates from recreational training agencies
The Professional Association of Diving Instructors (PADI), Scuba Schools International (SSI) and the
International Association of Nitrox and Technical Divers (IANTD) all advise divers to work out their
consumption rates from their gas usage during dives. Both the Sub-Aqua Association (SAA) and the
British Sub Aqua Club (BSAC) advise using a surface breathing rate of 25 l.min-1 for normal diving;
the stress/emergency rate recommended by the SAA was 30 l.min-1 whereas it was 50 l.min-1 for the
BSAC.
Breathing rates for equipment standards testing
There were a number of standards reviewed that stated the breathing rates that diving respiratory
equipment had to conform to. For example, the British/European standard for open-circuit selfcontained compressed air apparatus (BS EN 250, 2000) states a surface equivalent test rate of 62.5
l.min-1. For open-circuit umbilical supplied compressed gas diving apparatus, rates of 62.5 l.min-1
and 70-85 l.min-1 are stated (BS EN 15333-1, 2008).
Dive computer downloads
The first case study involved two scientific divers diving under ice in Antarctica. One diver
experienced a double free-flow at a depth of 30 metres and so both divers had to share a single air
supply back to the bailout cylinders below the ice-hole. The donor diver had integrated cylinder
pressure and heart monitoring; recordings were at 4-second intervals. From the recorded cylinder
pressures, data were converted to 1-minute rolling averages and corrected for surface-equivalent
pressure and BTPS. The donor diver prior to the incident was breathing at 9.7 l.min-1. As the divers
were sharing a single cylinder, individual rates could not be obtained, but during the share period the
97
average breathing rate per diver was 24.3 l.min-1 with a maximum of 61.1 l.min-1 for both divers.
Following the incident, the donor diver’s breathing rate remained elevated at 16.5 l.min-1.
In a second case, a recreational diving instructor ran out of air after 5-minutes of dive-time and was
unable to rescue his trainee who was in distress with their regulator out of their mouth. The trainee
was in 4.5 metres of water but was unable to fin to the surface as they were over-weighted and died.
The court case surrounding the incident focused on the volume of breathing gas in the cylinder of the
instructor when they initiated the dive. The instructor stated that they had 70bar pressure in a 12-litre
cylinder (840 litres); the computer download suggested this value could have been as low as 29bar
(348 litres). By integrating the curve to run out of air at 380 seconds, BTPS-corrected breathing rates
would have been 37.5 l.min-1 for the 29 bar scenario and 90.5 l.min-1 in the initial pressure had been
at 70 bar. The judgment was that the lower value was more likely.
Discussion
The human basal breathing rate is commonly understood to be around 13 to 17 breaths per minute
with a total volume per breath of between 500 to 600 ml BTPS. Of that, a young adult male will
consume 250 ml of VO2. This would give expected VE of approximately 6.5 to 10.2 l.min-1 at rest
(Slonim and Hamilton, 1981). As the diver works, the breathing rate increases, which is partly caused
by the body’s responses to the increased level of metabolic CO2 being produced.
When a diver finds themselves in an emergency situation a number of physical and psychological
effects occur and include an increase in breathing rate. These effects can be influenced by various
factors, such as training level, competence in dealing with an emergency, or the perceived threat to
the diver. The depth of the dive can also have an effect on the diver’s breathing rate, with the gas
density increasing along with the increased depth. This also has the added effect that at extreme depth
the diver will find it physically more difficult to clear the CO2 produced by the body if they are
working extremely hard (Mitchell et al., 2007).
The literature review produced a large range of measured breathing rates (e.g. 84-163 l.min-1), and a
number of different advisory values (e.g. 25-110 l.min-1). Whereas planning for high rates of use (e.g.
greater than 100 l.min-1) may cover more emergency scenarios (including sharing, for example), it
was considered that a single diver would have problems sustaining such a breathing rate and the
sharing scenario was too rare an event in the occupational diving sectors. A general breathing rate of
between a more pragmatic 50 l.min-1 or 75 l.min-1 was considered more appropriate. The decision on
the actual breathing rate employed when calculating bail out requirements would need to be derived
from the risk assessment for the dive being undertaken.
A common independent breathing gas supply employed in the UK scientific diving sector is the 3litre pony cylinder. At normal compression values of 232 bar, and with assumptions on ascent rate,
safety stops, switchover times, and water temperatures, such an arrangement could only be employed
to depths of 30 metres if breathing rates of 50 l.min-1 or lower were assumed, and for a single diver
only. Relatively controlled bailouts from depths at or approaching 50 metres could only be achieved
if breathing rates of 25 l.min-1 were assumed. Therefore, for deeper diving, planning needs to involve
larger bail-out cylinders if using scuba, the use of independently-rigged twin-sets, and/or staged
cylinders. Compressing to 300 bar is only a partial remedy as compression above about 240bar
complies more with real rather than ideal gas laws and the volumes available to the diver are much
less than standard calculations would suggest.
