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Submitted 10 November 2015
Accepted 23 August 2016
Published 4 October 2016
Corresponding author
Richard L. Pyle,
deepreef@bishopmuseum.org
Academic editor
Xavier Pochon
Additional Information and
Declarations can be found on
page 33
DOI 10.7717/peerj.2475
Copyright
2016 Pyle et al.
Distributed under
Creative Commons CC-BY 4.0
OPEN ACCESS
A comprehensive investigation of
mesophotic coral ecosystems in the
Hawaiian Archipelago
Richard L. Pyle1, Raymond Boland2,3, Holly Bolick1, Brian W. Bowen4,
Christina J. Bradley5,6, Corinne Kane7, Randall K. Kosaki8, Ross Langston1,
Ken Longenecker1, Anthony Montgomery4,9, Frank A. Parrish2, Brian N. Popp10,
John Rooney11,†, Celia M. Smith12 , Daniel Wagner8and Heather L. Spalding12
1Natural Sciences, Bernice Pauahi Bishop Museum, Honolulu, HI, United States
2Pacific Islands Fisheries Science Center, National Oceanographic and Atmospheric Administration, Honolulu,
HI, United States
3Hawai‘i Pacific University, Honolulu, HI, United States
4Hawai‘i Institute of Marine Biology, University of Hawai‘i at Manoa, Honolulu, HI, United States
5Life and Environmental Sciences, University of California at Merced, Merced, CA, United States
6Department of Oceanography, University of Hawai‘i at Manoa, Honolulu, HI, United States
7Environmental and Natural Resource Sciences, Washington State University, Pullman, WA, United States
8Papah¯
anaumoku¯
akea Marine National Monument, National Oceanic and Atmospheric Administration,
Honolulu, HI, United States
9Pacific Islands Fish and Wildlife Office, U.S. Fish and Wildlife Service, Honolulu, HI, United States
10 Department of Geology and Geophysics, University of Hawai‘i at Manoa, Honolulu, HI, United States
11 Joint Institute for Marine and Atmospheric Research, University of Hawai‘i at Manoa, Honolulu, HI,
United States
12 Department of Botany, University of Hawai‘i at Manoa, Honolulu, HI, United States
†Deceased.
ABSTRACT
Although the existence of coral-reef habitats at depths to 165 m in tropical regions
has been known for decades, the richness, diversity, and ecological importance of
mesophotic coral ecosystems (MCEs) has only recently become widely acknowledged.
During an interdisciplinary effort spanning more than two decades, we characterized
the most expansive MCEs ever recorded, with vast macroalgal communities and
areas of 100% coral cover between depths of 50–90 m extending for tens of km2in
the Hawaiian Archipelago. We used a variety of sensors and techniques to establish
geophysical characteristics. Biodiversity patterns were established from visual and video
observations and collected specimens obtained from submersible, remotely operated
vehicles and mixed-gas SCUBA and rebreather dives. Population dynamics based
on age, growth and fecundity estimates of selected fish species were obtained from
laser-videogrammetry, specimens, and otolith preparations. Trophic dynamics were
determined using carbon and nitrogen stable isotopic analyses on more than 750 reef
fishes. MCEs are associated with clear water and suitable substrate. In comparison
to shallow reefs in the Hawaiian Archipelago, inhabitants of MCEs have lower total
diversity, harbor new and unique species, and have higher rates of endemism in
fishes. Fish species present in shallow and mesophotic depths have similar population
and trophic (except benthic invertivores) structures and high genetic connectivity
with lower fecundity at mesophotic depths. MCEs in Hawai‘i are widespread but
associated with specific geophysical characteristics. High genetic, ecological and trophic
How to cite this article Pyle et al. (2016), A comprehensive investigation of mesophotic coral ecosystems in the Hawaiian Archipelago.
PeerJ 4:e2475; DOI 10.7717/peerj.2475
connectivity establish the potential for MCEs to serve as refugia for some species,
but our results question the premise that MCEs are more resilient than shallow reefs.
We found that endemism within MCEs increases with depth, and our results do not
support suggestions of a global faunal break at 60 m. Our findings enhance the scientific
foundations for conservation and management of MCEs, and provide a template for
future interdisciplinary research on MCEs worldwide.
Subjects Aquaculture, Fisheries and Fish Science, Biodiversity, Conservation Biology, Ecology,
Marine Biology
Keywords Mesophotic coral ecosystems, Hawaiian Archipelago, Endemism, Refugia, Closed-
circuit rebreathers, Amino acid isotopic composition
INTRODUCTION
Tropical coral reefs are compelling subjects for a wide range of scientific investigations
because they provide an optimal combination of high diversity, extensive existing
data, robust information infrastructure, large potential for the discovery of new
taxa, and opportunities to gain new insights into fundamental ecological dynamics
(Reaka-Kudla, 1997). They are also among the most severely threatened ecosystems on Earth
(Pandolfi et al., 2003;Knowlton et al., 2010). It has become increasingly evident in recent
years that anthropogenic impacts, such as overharvesting, pollution, coastal development,
invasive species, ocean acidification, and global climate change, imperil the health of
coral-reef ecosystems worldwide (Bruno & Selig, 2007;Burke et al., 2011). Although the
vast majority of known hermatypic coral reefs occur at depths of less than 40 m, there is
longstanding evidence for photosynthetic corals and associated reef communities at greater
depths. Zooxanthellate hermatypic corals have been found at 98 m in the tropical Atlantic
(Hartman, 1973;Fricke & Meischne, 1985;Reed, 1985), below 100 m in the Caribbean
(Locker et al., 2010;Bongaerts et al., 2015;Garcia-Sais et al., 2014;Smith et al., 2014),
112 m at Enewetak (Colin et al., 1986), 125 m on the Great Barrier Reef (Englebert et
al., 2014), 145 m in the Red Sea (Fricke & Schuhmacher, 1983), 153 m in Hawai‘i, and 165
m at Johnston Atoll (Strasburg, Jones & Iversen, 1968;Maragos & Jokiel, 1985;Kahng &
Maragos, 2006). Hopley (1991) reported 100% coral cover at 70 m on the Great Barrier
Reef, and Jarrett et al. (2005) reported up to 60% coral cover at 60–75 m at Pulley Ridge
in the Gulf of Mexico. Photosynthetic algae have been observed at similar or deeper
depths (Porter, 1973;Littler et al., 1985;Colin et al., 1986;Hills-Colinvaux, 1986), and fish
species at such depths belong almost exclusively to families typical of shallower coral-
reef environments (Pyle, 1996b;Pyle, 1999a). Despite these scattered reports, coral-reef
environments at depths greater than 30 m are poorly characterized, largely because of the
logistical difficulties associated with accessing such depths (Pyle, 1996c;Pyle, 1998;Pyle,
1999b;Pyle, 2000;Parrish & Pyle, 2001). There are potentially thousands of species that have
yet to be discovered and scientifically described from deeper coral reef habitats (Pyle, 1996d;
Pyle, 2000;Rowley, 2014) and the basic ecology and population dynamics of these commu-
nities, as well as their connectivity with shallow reefs, are just beginning to be explored.
Pyle et al. (2016), PeerJ , DOI 10.7717/peerj.2475 2/45
Most coral-reef monitoring programs are designed to target shallow reefs
(Jokiel et al., 2001;Brown et al., 2004;Preskitt, Vroom & Smith, 2004;Kenyon et al., 2006).
In recent years, there has been a greater effort to document coral-reef ecosystems at
depths of 30 to over 150 m, now referred to as ‘‘Mesophotic Coral Ecosystems’’ (MCEs)
(Hinderstein et al., 2010;Baker, Puglise & Harris, 2016). These research efforts have primar-
ily focused on aspects of MCEs that are relevant to management policies, such as their dis-
tribution, ecology and biodiversity, as MCEs have been identified as a conservation priority
(Blyth-Skyrme et al., 2013;Sadovy de Mitcheson et al., 2013). However, despite the growing
body of research targeting MCEs, they are often not included in reef assessment and
monitoring programs, management-related reports on the status and health of coral reefs
(Brainard et al., 2003), or general overviews of coral-reef science (Trenhaile, 1997). Most
studies of coral-reef development (and the models derived from them) (Dollar, 1982;
Grigg, 1998;Braithwaite et al., 2000;Rooney et al., 2004) and coral-reef ecology (Luckhurst
& Luckhurst, 1978;Friedlander & Parrish, 1998;Friedlander & DeMartini, 2002;Friedlander
et al., 2003) do not include MCEs. Indeed, most of our understanding of coral-reef
ecosystems is biased by the preponderance of data from depths less than 30 m, which
represents less than one-fifth of the total depth range of the tropical coral-reef environment
(Pyle, 1996b;Pyle, 1999a). An understanding of MCEs is essential to successfully characterize
the health of coral reefs in general, and to formulate effective management plans in the face
of increasing anthropogenic stress.
Coral-reef environments within the Hawaiian Archipelago have been extensively studied
and documented for decades (Maragos, 1977;Chave & Malahoff, 1998;Hoover, 1998;
Mundy, 2005;Randall, 2007;Fletcher et al., 2008;Grigg et al., 2008;Jokiel, 2008;Rooney
et al., 2008;Toonen et al., 2011;Selkoe et al., 2016). These islands and reefs stretch over
2,500 km across the north-central tropical Pacific Ocean, and consist of the eight Main
Hawaiian Islands (MHI) in the southeast, and a linear array of uninhabited rocky islets,
atolls, reefs, and seamounts comprising the Northwestern Hawaiian Islands (NWHI)
(Fig. 1). Many Hawaiian reefs are protected by local, state and federal laws, with a wide
range of management and conservation efforts already in place. In particular, the NWHI
fall within the Papah¯
anaumoku¯
akea Marine National Monument, a federally protected area
larger than all U.S. National Parks combined (>360,000 km2), which is listed as a World
Heritage site and includes about 10% of coral-reef habitats within U.S. territorial waters
(Rohmann et al., 2005).
The first investigations of MCEs within the Hawaiian Archipelago were conducted in the
1960s with SCUBA (Grigg, 1965) and submersibles (Brock & Chamberlain, 1968;Strasburg,
Jones & Iversen, 1968). These early investigations found an unexpected abundance of
reef-associated species (including hermatypic corals) at depths from 25 to 180 m. These
studies also revealed that many species of fishes previously believed to be restricted to
shallow water inhabit much greater depths than expected. In the decades that followed,
a smattering of publications reported on MCEs within the Hawaiian Archipelago
(Grigg, 1976;Agegian & Abbott, 1985;Maragos & Jokiel, 1985;Moffitt, Parrish & Polovina,
1989;Chave & Mundy, 1994;Parrish & Polovina, 1994;Pyle & Chave, 1994), but most of
these involved either a few individual species or habitats, or focused on a broader depth range
Pyle et al. (2016), PeerJ , DOI 10.7717/peerj.2475 3/45
Figure 1 Map of the Hawaiian Archipelago. Source Imagery: Landsat.
