Quantitative Analysis of the Mesophotic Coral Ecosystem Benthos

in the Northwestern Hawaiian Islands

Presented to the Faculty of the

Tropical Conservation Biology and Environmental Science Program

University of Hawai‘i at Hilo

in partial fulfillment of the requirements for the degree of

Master of Science

in Tropical Conservation Biology and Environmental Science

August 2021

By

Laura J. Knight

Thesis Committee:

Dr. Karla J. McDermid

Dr. Marta J. deMaintenon

Dr. Randall K. Kosaki

Keywords: Mesophotic Coral Ecosystem, Coral Reefs, Northwestern Hawaiian Islands

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TABLE OF CONTENTS

ABSTRACT........................................................................................................................ii

INTRODUCTION...............................................................................................................1

METHODS..........................................................................................................................9

RESULTS..........................................................................................................................10

DISCUSSION....................................................................................................................11

REFERENCES..................................................................................................................17

TABLES…………………………………………………………………………………31

FIGURES...........................................................................................................................39

APPENDIX 1…………………………………………………………………………….46

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Abstract

Mesophotic coral reef ecosystems are light-dependent coral communities at tropical and some

higher latitudes that occur from about 30 to 150 m deep, in the so-called “coral-reef twilight

zone” or “deep reefs.” New emphasis has been placed on investigating mesophotic communities

around the world. Advances in diving technologies have made it safer to conduct research at

these depths. In this study of the mesophotic zone of the Northwestern Hawaiian Islands(NWHI),

391 photoquadrat images were examined (Nihoa 155, French Frigate Shoals 60, Laysan 57, and

Kure 119) from a total of 23 transects (Nihoa 7, French Frigate Shoals 8, Laysan 3, and Kure

5). Transect depth ranged from 43.9 m on Nihoa to 96 m on Kure Atoll. Images were analyzed

using Coral Net BETA. Fifty random points were generated on each photograph of the

substratum, and the organism under each point was identified to the lowest taxonomic level

possible. Fifty-eight taxa, six species of Chlorophyta (green macroalgae), nine Phaeophyta

(brown macroalgae), 15 Rhodophyta (red macroalgae), 16 species of corals, and 12 non-coral

invertebrates) were recorded in the mesophotic communities. Each island or atoll had a different

suite of top ten living space-holders. The diversity of living taxa was highest at French Frigate

Shoals and the lowest at Laysan. The percent similarity in mesophotic communities was greatest

between Kure and Laysan (44%). The least percent similarity was found between French Frigate

Shoals and Kure Atoll (29%). Despite the mesophotic zone receiving a limited amount of

sunlight, substrata in the mesophotic zone are not barren, but rich in living organisms. This study

found that algal turfs comprised of multiple species are the most abundant space-holding entity

in the mesophotic benthic community. The low diversity of taxa documented in these mesophotic

communities may be a function of the low number of species adapted to mesophotic conditions

or the remoteness of the NWHI which limits the dispersal of species to the mesophotic zone.

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This study highlights the importance of distinct deepwater mesophotic communities. Each island

or atoll seems to host a unique community of algae, coral, and non-coral invertebrates, all of

which may be critical to supporting the rich ichthyofauna in the mesophotic zone.

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Introduction

The Northwestern Hawaiian Islands (NWHI) consist of numerous small basaltic islands,

atolls, submerged banks, and reefs, stretching from Nīhoa to Hancock Bank for more than 2000

km (Fig. 1). The lands and waters of the NWHI are protected as state and federal wildlife refuges

and as the Papahānaumokuākea Marine National Monument, which was established in 2006 and

expanded in 2016 (Coffman & Kim 2008, Selkoe et al. 2009). The combination of geographic

isolation, diverse geomorphology, and mixture of oceanographic conditions in the NWHI has

resulted in rich species diversity, complex ecological communities, and a very high level of

endemism. Previous studies have estimated as much as 11% endemism for macroalgal species on

French Frigate Shoals, and 7% at Gardner Pinnacles (Friedlander et al. 2009). The community

structure is also unusual in the NWHI because it is a top-down, or predator-dominated

ecosystem, in which over 54% of the total fish biomass is composed of apex predators

(Friedlander & DeMartini 2002). Cryptobenthic reef fishes (CRFs) (bottom‐dwelling,

morphologically or behaviorally cryptic species typically less than 50 mm in length) account for

almost 60% of the fish biomass consumed on the reefs studied in Belize, French Polynesia, and

Australia (Brandl et al. 2019). CRFs may also play an important trophodynamic role in the

NWHI shallow and mesophotic reef ecosystems.