98
Acknowledgments
Numerous formal and informal inputs to this study were received from the Military (UK and US),
human physiology researchers, diving equipment manufacturers, commercial diving operators, and
recreational training organisations.
Literature Cited
Anthonisen, N.R., G. Utz, M.H. Kryger, and J.S. Urbanetti. 1976. Exercise Tolerance at 4 and 6 ATA.
Undersea Biomedical Research, 3: 95-112.
Association of Diving Contractors (2012). Code of Practice: Conducting Diving Operations in Connection with
Renewable Energy Projects. ADC-CoP: 001. Issue 02-07-2012
BS EN 250. 2000. Respiratory equipment: Open-circuit Self-contained Compressed Air Diving Apparatus
Requirements, Testing, Marking.
BS EN 15333-1. 2008. Respiratory Equipment: Open-circuit Umbilical Supplied Compressed Gas Diving
Apparatus. Part 1: Demand apparatus
Diving at Work Regulations 1997. Statutory Instrument 1997 No 2776.
[http://www.legislation.gov.uk/uksi/1997/2776/contents/made; last accessed 14 July 2015]
Dwyer, J., H.A. Saltzman, and R. O’Bryan. 1977. Maximal Physical-work Capacity of Man at 43.4 ATA.
Undersea Biomedical Research, 4: 359 -372.
International Marine Contractors Association. 2002. D022: The Diving Supervisors Handbook. May 2000
incorporating the May 2002 erratum.
Mitchell, S.J., F.J. Cronjé, W.A. Meintjes, and H.C. Britz. 2007. Fatal Respiratory Failure During a "Technical"
Rebreather Dive at Extreme Pressure. Aviation, Space, and Environmental Medicine, 78: 81-86.
National Oceanic and Atmospheric Administration. 2013. NOAA Diving Manual: Diving for Science and
Technology 5th edition. Palm Beach, Fl. Best Publishing Co. 875pp.
Oil and Gas Producers. 2008. Diving Recommended Practice Report No. 411.
[http://www.ogp.org.uk/pubs/411.pdf; last accessed 14 July 2015]
Royal Navy. 2013. BR2806: Royal Navy Diving Manual.
Sayer, M.D.J., and E. Azzopardi. 2014. The Silent Witness: Using Dive Computer Records in Diving Fatality
Investigations. Diving and Hyperbaric Medicine , 44: 167-169.
Scientific and Archaeological Diving Projects. The Diving at Work Regulations 1997
Approved Code of Practice and Guidance - L107 [http://www.hse.gov.uk/pubns/books/l107.htm; last accessed
14 July 2015]
Slonim, N.B., and L.H. Hamilton. 1981. Respiratory Physiology 4th edition. St. Louis, Mo: CV Mosby & Co.
304pp.
Thalmann, E.D., D.K. Sponhotz, and C.E.G. Lundgren. 1979. Effects of Immersion and Static Lung Loading on
Submerged Exercise at Depth. Undersea Biomedical Research, 6: 259-290.
US Navy. 2008. U.S. Navy Diving Manual REVISION 6 SS521-AG-PRO-010 0910-LP-106-0957
99
In: Lobel L.K. ed. Diving for Science 2015.
Proceedings of the American Academy of Underwater Sciences 34th Symposium.
Mapping the 1860 Wreck of the US Coast Survey Vessel Robert J. Walker
Peter F. Straub1,*, Stephen D. Nagiewicz1,2 Vincent J. Capone3, Daniel Lieb2 and Steven P. Evert1
1
Stockton University, 101 Vera King Farris Drive, Galloway, NJ 08205, USA
[email protected]
2
New Jersey Historical Divers Association, Inc. 2201 Marconi Road Wall, NJ 07719, USA,
http://www.njhda.org/
3
Black Laser Learning, PO Box 339, Hockessin, DE 19707, USA,
[email protected]
* presenting and corresponding author
Abstract
The Robert J. Walker is an iron hull, paddlewheel steamship that saw service in the US Coast
Survey, predecessor to the NOAA Office of Coast Survey, before it was lost with 21 men
after a collision at sea off Atlantic City, NJ in 1860. The wreck was positively identified in
2013 by NOAA and subsequently placed on the US National Parks Service, National Register
of Historic Places. To further document and protect the site, NOAA requested that a
consortium of non-governmental groups undertake the archaeological site work as a
cooperative operation between governmental, non-governmental and academic institutions to
preserve our national maritime heritage. This consortium included local divers, represented by
the New Jersey Historical Divers Association (NJHDA), Stockton University and Black Laser
Learning, a marine survey and education company. Side scan and bathymetric surveys were
undertaken with a Klein 3900 digital side scan sonar and an Edgetech 6205 multi-beam
bathymetric sonar. A Seabotix LBV was deployed for remote video survey. Divers from the
NJHDA thoroughly surveyed the site over a weeklong expedition, taking precise
measurements, underwater photographs and video. Geo-referenced bottom maps were
constructed from mosaics of the sonar data and digitized wreck features in ARC-map.