(with MCEs representing only a small portion of the study). Beginning in the late 1980s,
the advent of ‘‘technical’’ mixed-gas diving opened up new opportunities for exploration
of MCEs in Hawai‘i and elsewhere (Pyle, 1996a;Pyle, 1999b;Pyle, 2000;Grigg et al., 2002;
Parrish & Pyle, 2002;Pence & Pyle, 2002;Parrish & Boland, 2004;Boland & Parrish, 2005;
Grigg, 2006). In 2006, the discovery of extensive MCEs with near-100% coral cover off Maui,
coupled with interest in documenting MCEs in the NWHI and a growing infrastructure sup-
porting mixed-gas diving operations among Hawaiian research institutions, led to a surge
of research in these deep-reef environments and a series of collaborative, multi-disciplinary
projects dedicated to improving the understanding of MCEs. These projects include
(1) the Deep Coral Reef Ecosystem Studies (Deep-CRES) program focused on the MCEs
of the ‘Au‘au Channel off Maui and their relationship to shallower reefs funded by the
National Oceanic and Atmospheric Administration’s (NOAA) Center for Sponsored Coastal
Ocean Research, (2) two separate studies funded by NOAA’s Coral Reef Conservation
Program to study MCEs off Kaua‘i and O‘ahu, and (3) ongoing annual research cruises
sponsored by NOAA’s Office of National Marine Sanctuaries to study MCEs within the
Papah¯
anaumoku¯
akea Marine National Monument. These projects, as well as many other
smaller surveys over the past two decades, have provided an opportunity for a coordinated
effort to explore and document MCEs across the Hawaiian Archipelago.
The overarching goal of these activities was to establish a baseline understanding of
MCEs in Hawai‘i at depths ranging from 30 to over 150 m, and to provide insights into
the structure, composition, ecological dynamics, and management needs of MCEs in
general. The primary research activities were driven by a series of hypotheses designed
to reveal fundamental characteristics of Hawaiian MCEs and how they compare with
both shallow reef habitats and non-MCE habitats at comparable depths. The questions
Pyle et al. (2016), PeerJ , DOI 10.7717/peerj.2475 4/45
behind these hypotheses involved characterizations in four general categories: (1) basic
geophysical habitat (water clarity, temperature, photosynthetically active radiation
[PAR], water movement, nutrient levels, and substrate type), (2) patterns of biodiversity
(species composition, relative abundance, and overlap, as well as patterns of endemism),
(3) population structure and dynamics (growth rates, impact from anthropogenic and
natural disturbance, connectivity, disease levels, age structure, fecundity and production),
and (4) broad ecological patterns (trophic dynamics and genetic connectivity). In addition,
data from these studies were used extensively to develop a spatial model based on physical
parameters and other factors to predict the occurrence of MCEs in Hawai‘i and globally
(Costa et al., 2015). Ultimately, our hope is that the insights gained from this research, such
as the predicted distribution and abundance of MCEs, the richness and uniqueness of the
biodiversity they harbor, and the potential for MCEs to serve as refugia for overexploited
biological resources on shallow reefs, will help guide future policy decisions in the
conservation and management of marine resources in Hawai‘i and elsewhere.
MATERIALS AND METHODS
As this synthesis represents a broad summary of MCEs in Hawai‘i, based on the results of a
multi-year interdisciplinary collaborative effort by many individuals, the methods involved
are extensive and diverse. The following represents a summary of methods used throughout
this study, particularly as they pertain to data not previously published elsewhere. More
detailed descriptions of methods used during this study, including aspects that have
been previously published, are included in Supplemental Information 1, and within cited
publications. The State of Hawai‘i Department of Land and Natural Resources developed
Special Activity Permits for the University of Hawai‘i and National Marine Fisheries Service
for work related to this project that occurred within State of Hawai‘i waters. All sampling
procedures and experimental manipulations were reviewed as part of obtaining the field
permit. All vertebrates (fishes) were collected in accordance with University of Hawai‘i
IACUC protocol 09-753-5, ‘‘Phylogeography and Evolution of Reef Fishes’’ (PI: Dr. Brian
Bowen), including collection and euthanization by spear.
Study sites
We examined MCEs at multiple sites throughout the Hawaiian Archipelago. The primary
MHI study sites were in the ‘Au‘au Channel off Maui, southeast Kaua‘i, and the southern
shore of O‘ahu (Fig. 2). Additional qualitative observations of MCEs around the islands
of O‘ahu, Kaua‘i, Maui, and Hawai‘i provide complementary insights into general
characteristics of MCEs in the MHI. Surveys of MCEs in the NWHI included visits to
ten islands and reefs labelled in Fig. 1.
Survey effort
Data from MCEs were gathered from mixed-gas rebreather dives, submersible dives,
Remotely Operated Vehicle (ROV) dives, and Towed Optical Assessment Device
(TOAD camera sled) transects. The submersible and ROV dives were conducted using
the Hawai‘i Undersea Research Laboratory’s (HURL) Pisces IV and Pisces V submersibles,
Pyle et al. (2016), PeerJ , DOI 10.7717/peerj.2475 5/45
Figure 2 Location of study areas. Inset shows remote camera survey (TOAD) track locations, and sites
for ‘‘John,’’ ‘‘Frank,’’ and ‘‘Tele 1’’ and ‘‘Tele 2’’ data moorings. MHI imagery from Landsat, USGS.
and the RCV-150 ROV. On several occasions, both submersibles and rebreather divers
conducted simultaneous, coordinated field operations (Fig. 3). Mixed-gas dives in the
NWHI were conducted from the NOAA Ship Hi‘ialakai. Dive sites in the MHI were
determined by a variety of factors, including previously known MCE habitat, bathymetry
data, and direct site identification by submersible, ROV and TOAD; whereas dive sites in
the NWHI targeted steep vertical drop-offs at depths of 50–85 m located using historical
charts and new multibeam sonar data collected with the Hi‘ialakai.
Geophysical habitat characterization
The majority of geophysical habitat characterization focused on the ‘Au‘au Channel site
(Fig. 2, inset). Existing moderate-resolution (20-m grid) bathymetry was supplemented
with multibeam surveys at a resolution of 5 m in a few areas. Video transects from
submersible, ROV and TOAD dives were used to document the spatial distribution
of corals and macroalgal communities across >140 linear km of habitat (Fig. 2). Two
specific areas were selected for detailed physical oceanographic characterization using four
oceanographic moorings with temperature and pressure loggers, current meter, and current
profiler. Additional temperature data were recorded at four sites between Maui and Kaua‘i
(Table 1). Underwater irradiance was measured by lowering a calibrated spherical (4π)
quantum sensor (Underwater LI-193SA, LI-COR, Lincoln, NE, USA) through the water
Pyle et al. (2016), PeerJ , DOI 10.7717/peerj.2475 6/45
Figure 3 Research divers place a dome over a set of corals 89 m deep. Research divers Ken Longenecker
(left), Dave Pence (center) and Christina Bradley (right) place a dome over a set of corals 89 m deep as
part of an experiment to determine coral feeding patterns, while pilot Terry Kerby and science observers
Brian Popp and Andrea Grottoli watch on from the HURL submersible Pisces V. Photo: RL Pyle.
Table 1 List of all temperature sensors deployed across Maui and Kaua‘i.
Location Latitude Longitude Depth (m) Deployment
Makaheuna Point, Kaua‘i 21◦51.388N 159◦26.003W 46 13 June 2009 to 12 July 2010
Makaheuna Point, Kaua‘i 21◦51.388N 159◦26.003W 63 13 June 2009 to 12 July 2010
Kipu Kai, Kaua‘i 21◦52.460N 159◦23.028W 57 17 June 2009 to 13 July 2010
Keyhole Pinnacle, Maui 20◦56.437N 156◦45.619W 70 6 April 2009 to 17 January 2010
Keyhole Pinnacle, Maui 20◦56.452N 156◦45.652W 88 6 April 2009 to 17 January 2010
Keyhole Pinnacle, Maui 20◦56.452N 156◦45.652W 102 6 April 2009 to 17 January 2010
Keyhole Pinnacle, Maui 20◦56.454N 156◦45.661W 116 6 April 2009 to 17 January 2010
Keyhole Pinnacle, Maui 20◦56.478N 156◦45.666W 134 6 April 2009 to 17 January 2010
Keyhole Pinnacle, Maui 20◦56.478N 156◦45.666W 160 6 April 2009 to 17 January 2010
Branching Coral Reef, Maui 20◦49.300N 156◦40.377W 58 14 December 2009 to 14 December 2010
Stone Walls, Maui 20◦52.890N 156◦43.794W 34 17 December 2009 to 13 December 2010
Stone Walls, Maui 20◦52.890N 156◦43.794W 34 17 December 2009 to 13 December 2010
Stone Walls, Maui 20◦52.890N 156◦43.794W 42 17 December 2009 to 13 December 2010
Stone Walls, Maui 20◦52.890N 156◦43.794W 46 17 December 2009 to 13 December 2010
Stone Walls, Maui 20◦52.890N 156◦43.794W 49 17 December 2009 to 13 December 2010
Stone Walls, Maui 20◦52.890N 156◦43.794W 58 17 December 2009 to 13 December 2010
Pyle et al. (2016), PeerJ , DOI 10.7717/peerj.2475 7/45
Figure 4 Collecting samples using the Pisces submersible manipulator arm. Photo: HURL.
via a profiling rig (n=6 profiles taken within one hour of noon on 4, 5, and 6 August 2008
and 12, 13, and 14 July 2010 over dense Leptoseris spp. reefs at a maximum depth of 91 m
off west Maui); data were stored with a LI-COR LI-1400 datalogger.
Biodiversity patterns
The biodiversity surveys focused primarily on macroalgae, fishes, marine invertebrates, and
corals. Surveys were conducted using a variety of visual, video, and collecting techniques.
Direct visual observations were made by trained individuals during mixed-gas SCUBA
dives and from submersibles. Videotapes were generated by divers, submersibles, ROV, and
TOAD camera system. Specimens were collected by divers and the manipulator arm of the
Pisces submersibles (Fig. 4). Qualitative collections and observations were made to determine
species presence, and quantitative transects were made to measure the distribution and
abundance of species. Depth ranges for algae and fishes known to occur at depths of less than
200 m were determined from quantitative and qualitative surveys, and available published
information. All specimens were photo-documented using high-resolution digital cameras,
and voucher specimens were deposited in the Bishop Museum Natural Sciences collections.