The NWHI are an important habitat for a variety of protected species. The Hawaiian

monk seal, one of the most endangered marine mammals in the world, lives primarily in the

NWHI (Antonelis et al. 2006). Green turtles (Chelonia mydas), listed as threatened under the

U.S. Endangered Species Act, migrate from feeding grounds in the main Hawaiian Islands

(MHI) to their primary nesting beaches in the NWHI (Balazs & Chaloupka 2006). The region is

also home to the largest nesting population of the Laysan albatross (USFWS 2005), as well as

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many other seabird species. Because of their remote location, 3,800 km from the nearest

continental land mass (Rooney et al. 2010), the marine habitats of the NWHI, especially those

greater than 30 m deep, are relatively understudied compared to areas that are easily accessible.

During the last two decades, there has been a notable increase in the study of deep-sea

environments, using submersibles and remotely operated vehicles (ROVs). However, the

intermediate depths (30 m to 150 m deep) have not received as much attention as either the

shallow reefs or the deep-sea (Blyth-Skyrme et al. 2013). Mesophotic coral reef ecosystems are

light-dependent coral communities at tropical and some higher latitudes that occupy depths of

about 30 to150 m, in the so-called “coral-reef twilight zone” or “deep reefs,” (Hinderstein et al.

2010, Bejarano et al. 2014, Pinheiro et al. 2016, Loya et al. 2016, Kahng et al. 2017, Baldwin et

al. 2018). The lower limit of the mesophotic zone (150 m) is defined as the maximum depth at

which there is sufficient penetration of sunlight to support photosynthesis and, hence, the growth

of zooxanthellate coral reefs (Bongaerts et al. 2010, Hinderstein et al. 2010, Baldwin et al. 2018).

Benthic members of mesophotic coral reefs include light-dependent corals, sponges, other

invertebrates, and algal species.

New emphasis has been placed on investigating mesophotic communities around the

world (Rooney et al. 2010, Weiss 2017a). Advances in diving technologies have made it safer to

conduct research at these depths. In 1989, the use of mixed-gas SCUBA and other technical

diving techniques gave researchers the ability to study coral reefs at depths of 60-150 m (Weiss

2017a, b). Dives in the Cook Islands, Papua New Guinea, and Palau resulted in over 200 fish

specimens, from over 100 species, 50 of which were new species (Pyle 2000). Most of the new

species belong to one of the five families: Gobiidae (gobies), Serranidae (groupers), Labridae

(wrasses), Pomacentridae (damselfishes) and Apogonidae (cardinal fishes) (Pyle 2000).

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Mesophotic fish assemblages in the NWHI have high total densities, dominated by planktivores

and invertivores (Fukunaga et al. 2016).

Studies investigating reef fish endemism in the NWHI reported that 69% of reef fish

encountered on mesophotic reefs are endemic, rising to greater than 85% endemism at Pearl and

Hermes Atoll and Midway Atoll (Kane et al. 2014), and 100% endemism of mesophotic fish at

the northernmost atoll, Kure (Kosaki et al. 2016). Species endemism in the Northwestern

Hawaiian Islands has been shown to increase with depth (Fukunaga et al. 2016, Pyle et al.

2016a,). Recently, several new species and new records of marine macroalgae (Spalding et al.

2016, Sauvage et al. 2019, Sherwood et al. 2020, 2021, Paiano et al. 2020, Cabrera et al. 2021)

and fish (Fukunaga et al. 2016, Pyle & Kosaki 2016, Pyle et al. 2016b) have been reported from

the mesophotic reefs of the NWHI.