Integration of data from multiple sensors allowed reconstruction of the site with digital CAD
drawings to produce rich multi-layered GIS products to support conservation of this historic
site and to promote its use in the dive community.
Keywords: wreck, Robert J. Walker, mapping, sonar, archaeology
Introduction
The United States Coast Survey Steamer (U.S.C.S.S.) Robert J. Walker was among the first iron
hulled, paddlewheel steamer vessels to see service in the United States Coast Survey, now the
National Oceanic and Atmospheric Administration (NOAA), {Office of Coast Survey (Figure 1.)}. In
1847 as part of an experimental series of eight vessels built as revenue cutters, the Walker was
commissioned by the Revenue Marine Service, the precursor service to today’s Coast Guard. The
Walker, like her other two sister ships, was deemed too large and too slow to be effective in the
Revenue Marine Service and was given over the Coast Survey in 1848 where they were more suitable
as hydrographic vessels. The Walker was instrumental in bathymetric survey of Mobile Bay in 1848,
and the Gulf and southeast coast of the United States in the decade prior to the outbreak of the US
Civil War. This information was vital to the later effectiveness of the wartime blockade strategy. In
addition, the Walker contributed to updated charts of the Gulf Stream (Delgado, 2013). While headed
north for repairs in New York City, the Walker collided at night in a gale with the commercial
schooner Fanny and sank off of Absecum (sic) approximately 10 miles west of Absecon Island and
Atlantic City, New Jersey (NY Times, 1860). Twenty-one lives were lost in the sinking while 49
100
survived. Accounts of the sinking by survivors referenced approximate distances from the Atlantic
City lighthouse which was clearly visible in the west (Theberge, 2007). In the confusion of the
sinking and in the subsequent entry of the country into civil war in 1861, the actual site of loss was
not determined, no salvage was attempted and the wreck site remained a mystery for 153 years
(Forsythe, 2013; Theberge, 2007).
Figure 1. Painting of the U.S.C.S.S Robert J. Walker by W.A.K. Martin, 1852 (courtesy of The Mariners
Museum and Park, Newport News, VA) and commemorative plaques (r) placed in memoriam at the
lighthouse, Atlantic City, NJ June 21, 2015 by the National Oceanic and Atmospheric Administration
(photos S. Nagiewicz).
Following up on local diver accounts, Joyce Steinmetz of East Carolina University and the Maritime
Heritage Program, NOAA Office of Marine Sanctuaries narrowed the possible sites of the R.J.
Walker sinking to a site known to local south Jersey divers as the $25 wreck, ostensibly named as the
numbers of the wreck were sold for this price. In response to the recent hurricane Sandy on the east
coast, NOAA Coast Survey was scheduled for the local area and took the opportunity to survey
several likely wreck sites. The NOAA team, including sonar, bathymetry and divers, was able to
positively identify the $25 wreck as the U.S.C.S.S. Robert J. Walker in the summer of 2013 based
particularly on a number of characteristics including its unique steam engines and paddlewheel
designs (Isherwood, 1852; Delgado, 2013).
The U.S.C.S.S. Robert J. Walker site was placed on the National Register of Historic Places by the
National Park Service in 2014 to recognize the historic nature of the wreck site and to preserve
artifacts at the site while allowing local divers to access the site. The Maritime Heritage Program of
NOAA Office of Marine Sanctuaries (NOAA-OMS) decided on this course of action in lieu of
designating the site a Marine Sanctuary which would have severely restricted access to only permitted
researchers (Delgado, 2013). To help conserve and curate the Robert J. Walker Historic Site, the
Maritime Heritage Program- NOAA-OMS enlisted the aid of a consortium of groups including local
divers represented by the New Jersey Historical Divers Association (NJHDA), academic institutions
represented by Stockton University and experts in underwater operations represented by Black Laser
Learning. The charge of this group was to put together a community based expedition that would
perform an archaeological survey of the Robert J. Walker historic site and produce base maps and a
photographic and video record that could be used to monitor and conserve the site over time. The
101
group operated under the flag of the Explorers Club, New York, New York and the Club’s historic
Ocean Flag #132 flew over the expedition.