Population dynamics
Colonies of Leptoseris were stained in situ using Alizarin Red for subsequent harvesting
to determine growth rates (Fig. 5). Additional test colonies of Leptoseris were sent to
Pyle et al. (2016), PeerJ , DOI 10.7717/peerj.2475 8/45
Figure 5 Colony of Leptoseris sp. being stained with Alizarin Red for growth rate studies. Photo:
HURL.
collaborators at the Woods Hole Oceanographic Institution for computerized axial
tomography (CT) scanning, 14C and U/Th (Uranium–thorium) dating and elemental
ratio analyses to determine growth rates. Three fish species exploited on shallow reefs
and reported from MCEs, Centropyge potteri (Jordan & Metz 1912), Ctenochaetus strigosus
(Bennett 1828), and Parupeneus multifasciatus (Quoy & Gaimard 1825), were selected to
compare with existing estimates of production and reproductive output in shallow habitats.
We collected specimens to describe length-weight and length-fecundity relationships,
growth, and size-specific sex ratios; and to estimate size-at-maturity for mesophotic
populations. Laser-videogrammetry surveys (Fig. 6) were used to estimate densities and size
structure of target species encountered during the belt transects, based on a high-definition
video camera fitted with parallel laser pointers. We then reviewed the video and captured
still frames when an individual was oriented perpendicular to the laser beam axes and
both lasers appeared on the fish. Because the beams are parallel, the lasers superimpose a
reference scale on the side of the fish, allowing length estimates by solving for equivalent
ratios. Results of life-history analysis and laser-videogrammetry surveys were incorporated
into a modified Ricker production model to estimate annual biomass production and
reproductive output for mesophotic populations.
Pyle et al. (2016), PeerJ , DOI 10.7717/peerj.2475 9/45
Figure 6 Ross Langston demonstrating the videogrammetry technique for estimating fish sizes. A
video camera fitted with parallel lasers (A); superimposes a measurement scale on target fish (B–D). Pho-
tos: H Bolick, K Longenecker and R Langston.
Broad trophic characterizations
To determine the trophic level of key food web components and functional groups, we
conducted stomach content and carbon and nitrogen stable isotopic analyses of reef fishes
from 45 species, 30 genera and 18 families (Bradley et al., in press). Further isotope analysis
was performed on 24 selected species from seven families without stomach content analysis
(Papastamatiou et al., 2015). We also used compound-specific isotope analysis of amino
acids to estimate trophic positions of fishes (McClelland & Montoya, 2002;McClelland, Holl
& Montoya, 2003;Pakhomov et al., 2004;McCarthy et al., 2007;Popp et al., 2007;Hannides
et al., 2009;Hannides et al., 2013) using the difference in δ15N values of trophic and
source amino acids for trophic position calculation (Chikaraishi et al., 2009;Bradley et al.,
2015). Additional isotopic analyses were performed on Galapagos sharks [Carcharhinus
galapagensis (Snodgrass & Heller 1905)] and giant trevally [Caranx ignobilis (Forsskål
1775)] in the NWHI (Papastamatiou et al., 2015).
RESULTS AND DISCUSSION
Our intention in this work is to provide a broad characterization of MCEs across the
Hawaiian Archipelago based on more than two decades of interdisciplinary and collaborative
research, with emphasis on a seven-year effort to document MCEs in Hawaii largely funded
Pyle et al. (2016), PeerJ , DOI 10.7717/peerj.2475 10/45
Figure 7 Generalized diagram of major components of MCEs in the ‘Au‘au Channel, Hawaiian Is-
lands. Illustration by RL Pyle.
by NOAA. Some portions of this overall research have already been published elsewhere,
and others are presented for the first time herein. For purposes of clarity and cohesiveness,
we present both novel and previously published information together. When information
has previously been published, we provide appropriate literature citations, and when
information is presented for the first time, we indicate it as such.
Our investigations revealed that MCEs throughout the Hawaiian Archipelago can be
broadly categorized into several distinct habitat types (Fig. 7). The shallowest portions
of MCEs (30–50 m) are characterized by a few of the coral species found on shallow
Hawaiian reefs, in particular Montipora capitata Dana 1846, Pocillopora meandrina Dana
1846, Pocillopora damicornis (Linnaeus 1758) and Porites lobata Dana 1846. At depths of
∼40–75 m, expanses of low relief ‘‘carpets’’ of branching M. capitata are found overlying
sediment fields, switching to a plate-like or laminar morphology on ledges and rocky
slopes (Rooney et al., 2010). All MCE depths had large Halimeda spp. meadows and other
dominant macroalgal communities over both hard and soft substrates. Although these
macroalgal communities generally did not comprise major habitats for large-bodied
fishes in the MHI (either in MCE depths, or in shallower areas), endemic reef-associated
fishes were found in macroalgal (Microdicyton spp.) beds at MCE depths in the NWHI
(Kane, Kosaki & Wagner, 2014). Throughout the archipelago, undercut limestone
ledges with small caves and other features (the remnants of ancient shorelines)
(Fletcher & Sherman, 1995) represent the dominant MCE habitat type at depths of
50–60 m, 80–90 m, and 110–120 m. In certain areas, particularly the ‘Au‘au Channel
off Maui and off southeastern Kaua‘i, near-100% Leptoseris coral cover extends for tens of
km2at 70–90 m. This habitat type, one of the primary subjects of our investigations,
Pyle et al. (2016), PeerJ , DOI 10.7717/peerj.2475 11/45
represents the most spatially extensive MCE environment documented to date
(Costa et al., 2015).
These MCE habitats are often not in close proximity to each other, but separated by vast
areas of sand lacking any rocky reef structure. Some of these sandy areas are characterized by
meadows of Halimeda kanaloana (Maui), Avrainvillea sp. and/or Udotea sp. (west and south
O‘ahu), while others are devoid of organisms associated with coral-reef ecosystems (i.e.,
non-MCE habitat within MCE depth ranges). Another MCE habitat within the Hawaiian
Archipelago that was not a primary subject of investigation for this work, but for which
we have extensive qualitative observations, are the steep slopes and drop-offs characteristic
of the island of Hawai‘i (i.e., the ‘‘Big Island’’), especially at the southeastern end of the
archipelago. This habitat is dominated by basaltic rock (rather than the coral and limestone,
which dominate MCE habitat throughout the rest of the archipelago). Finally, one MCE
habitat notably absent from the Hawaiian Archipelago, but prevalent throughout most
of the tropical Indo-Pacific, is steep limestone drop-offs, which often extend more or less
continuously from shallow-reef depths down to MCE depths and beyond.
In the sections that follow, we highlight and summarize the most salient aspects of MCEs
throughout the Hawaiian Archipelago. In particular, we compare and contrast patterns
across different MCE habitats, different parts of the archipelago, and among different taxa,
as well as emphasize both commonalities and differences among these patterns.
Geophysical habitat characterization
General habitat characterization
MCE habitats in different parts of the archipelago were characterized by contrasting
geophysical structures and bathymetric profiles. The general bathymetry of MCEs
throughout most of the archipelago (except the island of Hawai‘i, which was not a
primary study site) is characterized primarily by gradually sloping flat substrate with
occasional rocky outcrops of both volcanic and carbonate material. In most areas, the
gradually sloping bottom was interrupted by bathymetric discontinuities at approximately
50–60 m, 80–90 m, and 110–120 m depths (the 80–90 m discontinuity is buried in sand
throughout most of the NWHI, except for a small exposed area near Pearl and Hermes
Atoll). These discontinuities were typically continuous, rocky undercut limestone ledges
or steep sandy or limestone slopes parallel to shore. In some locations, such as within the
‘Au‘au Channel, these discontinuities were the result of karstification (Fig. 2). MCE habitats
identified within flat-bottom areas (i.e., between discontinuities) included macroalgal
meadows, macroalgal beds, and (especially in the 40–75 m range) expansive low relief
beds of interlocking branching colonies, or laminar tiers of Montipora spp. Gradually
sloping, flat-bottom areas were also commonly surfaced by sand, gravel, rhodoliths and
pavement, with very little coral cover. Corals were more common on exposed rock surfaces
along rock ledges and outcrops. In contrast to most sites in the Hawaiian Archipelago, the
80–90 m discontinuity within the ‘Au‘au Channel included very few exposed rocky areas
at MCE depths, except along very steep walls and in a few areas otherwise dominated by
Leptoseris spp.
Pyle et al. (2016), PeerJ , DOI 10.7717/peerj.2475 12/45
Figure 8 Temperature data from ‘‘John’’ and ‘‘Frank’’ moorings. Temperature data from ‘‘John’’ and ‘‘Frank’’ moorings, comparing seasonal and
daily fluctuations in water temperature at each of eight different depths off the ‘Au‘au Channel from August 2008 to July 2009. Graphs represent
the average daily temperature (A) and the daily standard deviation (SD) (B) at each depth. The thin black line below each depth trace in (B) repre-
sents SD =0, and the thin black line above represents SD =1; the greater the distance of the color line from the black line below (SD =0), the more
dynamic the daily temperature. SD is based on n=72 temperature values/day for data recorded at 84 and 123 m, and n=36 for other depths.
Geophysical factors
One of the most important geophysical characteristics of MCEs in Hawai‘i is water clarity.
Within the ‘Au‘au Channel, MCEs were found to occur in areas offshore with very clear
water, with a diffuse attenuation coefficient (Ko) of 0.041 ±0.001 m−1. In comparison,
nearby areas inshore of west Maui had higher attenuation coefficients (and thus more turbid
water), ranging from 0.107 m−1at 10 m depth to 0.073 m−1at 30 m depth (Spalding, 2012).
The average percent surface irradiance (SI) and irradiance values (PAR) at depth were 10%
SI at 34 m (245 ±15 SE µE m−2s−1), 1% SI at 90 m (25 ±3 SE µE m−2s−1), and 0.1%
at 147 m (2.5 ±0.4 SE µE m−2s−1). The 1% SI is often referred to as the compensation
point, where photosynthesis equals respiration; above this point, there is net photosynthesis
and production of organic matter; below this point, there is net consumption of organic
material, and respiration exceeds photosynthesis (Kirk, 2011). In general, areas with the
clearest water also supported the richest and most expansive MCEs.