New species of amphipods and other invertebrate species have also been discovered on

mesophotic coral reefs (Senna et al. 2014). Research on non-coral invertebrates is limited in

comparison to research on fish and coral in these depths, despite the abundance of invertebrates

at mesophotic depths. One study in Japan not only found new species at mesophotic depths, but

also found a cnidarian in the family Abyssoanthidae at 300 to 400 m from Kochi, Japan, that was

previously recorded only at depths of 2000 to 5600 m (Reimer et al. 2019). In the Mediterranean,

43 mollusc species were identified in the mesophotic zone of Israel that had not been previously

recorded in the area, bringing their overall mollusc diversity up by 7% (Albano et al. 2020).

In addition to discoveries of new species and new records, investigations into community

structure, abundance, and diversity of species at mesophotic depths have been conducted. From

2012 to 2013, the Great Barrier Reef mesophotic zone was studied during the “Catlin Seaview

Survey,” which found that zooxanthellate corals were scarce below 80 m (Englebert et al. 2014).

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In this study, although most corals were rare, wrinkle coral ( Leptoseris, family Agariciidae)

communities extended below 125 m on the Yonge Reef, Great Barrier Reef, and in the Coral Sea

at Bougainville Reef (Englebert et al. 2014). All of the Leptoseris spp. colonies from 115 to 125

m deep were small, encrusting, and less than 10 cm in diameter. Sequencing of the cox1-1-rRNA

intron for two of the deepest colonies revealed a 99% match with Leptoseris hawaiiensis

colonies from Hawai‘i (Englebert et al. 2014). Surveys of mesophotic communities off Tutuila,

American Samoa, had similar findings: plate-like corals on the deep reef slopes were dominated

by Leptoseris, Pachyseris, or Montipora genera (Bare et al. 2010, Montgomery et al. 2019).

Furthermore, seafloor videos of mesophotic communities in the main Hawaiian Islands (MHI)

and NWHI showed that Leptoseris corals were the dominant corals from 80 to 150 m deep

(Kahng & Maragos 2006, Rooney et al. 2010). In addition, habitat modeling in the Hawaiian

Islands has been used to predict the mesophotic distribution of Leptoseris and Montipora

(Veazey et al. 2016). In Bermuda, great star coral, Montastrea cavernosa (family

Montastraeidae) colonies have smaller surface area, but higher density of colonies in the

mesophotic zone (Goodbody-Gringley et al. 2015). Even the diversity of prokaryotes associated

with Caribbean mesophotic corals shows great variation (Glasl et al. 2017). Staghorn coral

(Acropora and Isopora) (family Acroporidae) diversity and morphology varied with depth in the

mesophotic zone of the Great Barrier Reef and Coral Sea (Muir et al. 2015). Mesophotic coral

communities in the Northern Great Barrier reefs are also dominated by Leptoseris colonies

(Englebert et al. 2017).

Mesophotic reefs are thought to have the potential to protect and restock shallow reefs.

The deep reef refugia hypothesis (Glynn 1996, Bongaerts et al. 2010) suggests that deep reefs

can provide new recruits to anthropogenically impacted shallow reefs. Deeper reefs are sheltered

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from thermal stress, and they can serve as refugia during coral bleaching events that decimate

shallow reefs (Glynn 1996). In the Eastern Pacific, the deep reef refugia hypothesis is supported

by evidence from the Holocene fossil record (5000 years ago) for coral species, including two

recent recoveries after El Niño events extirpated intricate fire coral, Millepora intricata (family

Milleporidae), in shallow water (Smith et al. 2014). Mid-range mesophotic reefs (60 to 80 m

deep) in the Caribbean were reported to have great potential to provide protection to shallow

water reefs because of the overlap of species in both the deep and shallow reefs (Bongaerts et al.

2010). Another study in the Caribbean demonstrated that the reproductive output of the

mesophotic coral species, Orbicella faveolata (mountainous star coral, family Merulinidae), had

far greater gamete (eggs) output than the same species on adjacent shallow reefs (Holstein et al.