Methods
Remote Sensing
Remote sensing was undertaken at the Walker site from the Stockton University vessel the RV
Gannet from May to July 2014. Geo-referenced side scan sonar was used to characterize the Walker
wreck and delineate the site. An L3/ Klein 3900 digital side scan was towed over the site at 445 kHz
and 900 kHz frequencies to locate and to image the wreck. Side scan data was processed in Sonar Pro
12.1 (L3/Klein, Salem, NH) software and mosaics of the site produced in Sonar Whiz 5 (Chesapeake
Technologies, Mountain View, CA) software. Bathymetric data was collected with an Edgetech 6205
(Edgetech West Wareham, MA) multi-phase echosounder bathymetric sonar and processed with
Hypack 2014 (Hypack, Middletown, CT) hydrographic survey and processing software. Video was
recorded of the site with a Seabotix LBV-300 S5 remotely operated vehicle.
Dive Operations
Divers from the New Jersey Historical Divers Association (NJHDA) dove the site for preliminary
analysis in May 2014. From this initial dive and from analysis of remote sensing data, a weeklong
expedition was planned for August 2014. Divers were assigned to teams and data collection on
specific sections of the wreck. A centerline tape was pulled over the wreck from bow to stern and the
individual sections of the wreck measured in great detail to produce initial drawings and size
calculations. The wreck was extensively photographed and video taken to document the individual
wreck components and their positions.
Mapping
All geo-referenced sonar and bathymetric mapping data exported as geo-Tiff files were assembled as
layers in ARC-GIS/ARC-MAP 10.2 (ESRI, Redlands, CA). Shape files were produced by digitizing
sonar images to delineate and map wreck components and produce a site map layer. Diver collected
data was used to produce a site map of the wreckage and a detailed computer assisted drawing of the
ship mechanisms, boilers, engines, drive, paddles was produced. Initial drawings of intact
components, based on in some cases the original specifications for the parts, i.e. Isherwood (1852),
were deconstructed to indicate their current deteriorated or damaged situation based on diver
measurements and photographs. 3-D drawings were done in Google Sketch Up Pro 2014 (Google,
Mountain View, CA), Adobe Photoshop and Adobe Illustrator, (Adobe, San Jose, CA).
Results
Initial characterization of the site was undertaken with side scan sonar and a mosaic of the site
developed. Bathymetry of the site showed, as did the side scan, that the wreck was located in a
depression (28 m) compared to the surrounding bottom (25 m) that is probably the result of 150 years
of scour based on currents being deflected by the wreckage (Figure 2). This depression tends to
accumulate silty particles that can make visibility at the site difficult when there is any significant
swell. A preliminary site map was drawn from the sonar images in Arc-Map to locate the prominent
landmarks of the wreck (Figure 2).
102
Figure 2. Robert J. Walker site maps including high frequency 900 kHz, 40 m range, side scan sonar (L),
bathymetry (bottom R.) and wreck diagram developed from side scan sonar data (top R.).
Low pass, high frequency (900 KHz) side scan sonar data more clearly images portions of the wreck
as seen in Figure 3. The bow stern and engine details are matched with photos from the diver survey
to get a better picture of the overall wreck site (Figure 3). The bow is bent back and broken off
indicating it probably hit the bottom first. Imagery of the drive train (Figure 4) shows that the
starboard paddle is still articulated to the drive mechanism while the port paddle has essentially been
broken free and probably impacted the bottom with enough force to bend the hub. The final 3-D
reconstruction of the U.S.C.S.S. Robert J. Walker is shown in Figure 5. The wreckage is shown in its
current configuration and to 3-D scale and will be particularly useful in future comparative studies.
Discussion
Detailed maps of the U.S.C.S.S. Robert J. Walker wreck site produced from this project will serve
dual roles. First, the mapping products will serve as a scientific baseline for historic conservation of
the wreck site. Second, the mapping products are also being used as educational tools and as the basis
for displays at a number of educational venues including NOAA headquarters, Silver Springs, the
Atlantic City Lighthouse, Stockton University, the New Jersey Maritime Museum, and the New
Jersey Historical Divers Association Shipwreck Museum. A diver’s slate for use of the sport diving
community is being produced to summarize the mapping information and site plan and to inform the
diving public of the significance of the site and of its preservation status.