Water temperatures in the Au‘au Channel from August 2008 through July 2009 ranged
from just below 21 ◦C to just over 26.5 ◦C throughout the water column over the time
period sampled. A seasonal temperature cycle was apparent throughout the water column,
with warmest temperatures from September to November, and coolest from February
to May. The temperature was consistently 2–3 ◦C cooler at the deep end of the sampled
depth range (Fig. 8A), with less short-term variability and less seasonal fluctuation. Water
temperatures were logged within three depth ranges: shallow (53 and 64 m), middle
(73, 84, and 93 m), and deep (102, 112, and 123 m). Water temperatures at the deepest
depths were the most stable on a daily basis, whereas temperatures at the middle depths
were the most dynamic. The shallowest depths were intermediate in terms of daily thermal
stability (Fig. 8B). Relatively large (1–2 ◦C) short-term (1 day) temperature excursions
Pyle et al. (2016), PeerJ , DOI 10.7717/peerj.2475 13/45
Figure 9 One-year temperature profile in two MCE habitat types at Kaua‘i and Maui. Branching coral (Montipora; A) habitat was at approxi-
mately 57 m and black coral (Antipathes, B) habitat was at 34 to 62 m.
occurred at 50–75 m, however, temperatures were very consistent on this time scale at the
deep site (Fig. 8B). The most dynamic temperatures for all but the deepest three depths,
corresponded with the warmest months (September to November), and the most thermally
stable months were the coolest (February to May). We were unable to determine whether
MCEs are influenced by tidally-correlated vertical thermocline shifts. The establishment of
moorings at the deep extreme of the MCE range would provide useful comparative data to
test for a tidal effect, versus bathymetric forcing. In March of 2009, the ‘‘Tele 1’’ mooring
slid down slope, causing the temperature sensor to change depth, so data from this mooring
were not included in the analyses. A comparison of temperatures between Maui and Kaua‘i
at 34–62 m showed that both islands had a seasonal trend, but Kaua‘i had a higher daily and
seasonal fluctuation than Maui (Fig. 9).
Acoustic profiler analysis indicated that the current magnitude at 70–90 m where corals
were most abundant fluctuated between 10–15 cm s−1with sporadic, brief pulses >25 cm
s−1, with a clear pulsing (strengthening and weakening) that corresponded with direction
changes on a tidal frequency (Fig. 10). At greater depths, the flow was almost stagnant with
little tidal signal and variable direction. These results are in stark contrast to the higher
magnitude currents (up to more than 40 cm s−1) that occur at shallow depths subject
to daily tidally forced flows (Fig. 10). Although there were clear differences in flow rates
observed at MCE depths, the observed direction of flow was highly variable and difficult to
attribute to tidal or wind driven processes. Greater resolution in sampling would be needed
to determine the relationship between flow direction and reef orientation for MCE habitats.
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Figure 10 Current magnitude profiles. Sontek 250 kHz Acoustic Doppler Profiler profiles of current
magnitude in cm s−1, with overlap shown in the black line between the deeper Frank mooring and shal-
lower John mooring. Broken down by seasons to show detail (A, Autum; B, Winter; C, Spring; D, Sum-
mer).
Biodiversity patterns
Species diversity
Seventy-two species of frondose macroalgae were identified based on morphological
characteristics from MCEs in the MHI, including 29 Chlorophyta, 31 Rhodophyta, and
12 Phaeophyceae. Estimates of macroalgal diversity are likely conservative because of
taxonomic limitations regarding morphological identifications. For instance, large green
algal ‘‘sea lettuce’’ blades from MCEs were all identified morphologically as ‘‘Ulva lactuca.’’
However, recent molecular analyses revealed that these specimens represent four new
species belonging to the genera Ulva and Umbraulva, which cannot be identified using
morphological characters alone (Spalding et al., 2016). Nevertheless, the methods used
were similar to current taxonomic treatments in Hawai‘i (Abbott, 1999;Abbott & Huisman,
2003;Huisman, Abbott & Smith, 2007) allowing for comparisons with the better-known
shallow-water flora. Macroalgal communities were found in discrete patches (separated
by sand or other benthic habitats) at all MCE depths in the MHI. Examples include
expansive meadows of Halimeda kanaloana Vroom in sand, beds of Halimeda distorta
(Yamada) Hillis-Colinvaux over hard substrates, as well as monospecific beds of Distromium
spp., Dictyopteris spp., Microdictyon spp., Caulerpa spp., and mixed assemblages of other
macroalgal species (Spalding, 2012). These MCE macroalgal assemblages are abundant,
diverse, and spatially heterogeneous with complex distributional patterns, contributing
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to heterogeneous structural complexity. In contrast, MCE macroalgal communities in
the NWHI tended to be dominated by beds of Microdictyon spp., although ROV video
around the banks of the NWHI also show regions of Sargassum or Dictyopteris species
(Parrish & Boland, 2004) (collections not yet available for verification).
Of the approximately fifty species of scleractinian corals known from the Hawaiian
Islands (Hoover, 1998), ten were recorded by this study from MCEs in the MHI. Three of
these—Pocillopora damicornis,P. meandrina,Porites lobata, and Montipora capitata—are
common species on adjacent shallow reefs. A previously published phylogeny resolved
six Leptoseris species in Hawai‘i: Leptoseris hawaiiensis Vaughan 1907, L. papyracea (Dana
1846), L. scabra Vaughan 1907, L. tubilifera Vaughan 1907, L. yabei (Pillai & Scheer,
1976), and a putative undescribed species, ‘‘Leptoseris sp. 1’’ (Luck et al., 2013;Pochon
et al., 2015). However, the reliability of coral phylogenies has been challenged due to
limited genetic variation (Sinniger, Reimer & Pawlowski, 2010). In addition to scleractinian
corals, eight antipatharian coral species were documented from MCE depths through work
associated with this study and published previously (Wagner et al., 2010;Wagner et al., 2011;
Wagner, 2015a;Wagner, 2015b).
One of the goals of this research was to identify key parameters that might determine
the presence and distribution of MCE habitats elsewhere in Hawaiian waters through the
development of a spatial model. This portion of our study has been published previously
(Costa et al., 2015), but in summary, depth, distance from shore, euphotic depth and sea
surface temperature were identified as the four most influential predictor variables for
partitioning habitats among the three genera of corals included in the modeling exercise
(Leptoseris,Montipora, and Porites). Costa et al. (2015) found that for corals that occur in
the shallower depth (50 m) of MCEs, hard substrate is necessary, but not sufficient, for
colonization. It is less certain whether hard substrate is necessary at greater depths, where
some of the Leptoseris beds were found in a density of three or more layers of coral plates
deep. Whether this is due to accretion on a hard substrate or a stable soft bottom needs
further examination. Additional details of the methods and results from this portion of
the study are available in Costa et al. (2015). Extensive Leoptoseris-dominated MCEs with
very similar structure, depth and species composition have been identified in two MHI
regions: the ‘Au‘au Channel, and off southeastern Kaua‘i (Fig. 11). Although no other
Leoptoseris-dominated MCEs have yet been located within the Hawaiian Archipelago,
similar MCE habitats may exist elsewhere in the MHI.
In addition to corals, nearly 200 specimens from among eight phyla of marine
invertebrates (Foraminifera, Porifera, Bryozoa, Annelida, Arthropoda, Cnidaria,
Ophiuroidea, and the subphylum Urochordata) were collected from MCEs in the MHI.
Unfortunately, many of these groups are poorly known taxonomically, and nearly three
quarters of these specimens remain unidentified.
Qualitative comparisons of fish assemblages associated with black coral beds are available
for two main islands: Kaua‘i (this study) and Maui (Boland & Parrish, 2005). Both were
similar in species number; the Maui survey recorded 60 species and Kaua‘i had 52 (Table 2).
A Wilcoxon Signed Rank Test showed no significant difference (P=0.100, W= −1.647)
in species abundance. When all fish were categorized by feeding guilds, both had similar
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Figure 11 Comparison of Leptoseris-dominanted MCE habitats. (A) Kaua‘i and (B) Maui, showing the
close similarity in general structure.
Table 2 Comparison of fish assemblages associated with black coral beds of two Main Hawaiian Is-
lands, Kaua‘i and Maui. Feeding guild percentages from number of fish in the feeding guild compared to
total number of fish observed in the island’s black coral bed.
Maui Kaua‘i
Total fish observed 2,080 1,322
Number of species observed 60 52
Herbivore 7% 5%
Planktivore 68% 67%
Omnivore 1% 1%
Benthic Carnivore 23% 26%
Piscivore 1% 1%
distributions. Both were dominated by planktivores with Maui at 68% and Kaua‘i at
67%, with the next largest group being benthic carnivores at 23% and 26%, respectively
(Table 2). By comparison, black coral MCEs of the Mid-Atlantic Ridge host 33% planktivores
and 9% benthic carnivores (Rosa et al., 2016).
Within the ‘Au‘au Channel site, both divers and submersible observers made repeated
anecdotal observations of highly heterogeneous fish diversity and abundance over Leptoseris
beds with similar morphology and abundance. Some areas were almost devoid of fishes
(Fig. 12A), whereas others harbored high levels of both diversity and abundance (Fig. 12B).
No transect data were performed to quantify this preliminary observation, and we can
think of no obvious reason why the pattern might exist. However, we feel this observation
is interesting enough, and was made consistently enough, to justify noting here in the hope
of prompting future research.
Elsewhere in the Pacific, MCEs harbor high numbers of species new to science
(Pyle, 2000;Rowley, 2014). The fish fauna of Hawai‘i has been better documented than
any other location in the tropical insular Pacific, so new species were not expected.
However, at least four undescribed species of fishes have been collected on MCEs in
Hawai‘i, including a highly conspicuous butterflyfish (Prognathodes) and three other
less conspicuous species (Scorpaenopsis,Suezichthys and Tosanoides). These have been
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Figure 12 Heterogeneous reef fish distribution on Leptoseris reefs in the ‘Au‘au Channel. Reef fish
distribution on Leptoseris reefs in the ‘Au‘au Channel was heterogeneous, with large areas nearly devoid of
fishes (A) punctuated with areas of high fish diversity and abundance (B). The fishes seen in the distance
in (A) represent a separate localized area of high abundance. All but two of the fishes visible in (B) belong
to endemic species (Endemics: Chaetodon miliaris, Pseudanthias thompsoni, Sargocentron diadema, Das-
cyllus albisella, Holacanthus arcuatus, Centropyge potteri; Non-endemic: Forcipiger flavissimus, Parupeneus
multifasciatus). Photos: HURL.
determined by experts in the respective taxonomic groups to be undescribed, and are in
various stages of formal description. At least one putative new species of scleractinian coral
(Leptoseris) has been identified (as noted above), and one putative new species and one
new record of Antipatharian corals for the Hawaiian Archipelago have been recorded
(Wagner et al., 2011;Opresko et al., 2012;Wagner, 2015a). Undescribed macroalgae will
require molecular characterizations that will likely increase the number and diversity
of recognized species. Likewise, the taxonomy of many groups of marine invertebrates
is poorly known (see Hurley et al. 2016), and many of the unidentified specimens of
invertebrates may prove to be new species, once subjected to the same taxonomic scrutiny
by appropriate experts that the aforementioned fishes, corals and algae have undergone.