2015) Their work suggests that deep mesophotic reefs can serve as a reproductive reservoir for

shallow reefs nearby (Holstein et al. 2015). Two mesophotic Alveopora species (family

Acroporidae) in the Red Sea showed a relationship between environmental factors (light and

temperature) and gamete development (Eyal-Shaham et al. 2016). In a northern Australian reef

(Scott Reef), Seriatopora hystrix (birdsnest coral, family Pocilloporidae) exhibits vertical

connectivity between shallow waters (<30 m deep) and mesophotic depths (30 to 60 m

deep), suggesting that the deep water corals can provide recruits to the shallow waters and assist

with shallow reef recovery in the area (van Oppen et al. 2011).

Many studies of connectivity between mesophotic reefs and adjacent shallow coral reefs

have focused on benthic mesophotic organisms. However, Tenggardjaja et al. (2014) found no

significant genetic differences between the shallow (<30 m deep) and the mesophotic

populations of three spot chromis, Chromis verater, an endemic reef fish in the Hawaiian

Archipelago and adjacent Johnston Atoll. This study concluded that a high level of vertical

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connectivity exists, and mesophotic populations could replenish shallow reefs (Tenggardjaja et

al. 2014). More studies on mesophotic fish species and their connectivity with shallow reefs are

needed.

Holstein et al. (2016) argued that the deep water refugia hypothesis is only effective if

there are species that are depth generalists, with vertical connectivity between deep and shallow

reefs. An analysis of 9000 benthic and suprabenthic species from the mesophotic zone in the

Gulf of Mexico, determined that taxonomic overlap between shallow (0 to 20 m deep) and

progressively deeper zones declined steadily with depth in all taxa (Semmler et al. 2016). Mid-

and lower mesophotic habitats (60 to150 m deep) showed 15–25% overlap with shallow habitats,

and upper mesophotic zones (30 to 60 m deep) had 30–45% overlap with shallow habitats for all

taxa combined, causing Semmler et al. (2016) to conclude mid- and lower mesophotic zones

would have less (but not inconsequential) potential to serve as refugia. Brazeau et al. (2013)

investigated the genetic differentiation of the coral species Montastraea cavernosa in the

Caribbean among shallow (3 to 10 m), medium (15 to 25 m), deep (30 to 50 m), and very deep

(60 to 90 m) depths. Montastraea cavernosa exhibited significantly different genetic structure at

different depths, and low population connectivity among, and within the sites. Brazeau et al.

(2013) concluded that M. cavernosa at mesophotic depths is not supplying successful recruits to

the adjacent shallow reefs. If the failure to recruit is a result of shallow reef coral species

outcompeting mesophotic immigrants to the shallow reef, then if shallow species are extirpated,

perhaps mesophotic species could successfully settle, recruit, and colonize. Coral community

structure in the upper mesophotic zones of the Caribbean is composed of approximately 25 to

40% depth-generalist coral species, while the lower mesophotic zone coral species are mainly

deep-water specialists (Bongaerts et al. 2015). In addition to genetic differences between deep

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and shallow reefs, reproductive differences within the same species can also impact whether a

deep water reef can replenish a damaged shallow water reef with viable recruits. In Okinawa,

Japan, Seriatopora hystrix, a coral species locally extinct on the shallow reef, but abundant on

the upper mesophotic reef (40 m depth), had a four-month shorter reproductive season, a more

rapid settling time, and a smaller larval stage on the mesophotic reef (Prasetia et al. 2017). The

differences in reproductive biology suggested that the contribution of mesophotic S. hystrix to

the shallow reef is minimal, but could occur during a multi-step, multi-generation process, or

through random mixing events, such as tropical cyclones (Prasetia et al. 2017). Therefore,

mesophotic reefs are neither a universal refuge nor “de facto refugia” (Smith et al. 2016). Some

studies warn that deep reefs will not guarantee the protection and survival of shallow reefs. If

shallow reefs are heavily impacted, there is a limited amount of protection that deep reefs can

provide (Bongaerts et al. 2017). Knowledge of the species composition and the connectivity of

deep reefs in the NWHI is crucial to our understanding of the role of deep reefs as refugia.

The threat of climate change and coral reef bleaching events make it imperative to study

and understand coral reef ecosystems’ responses, and potential coral reef resilience and recovery.