103
Figure 3. Side scan sonar, high frequency 900 kHz (center). Underwater photos from the dive team, top left is
the bow, top right is the remains of the stern, bottom left and right are the engines and boilers amidships
(photos J. Hoyt and bottom right Herb Segars).
104
Figure 4. Side scan imagery (900 kHz) of the starboard (L) and port (R) drive trains and paddle wheels. Below
are the diver photos of the same (photos J. Hoyt).
Figure 5. Final 3-D reconstruction of the Robert J. Walker wreck site to produce a representation of the
wreckage in its current configuration using dive measurements, photos, videos and sonar.
105
The model of community engagement that the NOAA-OMS Maritime Heritage Program has chosen
to pursue in the historical conservation of the U.S.C.S.S. Robert J. Walker resulted in “buy-in” from
the diverse stakeholder groups: local government, U.S. government scientists and archaeologists,
amateur archaeologists, academic scientists and archaeologists, sport divers and fishers and the
general public. By following this path, the Maritime Heritage Program has designated the site as a
registered Historic Place, alerted the public to its role in preserving historic places and at the same
time honored the memory of the twenty-one Coast Survey personnel who lost their lives in the service
of their country. The fact that this project used advanced hydrographic survey technology is a
testament to their pioneering contributions. On June 21st, 2015, World Hydrographic day, NOAA
officially honored the memory of the crew lost in the tragic disaster in a ceremony at the Lighthouse
in Atlantic City, NJ, perhaps the last sight of land they saw. At the lighthouse is a mosaic compass
rose with embedded plaques (Figure 1) honoring the crew and dead of the U.S.C.S.S. Robert J.
Walker so their memory and our debt to them will not be forgotten.
Acknowledgments: The authors acknowledge the contributions of the expedition divers: Dan Lieb,
Steve Nagiewicz, Joyce Steinmetz, Joe Hoyt, Matt Lawrence, Herb Segars, Harry Roecker, Matt
Nigro, Joe Fiorentino, Mike Haas, Mike Pizzio, Mike Lavitt, Shawn Sweeney, Matthew Partrick,
Howard Rothweiler, Al Vogel, Ryan Beatty and the dive expedition surface support team: Paul and
Ruth Hepler/ Venture dive, Ronnie Segars, Jim Delgado and technical support Harry Roecker.
Project support provided by Edward Marsh, Ryan Beaty, Travis Nagiewicz and Howard Rothweiler.
Sponsors support was provided by Stockton University, The Revel Hotel and Casino, Black Laser
Learning and the Maritime Heritage Program in NOAA’s Office of National Marine Sanctuaries.
Stockton University students, Jamie Taylor, Chelsea Shields, Walter Poff, Emily Burnite and Lauren
O’Neil contributed to the project as well as the crew of the RV Gannett, Nathan Robinson, Elizabeth
Zimmermann and Mark Sullivan. This expedition carried flag #132, Ocean flag of the Explorers
Club, New York City, NY.
Literature Cited
Delgado, J. P. (2013). Identification of the wreck of the U.S.C.S.S. Robert J. Walker off Atlantic City, New
Jersey. NOAA’s Office of National Marine Sanctuaries, Silver Spring, Maryland. 56 pgs. Retrieved from:
http://www.lib.noaa.gov/noaainfo/heritage/coastandgeodeticsurvey/RobertJWalker_Preliminary_Archaeologica
l_Report-NOAA.pdf.
Forsythe, D. (2013). The story of the coast survey steamer ROBERT J. WALKER. NOAA Office of Coast
Survey, Coast Survey Communications. 9 pp. Retrieved from:
http://www.nauticalcharts.noaa.gov/RobertJWalker/misc.html.
Isherwood, B.F. (1852). Notes on the U.S. surveying Steam Walker. Journal of the Franklin Institute, Third
Series 24(1):49-55.
Theberge, A. (2007). The Coast Survey 1807-1867; Collisions. NOAA Central Library
Retrieved from: http://www.lib.noaa.gov/noaainfo/heritage/coastsurveyvol1/BACHE5.html#COLLISION.
The New York Times (1860). Loss of the U.S. steamer Walker. New York Times, Jun 23, 1860; The New York
Times Article Archives (1851 – present), NY, NY. pg 8.
Retrieved from: http://www.nytimes.com/1860/06/23/news/loss-us-steamer-walker-twenty-persons-missingparticulars-disasterarrival.html.
106