Sponge taxonomists have indicated numerous undescribed species and genera from among
MCE collections. This is likely the case for the other phyla as well, especially within
polychaetes, small crustaceans, and tunicates.
Depth zonation
The preponderance of new species within MCE habitats reinforces the observation that the
species inhabiting deeper MCEs are generally different from those inhabiting shallow reefs.
Overall, diversity was lower on MCEs than on nearby shallow reef habitats. This pattern was
consistent for macroalgae, corals, macroinvertebrates and fishes. However, within MCE
habitats, different taxonomic groups showed different patterns of diversity.
Survey results for macroalgae show more species at 70–100 m compared to 40–60 m,
with the most distinctive changes in diversity (i.e., the most substantial changes in total
number of species at each depth interval) occurring at 80–90 m and 110–120 m depths
(Fig. 13). These depths corresponded to ∼3% and 0.5% of SI, respectively, and included
depths where large changes in seasonal thermoclines were observed. The water column at
most sites was characterized by high clarity and deep penetration of irradiance (10 µmol
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Figure 13 Total number of macroalgal species (over all sites combined) found at each depth surveyed.
Depth of occurrence is based upon collections and visual observations when species level identifications
were verified. Shallower depths (40–60 m) were collected by mixed-gas divers while depths ≥70 m were
collected by submersibles. See Spalding (2012) for collection locations. Data are included in the ‘‘Algae-
Data’’ (Supplemental Information 2; Tab 1) worksheet of the Raw Data file.
m−2s−1at 110 m depths), although sedimentation from terrigenous sources appeared to
reduce macroalgal abundance at a few sites.
A similar pattern may exist for scleractinian corals. Three species of corals were found
at 30–50 m (M. capitata,P. damicornis and P. lobata). P. damicornis and P. lobata were
only seen at the shallowest MCEs (<50 m), while M.capitata occurred at greater depths
(50–80 m) (Rooney et al., 2010). At these greater depths, M. capitata was most commonly
observed in a branching morphology that formed low-relief reefs carpeting tens of km2
of sea-floor off the west coast of Maui. Similar reefs have been observed off Kaua‘i and
Ni‘ihau, although a plate-like morphology is dominant around O‘ahu. At greater depths,
the dominant corals are within the genus Leptoseris. Starting at a depth of ∼65 m, Leptoseris
corals were most commonly encountered, becoming the dominant corals at depths below
∼75 m, and continuing in high abundance down to 130 m, with solitary colonies at
depths in excess of 150 m (Rooney et al., 2010). Of these, recent evidence indicates that
L. hawaiiensis was found exclusively at depths below 115–125 m (Pochon et al., 2015). The
latter study also investigated endosymbiotic dinoflagellate Symbiodinium and resolved three
unambiguous haplotypes in clade C, with one haplotype exclusively found at the lower
MCE depth extremes (95–125 m) (Pochon et al., 2015). These patterns of host–symbiont
depth specialization indicate limited connectivity between shallower and deeper portions
of MCEs, and suggest that niche specialization plays a critical role in the host–symbiont
evolution of corals at MCE depth extremes.
Invertebrate identifications completed thus far indicate that many species from various
phyla are deep-water specialists, such as the polychaete Eunice nicidioformis (Treadwell
1906), which was originally described from a specimen collected at 200–300 m in the
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Hawaiian Islands. Hurley et al. (2016) observed strong zonation of brachyuran crab species
by depth off O‘ahu, and this trend is likely to extend to all invertebrate phyla. Remarkably
few amphipods were found, and most were parasitic or inquiline species (Longenecker &
Bolick, 2007); possibly an artifact of sampling with submersibles (i.e., free-living species
may have been swept off during ascent).
The pattern of depth stratification was much less apparent among fishes. Depth ranges
of all reef-associated fish species known to occur at depths of less than 200 m (n=445)
were obtained through this study and from historical literature, and are included in the
‘‘FishData’’ (Supplemental Information 2; Tab 2) worksheet of the Raw Data file. Among
species recorded at depths greater than 30 m (n=346), 87% (n=302) also occur at shallower
depths (i.e., only 12% (n=44) of fishes recorded from MCEs are restricted to MCEs). In
the Northwestern Hawaiian Islands, Fukunaga et al. (2016) found that fish assemblages at
mesophotic depths (27–67 m) had higher densities of planktivores and lower densities of
herbivores than on comparable shallow reef-fish assemblages between 1 and 27 m. It has been
suggested that there may be a consistent and relatively sharp faunal break at around 60 m
(Slattery & Lesser, 2012). An analysis of beta-diversity among fishes in the Red Sea found that
the rate of species turnover increased with depth (Brokovich et al., 2008); however, this study
only extended to 65 m, the shallowest portion of MCEs. Moreover, traditional approaches
to quantifying beta-diversity changeover are designed to measure presence/absence data
for multiple discrete zones, and would require multiple replicate transects at multiple
depth zones across many different habitats and geographic locations (i.e., potentially
thousands of transects) to adequately characterize species transition patterns. Instead,
the question of where the largest and most substantial species assemblage transitions
occur can be addressed by a more holistic approach to known species depth ranges
(see Supplemental Information 1). Figure 14A, which summarizes data included in
the ‘‘FishData’’ (Supplemental Information 2; Tab 2) worksheet of the Raw Data file,
reveals that the most substantial faunal transitions in fishes occur in the range of 10–30
m and 110–140 m, and the least substantial transitions occur in the range of 40–60
m, with moderate transitions in the range of 70–100 m. The most substantial floral
transitions (from data included in the ‘‘AlgaeData’’ (Supplemental Information 2; Tab
1) worksheet of the Raw Data file) occur between 90–110 m and at 130 m depths
(Fig. 14B), indicating that 60 m is not a significant transition for species changeover
in macroalgae. Brachyuran crabs show the strongest transitions between 60 and 90 m
(Hurley et al., 2016). The diversity of coral species is insufficient to allow the application
of this type of analysis; however, applying this method to other taxa and in other regions
should provide insight into whether floral and faunal breaks are consistent on a broader
taxonomic and geographic scale.
Endemism
Our findings support previous reports of higher rates of endemism (species that occur only
within the Hawaiian Islands) among fishes on MCEs (Pyle, 1996b;Pyle, 2000;Kane, Kosaki
& Wagner, 2014). Among 259 species of fishes recorded on MCEs across the Hawaiian
Archipelago, 70 (27%) are endemic (inclusive of Johnston Atoll), considerably higher than
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Figure 14 Fish and macroalgal species changeover at 10-m depth intervals. The degree of fish (n=445) changeover (A) and macroalgal (n=
72) species changeover (B) at 10-m depth intervals. Values of each bar represent the number of species with a maximum known depth limit within
10 m above each depth interval plus the number of species with a minimum known depth limit within 10 m below each interval, expressed as a per-
centage of the total species present at the interval. A high value indicates a more substantial break, and a low value represents a less substantial break.
Data are included in the ‘‘AlgaeData’’ ((Supplemental Information 2; Tab 1)) and ‘‘FishData’’ (Supplemental Information 2; Tab 2) worksheets of
the Raw Data file.
the 20.5% of endemic fishes across all reef and shore fishes reported for the Hawaiian
Archipelago (Randall, 1998). However, with more careful analysis, the trend of increasing
endemism with increasing depth within MCEs is even stronger.
Based on our surveys, the rate of endemism among reef fishes found exclusively
shallower than 30 m (n=126) was 17%, and the rate of endemism among reef fishes
found exclusively deeper than 30 m (n=42) is 43%. The rate of endemism remained
roughly the same (16–17%) for fishes found only shallower than 40 to 80 m depths (in
10-m depth increments), but changed to 44% for fishes found only deeper than 40 m,
41% below 50 m, 50% below 60 m, and 51% for fishes found only deeper than 70 m. This
trend appears to be restricted to fishes inhabiting MCEs (rather than a general trend of
increasing endemism with increasing depth), because among fishes restricted to depths
greater than 150 m, the rate of endemism is 14% (Mundy, 2005). The proportion of
endemic fish species increases even further with increasing latitude across the Archipelago.
At the northwestern-most atolls, endemism among MCE fishes reaches 76% (Fig. 15).
This represents one of the highest rates of endemism reported for any marine ecosystem,
which could be due to cooler water temperatures limiting the northward distribution of
tropical species (Kane, Kosaki & Wagner, 2014). Figure 16 shows a comparison of overall
rates of endemism among fishes in both MCEs and shallow reefs of the NWHI and ‘Au‘au
Channel, against general rates of endemism (mostly biased toward shallow reefs) for
the tropical Indo-Pacific and Eastern Pacific. The trend towards elevated endemism is
even stronger when relative abundance is taken into consideration. Not only are more
endemic species found on MCEs, but the endemics also tend to be the most abundant
species. At the northernmost end of the NWHI, the relative abundance of endemic reef
fishes exceeds 92% (Kane, Kosaki & Wagner, 2014), and even reach 100% in some places
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Figure 15 Proportion of endemic reef fish species in mesophotic fish communities of the NWHI.
(Kosaki et al., 2016). This pattern is also evident in the MHI, as illustrated by Fig. 12B (taken
at 90 m in the ‘Au‘au Channel) in which all but two of the hundreds of fishes are endemics.
This pattern may represent a combination of both depth and latitudinal gradients, and
ongoing quantitative surveys throughout the Hawaiian Archipelago should reveal more
detailed interpretations of these patterns.
Patterns of endemism among other groups (particularly macroalgae and marine
invertebrates) are more difficult to quantify. The full extent of endemism and the broader
diversity within the MCE flora can only be determined after molecular studies are conducted
and data are gathered from similar MCE habitats elsewhere in the Pacific. Until the
unidentified specimens of invertebrates from MCEs are examined by appropriate experts,
and comparable sampling is conducted elsewhere in the Pacific, it will not be possible to
determine proportions of endemism among marine invertebrates on Hawaiian MCEs.