Many locations that are currently biodiversity hotspots will not match up with future locations

that are suitable for coral reefs (Descombes et al. 2015). Research and monitoring efforts are

increasingly important to assess coral reef health as coral reefs decline globally (Hodgson 1999,

Hughes et al. 2003, Hoegh-Guldberg et al. 2007). Coral reef monitoring provides data that can

support effective management (Rogers et al. 1994). Percent cover of corals and composition of

fish species communities are two of the biological parameters that coral reef managers use to

measure the status and trends on coral reefs (Bay et al. 2001, Hill & Wilkinson 2004). Percent

cover of hermatypic, scleractinian coral is a well-known indicator of coral reef health because

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many organisms rely on hermatypic corals for their survival (Carpenter et al. 1981, Bell &

Galzin 1984, Sano et al. 1984). Certain obligate corallivores such as butterflyfishes (Hourigan et

al. 1988, Crosby & Reese 1996), can serve as indicator species for coral reef health. Numerous

studies have focused on the species composition, abundance, and health of shallow water coral

reef ecosystems in the Hawaiian Archipelago (Hixon & Brostoff 1983, Gulko et al. 2000, Tissot

& Hallacher 2003, Friedlander et al. 2009); however, much less is known about the deep reefs.

In a coral reef ecosystem, living corals provide habitat complexity, which can in turn

increase fish abundance and diversity (Carpenter et al. 1981). A high percentage of coral cover is

indicative of a relatively high degree of rugosity, as opposed to the relatively low rugosity of flat

sandy regions that do not provide fish assemblages with shelter (Roberts & Ormond 1987). In

structurally complex coral reef habitats, there are more crevices and spaces, resulting in greater

surface area for recruitment of coral and algae (Hixon 1991). Certain larval fish utilize coral as a

specific habitat for settlement (Sweatman 1988). Additionally, structurally complex reefs

provide habitat for invertebrates, which serve as a food source for many reef fishes. Certain

corals themselves are a food source for obligate corallivores (Parrish et al. 1985). The

implications for the relationship between habitat complexity and fish assemblages can be

substantial for conservation efforts. If we gain a better understanding of coral reef habitats, we

can better focus our efforts on choosing which marine areas are most critical for protection. The

present study aims to investigate percent cover, species richness, and species diversity in the

mesophotic reefs of the NWHI, and provide information that can be compared among

communities at different mesophotic locations. The prediction was that the mesophotic reefs 50

to 100 m deep in the NWHI would be similar to other mesophotic communities in the Caribbean

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and Great Barrier Reef where small Leptoseris coral colonies and crustose coralline algae

dominate the substratum.

Methods

The data for these studies were collected during research cruises to the NWHI between

2012 to 2016. All dives were conducted between 50 and 100 m, utilizing mixed-gas SCUBA and

closed-circuit rebreather apparatus. Dives were made at Nīhoa, Necker (Mokumanamana),

French Frigate Shoals (Lalo), Gardner Pinnacles (ʻŌnūnui/ʻŌnūiki), Maro Reef

(Kamokuokamohoali‘i), Laysan (Kamole), Lisianski (Kapou), Pearl and Hermes (Manawai),

Midway (Kuaihelani), and Kure (Hōlanikū). Divers photographed the benthos at one meter

intervals along a 25 m transect. Some of the photographs were taken using a 0.25 m2 quadrat with

camera attached (Preskitt et al. 2004); however, because of logistical issues related to the

bulkiness of the quadrat, the divers switched to using a pole-mounted camera

(monopod). Quality of the photographs and analysis of the photos were not impacted by the

mount-style of the camera. Divers captured 3,634 images and recorded the date, time, and depth

of each survey. When time permitted, the divers collected vouchers of macroalgae, sponges,

corals, and other invertebrates that could not be identified during the dives. These specimens

were put into separate bags, and preserved for identification by taxonomic experts.