Population dynamics
We hypothesized that growth rates (the radial extension of the carbonate plate) of Leptoseris
sp. corals, the dominant benthic organism at depths of 70–150 m in the Main Hawaiian
Islands, were similar to the only published growth rate for L.fragilis from the Red Sea
(0.2–0.8 mm yr−1) (Fricke, Vareschi & Schlichter, 1987). Because direct measurement via
submersible was unlikely to have the precision to measure such rates over the period of our
study, colonies were stained for later recovery and analysis. The stained colony recovered
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Figure 16 Proportion of endemic coral reef fish species across the tropical Indo-Pacific by island/re-
gion. Sources: Randall, 1998;Moura & Sazima, 2000;Allen, 2008;Floeter et al., 2008.Kane, Kosaki & Wag-
ner, 2014; this study.
from a depth of 83 m had stain appearing only in two marked patches of the skeleton,
making it difficult to conclusively describe the complete radial growth of the coral plate.
X-radiographic imaging of entire Leptoseris test colonies did not reveal the resolution
required to discern banding patterns. Additional colonies examined using CT scanning of
the entire plate yielded excellent images, clearly revealing fine banding parallel to the outer
edge of the colony. However, 114C analysis showed that all samples were younger than the
14C peak from the early 1960s that occurred as a result of nuclear weapons testing. This
result indicated that bands are approximately an order of magnitude too closely spaced
to be annual, but the cause of the banding remains unclear. The edge adjacent to the
stain on the marked colony showed an addition of 12 to 13 new bands but these did not
correspond to the two-year seasonal temperature cycle from the data logger deployed when
the coral was marked (Fig. 17). This first marked colony indicates some type of monthly
banding cycle so the additional colonies stained in-situ are an important part of future
studies. A series of U/Th dates from eight representative portions of the stained colony
indicate a colony age of ∼15 years (Table 3). Although 2-σuncertainty for U/Th dating is
generally ±0.1 years, each sub-sample integrates material from several years and different
sides of the colony extended further from the center. Also, no sample was collected from
the exact center of the colony, but based on the age difference between the two samples
nearest the center (LH1, LH2) approximately another 2.2 years was added to the age of
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Figure 17 Temperature log from stained coral.
Table 3 Ages of Leptoseris sp. colony samples based on Uranium/Thorium (U/Th) dating techniques. The colony was marked in December 2007
and sampled January 2010.
Sample Uranium–Uranium
234/238 activity
Thorium–Uranium
230/238 activity
Initial delta 238U Age (yr) before 2012.75 Estimated sample
age (yr)
LH1 1.1467 ±0.0002 0.000160 ±7.1 ×10−7146.7 ±0.23 15.3 ±0.07 14.8
LH2 1.1470 ±0.0002 0.000137 ±7.0 ×10−7147.0 ±0.19 13.1 ±0.07 10.4
LH3 1.1470 ±0.0002 0.000132 ±9.5 ×10−7147.0 ±0.17 12.6 ±0.09 9.9
LH4 1.1469 ±0.0002 0.000138 ±1.1 ×10−6146.9 ±0.23 13.1 ±0.11 10.4
LH5 1.1469 ±0.0003 0.000061 ±5.6 ×10−7146.9 ±0.27 5.8 ±0.05 3.1
LH6 1.1469 ±0.0002 0.000053 ±3.3 ×10−7146.9 ±0.18 5.0 ±0.03 2.3
LH7 1.1471 ±0.0002 0.000138 ±8.6 ×10−7147.1 ±0.24 13.2 ±0.08 10.5
LH8 1.1468 ±0.0002 0.000112 ±7.3 ×10−7146.8 ±0.18 10.7 ±0.07 8.0
sample LH1 to determine a final colony age of ∼14.8 years at the time of recovery. The
mean of several radius measurements is 14.9 cm providing a mean growth rate of ∼1
cm yr−1, or more than an order of magnitude faster than that reported for L. fragilis.
Logistical constraints associated with working at mesophotic depths severely limited
the number of specimens available for life-history analysis (37 Centropyge potteri, 33
Ctenochaetus strigosus, and 33 Parupeneus multifasciatus), and the number of length
estimates obtained from laser-videogrammetry surveys (21 C. potteri, 28 C.strigosus, and
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90 P. multifasciatus). Thus, the results presented here should be considered preliminary
and did not warrant rigorous statistical analysis. Table 4 presents densities, average lengths,
and life-history parameters for mesophotic populations from the ‘Au‘au Channel and for
previously studied shallow-water populations from across the main Hawaiian Islands. The
results were not consistently higher or lower in MCEs compared to shallow reefs. The net
effect of these differences, when combined with size-structure data, was predicted by the
Ricker model (Everhart & Youngs, 1992), which we modified as described in the detailed
‘Materials and Methods’. The results presented in Table 5 indicate that biomass and egg
production estimates were lower at MCE depths, and estimates for shallow depths are at
least an order of magnitude higher for all except the egg production of P. multifasciatus.
The parameters used in the Ricker model interact in complicated ways, making it difficult
to determine reasons for the differences between MCEs and shallow depths. Given the
admittedly preliminary nature of our results, we are unwilling to speculate on the cause(s)
of these differences. Nevertheless, the possibility that biomass production and reproductive
output of exploited fish populations are lower in MCEs deserves full consideration in future
fishery management and habitat conservation efforts.
Broad trophic characterizations
The relative representation of different trophic groups of fishes on shallow reefs and
MCEs in the NWHI is illustrated in Fig. 18. Shallow reefs were numerically dominated
by herbivores and mobile invertivores, whereas MCE fish communities were numerically
dominated by planktivores (See the ‘‘NWHIFishTrophic’’ (Supplemental Information 2;
Tab 3) Worksheet of the Raw Data file).
Isotopic analysis of benthic reef fishes from different feeding guilds in both shallow and
MCE habitats of the MHI revealed that carbon isotopic (δ13C) values for all feeding guilds
overlapped across shallow and MCE depth ranges, but some significant differences were
observed (Bradley et al., in press). Ranges of δ13C values in planktivorous fish were smaller
than those of benthic invertivores in both shallow and MCE communities. Omnivores
showed a greater range in carbon isotopic composition at shallow depths than at MCE
depths, and pooled data across O‘ahu and Maui revealed significantly lower δ13C values
for individuals from MCEs compared to shallow individuals (Bradley et al., in press). In
addition, significant differences in δ13C values were found between depths for benthic
invertivores, but not in planktivores. Shallow omnivore δ15N values were slightly (but
significantly) higher than MCE omnivores, but no significant differences for the overall
populations of invertivores and planktivores were found between depths (Bradley et al.,
in press). Nitrogen isotopic (δ15N) values for the majority of source and trophic amino
acids (Popp et al., 2007) were not significantly different between depths for any taxon with
the exception of Centropyge (Pomacanthidae) and Sargocentron (Holocentridae), where
δ15N values were lower in MCE fishes compared to shallow fish (Bradley et al., in press). No
significant differences in trophic position calculated from amino acid isotopic compositions
were found with increasing fish standard length between islands in any feeding guilds.
Between depths, amino acid–based trophic positions of MCE benthic invertivores were
slightly but significantly higher than those from shallow depths (Bradley et al., in press).
Pyle et al. (2016), PeerJ , DOI 10.7717/peerj.2475 25/45
Table 4 Life history and population characteristics of exploited fishes at MCE and euphotic depths. Lengths (L) as fork length (FL) or total length (TL) are in mm,
weights (W) are in g, time (t) is days, batch fecundity (BF) is number of eggs. MCE columns represent the ‘Au‘au Channel, shallow columns from previous studies
throughout the main Hawaiian Islands (Longenecker & Langston, 2008;Langston, Longenecker & Claisse, 2009).
C. potteri (TL) C. strigosus (FL) P. multifasciatus (FL)
MCE Shallow MCE Shallow MCE Shallow
Density (#/m2) 0.0024 0.0120 0.0025 0.0524 0.0287 0.0442
Mean L 77.7 70.0 96.7 99.2 122.5 133.8
L-W W=4.99·10−5
(L)2.877
W=2.28·10−5
(L)3.053
W=2.13·10−5
(L)3.037
W=6.51·10−5
(L)2.8499
W=2.02·10−5
(L)2.970
W=3.45·10−5
(L)2.868
Growth Lt=103.18
(1-e−0.01196(t+146.14))
Lt=127
(1-e−0.00228(t+63.9))
Lt=129.86
(1-e−0.00439(t+96.52))
Lt=142.62
(1-e−0.00717(t−60.31))
Lt=167.646
ee−0.0322504(t−87.2819)
Lt=303
(1-e−0.00207(t+49.4))
♀L50 73 54 79 84 136 145
L-BF BF =5.494 ·10−12
(L)7.6343
BF =0.0118
(L)2.596
BF =1.5889·10−29
(L)16.1377
BF =1.2766·10−5
(L)4.1663
BF =1.8865
(L)1.7271
BF =0.0018
(L)3.092
Size-specific sex ratios %♀=232.96−
1.88(L)
%♀=405.5−
4.44(L)
%♀=1239.1−
10.9(L)
%♀=5.99 +85.4
9(−.5∗((L−95.58)/26.92)∧2)
%♀=346.76−
1.78(L)
%♀=141.3−
0.617(L)
Pyle et al. (2016), PeerJ , DOI 10.7717/peerj.2475 26/45
Table 5 Estimates of biomass and egg production for exploited fishes at mesophotic and euphotic
depths. MCE column represents the ‘Au‘au Channel, shallow column from previous studies throughout
the main Hawaiian Islands (Longenecker & Langston, 2008;Langston, Longenecker & Claisse, 2009).
MCE Shallow
C. potteri g/m2/yr 0.0773 1.9861
eggs/spawning event/m27 26
C. strigosus g/m2/yr 0.0382 6.9699
eggs/spawning event/m22 340
P. multifasciatus g/m2/yr 1.9702 19.9779
eggs/spawning event/m2133 155
For omnivores and planktivores, these results indicate that changes in nutrient sources
over the depth range studied did not affect their position within the food web. The small
but significantly high trophic position of benthic invertivore feeding guilds from MCEs
most likely resulted from consumption of fewer macroalgal grazers on MCEs compared to
shallow reefs (Bradley, 2013;Bradley et al., in press).