For this study, images from Nihoa, French Frigate, Laysan, and Kure (Fig. 2) were

analyzed using Coral Net BETA, an open-source software program (coralnet@ucsd.edu). Fifty

random points were generated on each photograph of the substratum, and the organism under

each point was identified to the lowest taxonomic level possible (Fig. 3). Voucher specimens (if

available) were examined. Resources used for identification included Abbott (1999), Hoover

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(1999), Abbott and Huisman (2004), Huisman et al. (2007), and Wagner et al. (2016). The

photos were analyzed and percent cover of each taxon in each quadrat was determined. Average

percent cover of taxa was calculated for each atoll/island. Using data from the photoquadrats,

species richness (S), species diversity as H’= -pi(lnpi) using average percent coverage for each

taxon on an atoll, species evenness as J’= H’/lnS, and community percentage similarity were

determined for each atoll.

The Coefficient of Jaccard or Jaccard Index (Krebs 1999) was used to compare the

benthos of the four locations. The Jaccard Index is a binary similarity measure, expressed as:

Jaccard Index = c/a +b+c) x 100,

In which “c” is the number of the taxa in common, “a” is the number of taxa found at the first

location, and “b” is the number of taxa found only at the second location.

Results

Three hundred ninety-one photoquadrat images were examined in this study (Nihoa 155,

French Frigate Shoals 60, Laysan 57, and Kure 119) from a total of 23 transects (Nihoa 7, French

Frigate Shoals 8, Laysan 3, and Kure 5). Transect depth ranged from 43.9 m on Nihoa to 96 m

on Kure Atoll (Table 1).

Fifty-eight taxa (6 species of Chlorophyta (green macroalgae), 9 Phaeophyta (brown

macroalgae, 15 Rhodophyta (red macroalgae), 16 species of corals and 12 non-coral

invertebrates) were recorded in the mesophotic communities from 391 quadrats (Table 2). The

living benthic substratum was dominated by algal turf on hard substratum and crustose coralline

algae (CCA) on hard substratum (Fig. 4 and Appendix 1). However, each island or atoll had a

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different suite of top ten living space holders (Figs. 5, 6A--D). Leptoseris spp. corals were

among the top ten most abundant species in mesophotic communities at Kure. Algae (turf +

CCA + macroalgae) dominated themesophotic benthic substratum at Nihoa, French Frigate

Shoals, and Kure (Fig. 7). Coral species average cover was highest at Nihoa (Fig.7).

The total number of taxa (richness) ranged from 21 to 34 (Tables 2 and 3). The diversity

of living taxa was highest on French Frigate Shoals and lowest on Laysan (Table 3). Evenness

was equitable among all locations (Table 3) and ranged from 0.58 at Laysan to 0.71 at Nihoa.

The Jaccard Index showed that the percent similarity in mesophotic communities was

greatest between Kure and Laysan (44%) (Table 4). The smallest percent similarity was found

between the two atolls of French Frigate Shoals and Kure (29%).

Discussion

Low light levels are a defining environmental characteristic of the mesophotic zone. Only

1 to 2% of surface irradiation reaches 85 m deep at Penguin Bank off Moloka‘i, Hawai‘i (Norris

et al. 1995, Runcie et al. 2008) and only 0.01% of surface irradiance or about 0.0045 moles

photons/m2/day reaches the substratum at 201 m deep (Runcie et al. 2008). Values would be

similar in the mesophotic zone in the NWHI. Despite the mesophotic zone receiving a limited

amount of sunlight, substrata in the mesophotic zone are not barren, but rich in living organisms.

Corals, algae, and invertebrate species dominate this benthic environment. This study found that

algal turf composed of multiple species is the most abundant benthic entity in the NWHI

mesophotic community. Early studies of deep water macroalgae (Doty et al. 1974, Agegian &

Abbott 1985) also reported an abundant and diverse marine flora in the benthic mesophotic

community of the main Hawaiian Islands (MHI). Foliose, fleshy, and filamentous red, green,

and brown macroalgae, as well as crustose coralline algae, have been reported from the MHI at

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depths from 83 to 212 m (Kahng & Kelley 2007, Runcie et al. 2008, Rooney et al. 2010,

Spalding 2012, Spalding et al. 2016). The algal dominance of the mesophotic substratum in the

NWHI is similar to the findings of “algal dominated” reefs in the NWHI at shallower depths

(Vroom & Braun 2010).