Isotopic results show that individual fish species generally do not differ greatly in trophic
position between the two reef ecosystems (Bradley, 2013;Bradley et al., in press), indicating
that managing reef fish species as one group across depths may be appropriate. An exception
to this general observation was found in a study of diet and movements of Galapagos sharks,
Carcharinus galapagensis (Snodgrass & Heller, 1905), and Giant trevally, Caranx ignobilis
(Forsskål, 1775), from a MCE at Pearl and Hermes Atoll in the NWHI. Based on stable
isotopic analysis and acoustic telemetry to study diet and movements, Papastamatiou et
al. (2015) found that giant trevally occupied a wide range of trophic positions potentially
due to intraspecific competition. However, carbon isotopic compositions of several species
of benthic feeding fish indicate that carbon flow in the two ecosystems may be distinct
(Papastamatiou et al., 2015;Bradley et al., in press). While this does not alter the relative
trophic position of the fish, it implies that caution should be taken when considering shallow
reefs and MCEs as a single ecosystem as the flow of biomass may be different in the two
ecosystems.
MCEs as refugia
Much has been written about the potential for MCEs to serve as refugia for shallow-reef
species (Hughes & Tanner, 2000;Riegl & Piller, 2003;Bongaerts et al., 2010;Hinderstein
et al., 2010;Bridge & Guinotte, 2013;Kahng, Copus & Wagner, 2014;Holstein et al., 2015).
Most of the discussion has focused on MCEs having reduced susceptibility to coral bleaching
events due to reduced irradiance and increased thermal stability, as well as protection from
storms and mechanical disturbances (such as anchor damage). To some extent, especially
in the MHI where the horizontal distance of many MCEs from shore is large, distance may
confer some protection from coastal impacts, such as sedimentation and pollution. In some
cases, MCEs may offer protection from fishing pressure, particularly for fisheries that rely
on divers or are otherwise impractical at greater depths (Lindfield et al., 2016).
Pyle et al. (2016), PeerJ , DOI 10.7717/peerj.2475 27/45
Figure 18 Comparison of fish assemblage trophic structure between shallow and mesophotic reefs in
the NWHI. NIH, Nihoa; FFS, French Frigate Shoals; MID, Midway Atoll; PHA, Pearl and Hermes Atoll;
KUR, Kure Atoll.
As summarized by Bridge & Guinotte (2013), in order to consider MCEs as refugia for
inhabitants of shallow reefs, MCEs must harbor populations of species that are impacted
on shallow reefs, in ways that would allow propagules from MCE populations to colonize
shallow reef habitat (i.e., adequate genetic connectivity; although potential for propagule
dispersion and settlement is not the only determinant of genetic connectivity). MCEs
Pyle et al. (2016), PeerJ , DOI 10.7717/peerj.2475 28/45
must also be more resilient to stresses that affect shallow reefs. Bongaerts et al. (2010)
reviewed the literature regarding the ‘deep reef refugia’ hypothesis for Caribbean reefs and
concluded that it is more likely to apply to ‘‘depth generalist’’ species and may serve a
greater importance in the upper range of MCEs (30–60 m). This was exemplified by the
coral Seriatopora hystrix in Okinawa, which was extirpated from shallow water, and later
discovered at 35–47 m (Sinniger, Morita & Harii, 2013). A primary goal of our research
was to understand the extent of connectivity by species across the archipelago, and both
genetic and trophic relationships between MCEs and nearby shallow reef habitats. In the
first genetic comparison of shallow and MCE reef fishes, the damselfish Chromis verator
showed no population structure across depths (Tenggardjaja, Bowen & Bernardi, 2014).
Thus, the initial genetic data and the high degree of shared fish species between shallow
reefs and MCEs (84%, when considering the full depth range of MCEs) indicate that MCEs
may function as refugia for some impacted populations on shallow reefs, especially for
fishes (Lindfield et al., 2016). However, biomass and egg production estimates for three
exploited species (C. potteri,C. strigosus, and P. multifasciatus) from this study (Table 5)
are consistently lower for MCE populations, even though estimates for shallow populations
incorporate the effects of fishing mortality. Moreover, patterns of larval dispersal between
and among shallow and MCE populations are not well known. Rather than being viewed
as a source for shallow-water reef fish, the MCE populations may require more protection
than their shallow-water counterparts.
Vertical distribution of scleractinian coral species in the Hawaiian Islands is well known
for common, conspicuous species while rare, cryptic or hard to identify species are less
understood. Rooney et al. (2010) and Luck et al. (2013) both reported depth ranges for
scleractinian species. Based on the anecdotal observations of this study, we observed a
similar pattern of species distribution where there appears to be greater species overlap
between shallow reefs and upper MCEs (30–60 m) than between shallow reefs and lower
MCEs (>60 m). As such, the lower MCE populations do not serve as effective scleractinian
species refugia for shallow reefs. This pattern of coral segregation by depth has also
been reported by Kahng, Copus & Wagner (2014). Corals in the upper MCE may in some
cases serve as refugia for shallower populations, as modeling studies indicate high larval-
mediated connectivity (Thomas et al., 2015;Holstein, Smith & Paris, 2016). Few studies
have tested genetic connectivity across depths for corals. Based on a microsatellite survey
of Porites astreoides in the West Atlantic, Serrano et al. (2016) showed high connectivity
between shallow and deep reefs in Bermuda and U.S. Virgin Islands, but some evidence of
population structure between shallow and deep reefs in Florida. Van Oppen et al. (2011)
showed a restriction of gene flow between shallow and deep colonies of the brooding coral
Seriatopora hystrix, but also some evidence that larvae from deep reefs may seed shallow
reefs. Hence the evidence for coral refugia is equivocal at this time, and studies in Hawaii
would be valuable contributions to this debate.
Recently, the Caribbean coral, Porites astreoides, was shown to have similar reproductive
characteristics across depths. Holstein, Smith & Paris (2016) modeled the vertical
connectivity of two Caribbean species, P. astreoides (brooder) and Orbicella faveloata
(broadcaster) and predicted significant contribution from both species with a high local
Pyle et al. (2016), PeerJ , DOI 10.7717/peerj.2475 29/45
contribution from the brooder (Holstein et al., 2015). However, both of these studies
were conducted in shallow reefs and the upper MCE and not in the lower MCE further
suggesting less connectivity with the lower MCE. Prasetia, Sinniger & Harii (2016) examined
the reproductive characteristics of Acropora tenella from the upper MCE and found the
reproductive characteristics to be similar to shallow reef acroporids, but they did not
examine lower MCE colonies.
While MCEs in Hawai‘i may fulfill the first requirement for refugia (at least for fishes
and some corals), the resilience of Hawaiian MCEs as compared to their shallow-reef
counterparts remains unknown. Several abiotic factors (e.g., exposure to high light or
temperature fluctuations) would intuitively cause more stress for shallow reef systems than
for MCEs, but the impact of these stressors on coral resilience is not always straightforward.
Corals with regular exposure to high temperatures or elevated PAR may be more tolerant of
extreme conditions than corals without such exposure (West & Salm, 2003;Grimsditch &
Salm, 2006). Conversely, corals inhabiting more stable and cooler conditions on MCEs may
be less resilient to temperature changes than their shallow-reef counterparts. The impacts of
climate change on MCEs are not yet understood, and we are in need of additional research
and predictive modeling before assumptions can be made about the resilience of MCEs as
compared to shallow reefs. While vertical thermal stratification maintains some MCEs at
lower temperatures than shallow reefs, MCEs may still be vulnerable to thermal anomalies
that drive bleaching on shallow reefs. During a September 2014 mass-bleaching event in
the NWHI, water temperatures of 24 ◦C were recorded by divers at 60 m at Lisianski,
approximately 4 ◦C higher than typical for that depth. Mesophotic coral communities may
potentially be as vulnerable to bleaching events as adjacent shallow reefs. However, our
ability to predict the oceanographic conditions that cause thermal conditions at MCE depths
is more limited than shallow reefs. This threat has potentially severe implications for the
numerous undescribed species of algae collected from the same MCE site at Lisianski; with
an increased frequency and severity of warm-water thermal anomalies, we may be at risk of
losing some of these species to climate change before we even document their existence.
Corals in MCEs are growing at considerably lower SI, and are potentially near the lower
limit of light intensity required for photosynthesis. Water clarity was identified as a key
factor in predicting the presence of MCEs, with less well-developed MCEs in areas with less
light penetration (Costa et al., 2015). It is conceivable that a small increase in turbidity near
the surface (e.g., from coastal activities that either produce excess sedimentation directly or
increase nutrient levels causing increased plankton densities) could have greater impacts
on MCEs than on their shallow-reef counterparts.
As has been suggested previously (Stokes, Leichter & Genovese, 2010;Lesser & Slattery,
2011), the potential for MCEs to serve as refugia for shallow reefs likely depends on
multiple factors and should be evaluated on a case-by-case basis for different taxa and
different sources of disturbance. One important question that has not been addressed in
the previous literature is the extent to which shallow reefs might serve as refugia for MCEs.
Given the uncertainties about the relative resilience and insulation from a wide range
of environmental stress factors that impact coral-reef environments between MCEs and
shallow coral reefs, it is premature to make any assumptions about which habitat is more
Pyle et al. (2016), PeerJ , DOI 10.7717/peerj.2475 30/45
vulnerable to disturbance or which might serve as a refuge. Thus, when future studies assess
the potential for MCEs to serve as refugia to replenish disturbed shallow reefs, they should
also consider the implications of the reverse relationship as well.
Management implications
Our multi-year collaborative research on MCEs across the Hawaiian Archipelago has
provided new insights on basic geophysical characteristics, patterns of biodiversity, and
information on genetic and trophic connectivity that can enhance the foundations for
management and conservation of MCEs and coral-reef environments in general.
The ‘Au‘au Channel is the most extensive complex of MCE coral and macroalgal
communities in Hawai‘i. Growing on the island’s deep slope, its fragile structure and
biodiversity is currently isolated from some anthropogenic impacts, but MCEs should be
considered in all future coastal zone management plans for the region. Currently, part
of the ‘Au‘au Channel is listed as a Habitat Area of Particular Concern by the National
Marine Fisheries Service. Given its unique geomorphology and biotic characteristics, state
or federal managers should include a fully protected area. The discovery of similar MCEs
off Kaua‘i, Ni‘ihau, and in the NWHI confirm that such environments occur elsewhere
within the Hawaiian Archipelago and likely the broader Pacific. Although these sites have
not been studied to the same extent as the ‘Au‘au Channel, it is clear from divers and remote
camera surveys that the corals form fragile complexes and would be easily damaged from
bottom contact. There also appears to be a rich diversity of mesophotic macroalgae in the
NWHI. The need to fully protect the ‘Au‘au Channel and other MCE hotspots within the
Hawaiian Archipelago is underscored by the fact that upper MCEs (30–60 m) are likely to
serve a more prominent role as a refuge for corals, while the lower MCEs (>60 m) harbor
unique assemblages of species with higher rates of endemism. As noted previously, MCEs
may also potentially serve as spatial refugia for some overexploited shallow-reef fishes, but
this potential must be evaluated on a species-by-species basis.