Mesophotic coral ecosystems are recognized as important habitats for mesophotic reef

fish (Kane et al. 2014); however, in this study, herbivorous fish and urchins were scarce in the

photoquadrats despite the abundance of macroalgae. Natural chemicals or thallus toughness or

texture might make the mesophotic algae unpalatable to grazing fish or urchins. In the

Caribbean, algae below 30 m showed greater chemical defenses and herbivory was reduced (Hay

1981, 1997, Slattery & Lesser 2014). However, in feeding experiments on the coast of Hawai‘i

Island conducted in 10 m of water, turf algae collected from 40 m deep were readily eaten by

surgeonfish when translocated to shallow reefs, and both grazing time and grazing intensity were

significantly greater on the mesophotic turf samples than on shallow water turf samples (Kane et

al. 2020), suggesting that mesophotic turf algae are palatable. The paucity of herbivorous fish at

mesophotic depths may be a result of low light which reduces the visual acuity of herbivorous

fish (Kane et al. 2020) more than of piscivores. Kane et al. (2020) concluded that non-

consumptive predation risk was the most probable mechanism limiting herbivore distribution

with depth. Additionally, lower temperatures may constrain the digestion of algae by herbivorous

fish (Smith 2008, Clements et al. 2009), and could explain the lack of fish herbivores in the

mesophotic zone. Yet, thalli of mesophotic algae often display holes, e.g. Ulva and Umbraulva

species in the NWHI (Spalding et al. 2016). Perhaps mesograzers, such as gastropods and

amphipods are the major herbivores in the mesophotic.

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Could the largest marine herbivore in the Hawaiian Islands--green turtles--reach the

mesophotic benthos to graze? Rice & Balazs (2008) recorded the diving behavior of an adult

female and two adult male green turtles during their roundtrip breeding migration from Oahu, to

French Frigate Shoals in the NWHI. All three turtles exhibited biphasic diving behavior: diurnal

shallow (1 to 4 m deep), short (1 to 18 min) dives, but nocturnal deep diving with a mean

maximum dive depth of 35 to 55 m and a mean duration of 35 to 44 minutes. The adult female

made two dives in excess of 135 m and one male made several dives in excess of 100 m. Clearly,

these green turtles reached mesophotic depths, but whether foraging occurred is unknown.

This study did not find a high level of diversity at each island/atoll. Perhaps few species

are adapted to mesophotic conditions or the remoteness of the NWHI limits dispersal of species

to the mesophotic zone. In addition, the challenges involved in identifying organisms to species

level from photographs may account for the relatively low diversity indices. Taxonomic

categories were established, such as filamentous red, or green macroalgae when they could not

be identified to lower taxonomic groups without voucher specimens.

Further studies examining the algal turf communities at these depths would provide a

deeper understanding about species abundance and overall species diversity. A detailed,

quantitative study of algal turf communities in the shallow subtidal zones on Hawai‘i Island

displayed high species richness and diversity, new records of species, and patchy spatial

distribution of species even along individual transects (Stuercke & McDermid 2004). Collection

of turf samples would assist in being able to identify these species, because it is not possible to

confirm the identity of most turf species from photos alone. Accurate taxonomy of turf algae can

be achieved only through microscopic examination or DNA analysis.

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Leptoseris corals were expected to be prevalent at all of the sites; in fact, there were

Leptoseris spp. present at three of the four atolls, and Leptoseris hawaiiensis was among the top

ten species present at Kure. This finding supports previous ROV videos that showed Leptoseris

as an abundant taxon at mesophotic depths in the NWHI (Rooney et al. 2010). Although

Leptoseris was present, it was not the dominant space-holding species observed in studies in

other mesophotic zones in American Samoa (Bare et al. 2010), the Great Barrier Reef (Englebert

et al. 2014), and the MHI (Kahng & Maragos 2006, Rooney et al. 2010). In addition, Lepstoseris

colony sizes in the photoquadrats were small (8-25 cm. diam.), in comparison to the large

colonies (1 m and greater diam) of the mesophotic zone off Maui Nui, Hawai'i (Rooney et al.