Our research reinforces the theme that MCEs require clear water, likely due to increased
levels of PAR reaching greater depths. These findings indicate that MCEs are less resilient
to certain stresses than their shallow-reef counterparts, particularly surface-water clarity.
Assessments of the impact of increased turbidity (e.g., from shore-based run-off or nutrient
enrichment and its impact on plankton densities) should not be limited to shallow coral-
reef ecosystems directly exposed to impaired water quality; it may well be the case that vast
expanses of MCE habitat at the limits of photosynthetic production could also be heavily
impacted. Examples of dead, coralline algal-covered plate coral formations were observed
during this project and highlighted the reality of threats to MCEs.
Other potential impacts to MCE habitats (e.g., fishing pressure, cable laying, placement
of permanent moorings and dredging) should be considered in coastal zone management
activities, especially when the full extent of MCEs has not yet been documented. For
example, with the increasing push for renewable energy and integrated electric grids
between islands (undersea cables, offshore windmills, wave energy structures, or other
renewable technologies), areas with shallow to intermediate bathymetry, protection from
large swells, and a greater distance from shore make certain MCE areas (like the ‘Au‘au
Pyle et al. (2016), PeerJ , DOI 10.7717/peerj.2475 31/45
Channel) ideal locations for renewable energy structures. Planning for such activities needs
to consider vulnerabilities associated with MCEs.
In addition to thermal stress (discussed above), climate-driven threats to MCEs
may come in the form of increased frequency and severity of large storms (Emanuel,
2005). Currently, major storms that form in the Eastern Tropical Pacific usually pass
south of Hawai‘i, but increasing sea surface temperatures may allow these storms to
move north (Pachauri & Meyer, 2015). High benthic cover by corals (Leptoseris spp.)
on MCEs in the ‘Au‘au Channel is in part facilitated by shelter from wave energy
provided by the islands of Maui, Lana‘i, Kaho‘olawe, and Moloka‘i (Costa et al., 2015).
A direct hit by a major storm may cause enough mixing of warm stratified surface
waters to cause thermal stress at depth, and even a small increase of benthic sheer
stress at depth may damage or destroy fragile MCE corals. Finally, ocean acidification
may threaten not only corals, but also crustose coralline algae (Jokiel et al., 2008).
Rhodolith beds are common features of NWHI and MHI MCEs (Spalding, 2012), and
both crustose coralline algae and rhodoliths serve as attachment substrata for MCE
algae and antipatharian corals. While there is little that local resource managers can
do to alleviate large-scale climate events, it is nevertheless important to understand the
potential impacts climate change can have when establishing conservation priorities.
We still know little about MCEs, even in well studied areas such as Hawai‘i, and we do not
yet understand the threats to or importance of MCEs in a changing climate. Research needs
to be conducted to better characterize whether MCEs will be more or less vulnerable to
warming and acidification, or if they will increase the resilience of coral reefs or individual
taxa. A better understanding of the basic biodiversity characteristics (e.g., discovering,
documenting and describing new species, improving our understanding of depth ranges
and endemism, and levels of genetic and trophic connectivity between populations of
conspecifics in shallow-reef and MCE habitats) is critical for making informed management
decisions. The functional role of MCEs beyond direct connectivity to broader coral reef
management must be integrated in future management plans or actions addressing coral
reefs.
While this project established core baselines for community dynamics within several
regions of the Hawaiian Archipelago, it is vitally important to investigate MCE communities
elsewhere throughout the Pacific to provide essential context for comparisons of patterns
and processes. Most areas of the Pacific remain completely unexplored. This lack of
understanding has profound implications for US waters within the Pacific with the recent
listing of 15 coral species under the Endangered Species Act and an additional three species
proposed for listing. Several of these species are known to exist in MCEs (Bare et al., 2010)
and others may be present, but not documented. Clearly the documentation of MCEs is
essential for prudent management of Hawaiian resources, and comparison to other Pacific
habitats will lead to a better understanding of the unique biodiversity within Hawaiian
waters.
Pyle et al. (2016), PeerJ , DOI 10.7717/peerj.2475 32/45
ACKNOWLEDGEMENTS
We dedicate this work to our friend, colleague, and co-author John Rooney, whose
commitment to documenting MCEs in Hawaii was inspirational to us all. Our sincere
gratitude goes to Kimberly Puglise for her constant support and encouragement. We thank
Matt Ross, Joshua Copus, Robert Whitton, Sonia Rowley, Dave Pence, Jason Leonard, Brian
Hauk, Keolohilani Lopes, Christian Clark, Greg McFall, Elizabeth Kehn, Sarah Harris, Paul
Murakawa, Brett Schumacher, Russell Sparks, Skippy Hau, Brad Varney, Linda Marsh,
Bill Gordon, Kim Tenggardjaja, and the staff, officers and crew of the NOAA Ships
Hi‘ialakai and Ka‘imikai-o-Kanaloa. Many thanks to the pilots and support staff of HURL
for their amazing assistance with the submersibles and ROV. Jacqueline Padilla-Gamino,
Xavier Pochon, Zachary Forsman, Melissa Roth, Robert Toonen, and Ruth Gates were
instrumental with coral molecular analyses. Alison Sherwood, Roy Tsuda, Isabella Abbott,
and Gerald Kraft assisted with macroalgal identifications. The dating analysis of the marked
Leptoseris hawaiiensis coral was conducted by the Cohen Laboratory at the Woods Hole
Oceanography Institution. Sonia Rowley provided very helpful editorial comments and
insights. The findings and conclusions in this article are those of the author(s) and do
not necessarily represent the views of the US Fish and Wildlife Service or NOAA. This is
the School of Ocean and Earth Science and Technology contribution number 9814, and
Contribution No. 2016-016 to the Hawaii Biological Survey.
ADDITIONAL INFORMATION AND DECLARATION
Funding
This paper includes results of research funded by the National Oceanic and Atmospheric
Administration (NOAA) Center for Sponsored Coastal Ocean Research (Coastal Ocean
Program) under award NA07NOS4780188 to the Bishop Museum, NA07NOS4780187
and NA07NOS478190 to the University of Hawai‘i, and NA07NOS4780189 to the State of
Hawai‘i; submersible support provided by NOAA Undersea Research Program’s Hawai‘i
Undersea Research Laboratory (HURL); funding from the NOAA Papah¯
anaumoku¯
akea
Marine National Monument to the Bishop Museum and the Univ. of Hawai‘i Department
of Botany, and funding from the NOAA Coral Reef Conservation Program research grants
program administered by HURL under award NA05OAR4301108 and NA09OAR4300219,
project numbers HC07-11 and HC08-06. Staff and NOAA ship vessel time for three research
cruises were provided by National Marine Fisheries Service, Pacific Islands Fisheries
Science Center. Additional funding for this project was provided by the State of Hawaii,
Department of Land and Natural Resources, Division of Aquatic Resources. Support for
additional rebreather-based surveys off Hawai‘i and elsewhere in the Pacific were provided
by the Association for Marine Exploration. Life-history analysis of shallow-water fishes was
funded by the Hawaii Coral Reef Initiative and the Dingell-Johnson Sportfish Restoration
program. The funders had no role in study design, data collection and analysis, decision to
publish, or preparation of the manuscript.
Pyle et al. (2016), PeerJ , DOI 10.7717/peerj.2475 33/45
Grant Disclosures
The following grant information was disclosed by the authors:
National Oceanic and Atmospheric Administration (NOAA) Center: NA07NOS4780188,
NA07NOS4780187, NA07NOS478190, NA07NOS4780189.
NOAA Undersea Research Program’s Hawaii Undersea Research Laboratory (HURL).
NOAA Papah¯
anaumoku¯
akea Marine National Monument.
NOAA Coral Reef Conservation Program: NA05OAR4301108, NA09OAR4300219, HC07-
11, HC08-06.
State of Hawaii, Department of Land and Natural Resources, Division of Aquatic Resources.
Hawaii Coral Reef Initiative.
Dingell-Johnson Sportfish Restoration program.
National Marine Fisheries Service, Pacific Islands Fisheries Science Center.
Association for Marine Exploration.
Competing Interests
The authors declare there are no competing interests.
Author Contributions
•Richard L. Pyle, Ken Longenecker, Frank A. Parrish and John Rooney conceived and
designed the experiments, performed the experiments, analyzed the data, wrote the
paper, prepared figures and/or tables, reviewed drafts of the paper.
•Raymond Boland, Holly Bolick, Corinne Kane, Randall K. Kosaki, Ross Langston,
Anthony Montgomery and Daniel Wagner conceived and designed the experiments,
performed the experiments, analyzed the data, wrote the paper, reviewed drafts of the
paper.
•Brian W. Bowen and Heather L. Spalding conceived and designed the experiments,
performed the experiments, analyzed the data, contributed reagents/materials/analysis
tools, wrote the paper, reviewed drafts of the paper.
•Christina J. Bradley and Brian N. Popp conceived and designed the experiments,
performed the experiments, analyzed the data, contributed reagents/materials/analysis
tools, wrote the paper, prepared figures and/or tables, reviewed drafts of the paper.
•Celia M. Smith conceived and designed the experiments, analyzed the data, wrote the
paper, reviewed drafts of the paper.
Animal Ethics
The following information was supplied relating to ethical approvals (i.e., approving body
and any reference numbers):
All vertebrates (fishes) were collected in accordance with University of Hawaii IACUC
protocol 09-753-5, ‘‘Phylogeography and Evolution of Reef Fishes’’ (PI: Dr. Brian Bowen),
including collection and euthanization by spear.
Field Study Permissions
The following information was supplied relating to field study approvals (i.e., approving
body and any reference numbers):
Pyle et al. (2016), PeerJ , DOI 10.7717/peerj.2475 34/45
The State of Hawai‘i Department of Land and Natural Resources developed Special
Activity Permits for the University of Hawai‘i and National Marine Fisheries Service for
work related to this project that occurred within State of Hawai‘i waters. All sampling
procedures and experimental manipulations were reviewed as part of obtaining the field
permit. Special Activity Permits do not have reference numbers. Papah¯
anaumoku¯
akea
Marine National Monument provided research permits for field work in the Northwestern
Hawaiian Islands.
Data Availability
The following information was supplied regarding data availability:
Global Biodiversity Information Facility: http://www.gbif.org/dataset/b929f23d-290f-
4e85-8f17-764c55b3b284
Supplemental Information
Supplemental information for this article can be found online at http://dx.doi.org/10.7717/
peerj.2475#supplemental-information.
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