2010). In the NWHI mesophotic depths, the water temperatures may be colder or the habitats are

less protected from oceanic swells, which is the case in mesophotic communities near

Maui. This study did not selectively investigate Leptoseris communities, but with more surveys

at many more sites it is possible that there could be Leptoseris present at all the sites in the

NWHI. Leptoseris cover and overall coral cover in the NWHI mesophotic benthic community is

lower than in other Pacific mesophotic reefs, perhaps because the Hawaiian Islands are

depauperate in coral species because of geographic isolation and cooler water temperatures.

Non-coral invertebrates were frequently seen in the photoquadrats, but because of their

small size the randomly generated points rarely encompassed invertebrates. Non-coral

invertebrates play an important role in coral reef communities and invertebrates in the benthic

communities, particularly in the NWHI, are understudied.

Expectations were that the northernmost atoll, Kure at 28.4 ०N latitude, and the

southernmost island in the NWHI, Nihoa at 23.1०N latitude, would host mesophotic communities

with the least similarity because of geographic distance. However, Kure and French Frigate

15

shoals were the most dissimilar. Kure and Laysan showed the greatest similarity perhaps

because the average depth of transects was deeper than the other two sites. The average depth of

the Nihoa transects was 57.12 m, French Frigate Shoals 66.88 m, Laysan 72.49 m, and Kure

90.66m. This study did not investigate the influence of depth among the sites, but a future

investigation could determine if variability in depth, irradiance, water temperature, water motion

(deep currents, swell exposure), and/or geomorphology (atoll vs. island, as well as more fine

scale heterogeneity in rugosity or slope) play a role in the community structure in the mesophotic

deep reef.

The mesophotic reefs at Johnston Atoll, 856 km upcurrent from the NWHI, showed high

percent cover of turf algae and low coral cover at most sites (Wagner et al. 2014), similar to the

results of the analysis of photoquadrats at Nihoa, French Frigate Shoals, and Laysan in this

study. Crustose coralline algae dominated the surveys at some sites in the mesophotic reefs at

Johnston, reminiscent of the results at Kure in this study. However, the overall mesophotic

macroalgal cover at Johnston Atoll is lower than in the mesophotic reefs in the NWHI. Johnston

Atoll seems to be a stepping stone for trans-Pacific dispersal to the Hawaiian Islands for fish

species, e.g. Hawaiian grouper; Acropora corals; vermetid gastropods; and perhaps marine

macroalgae via the Subtropical Countercurrent, an upper ocean current with maximum depth 300

m, and the Hawaiian Lee Countercurrent (Grigg 1981, Chu et al. 2002, Kobayashi

2006). Species with pelagic larval/spore/propagule durations or competency periods three

months or longer could be carried in these currents to the NWHI. Johnston Atoll’s total marine

algal flora stands at 191 species (Tsuda et al. 2010, Wagner et al. 2014) with 162 eukaryotic

algae, over 50% of which are found at French Frigate Shoals. Similar close taxonomic affinities

16

may also exist between the mesophotic benthic community at Johnston and the NWHI atolls to

the north and south of French Frigate Shoals.

This study establishes a baseline to detect future shifts in the deep reef benthic

community in the NWHI, particularly changes in the percent cover of corals and crustose

coralline algae in the face of climate change and ocean acidification. The impacts of ocean

acidification may be greater at depth because the aragonite saturation level is naturally lower in

deeper waters (Jiang et al. 2015).

This study highlights the importance of distinct deep water mesophotic communities.

Each island or atoll is home to a unique community of algae, coral, and non-coral invertebrates,

all of which may be critical to supporting the rich ichthyofauna in the mesophotic zone. Future

studies investigating the role of depth, currents, and latitudinal and longitudinal differences on

the community composition should be conducted to further understand these ecologically

important and unique environments.

17

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Table 1. Average depth of sites analyzed. Values in parentheses represent standard deviations. Site Average Depth (m)

Nihoa 57.12 (9.2)

French Frigate Shoals 66.88 (13.9)

Laysan 72.49 (18.6)

Kure 90.66 (8.3)

32

Table 2. Total number of taxa (richness) at each island or atoll location. Taxa that are present are represented with a “+”, taxa not represented are noted with a “-”

Taxa List

Nihoa French Frigate Shoals

Laysan Kure

Chlorophyta

Caulerpa sp. - - + -

Halimeda sp. + + + -

Microdictyon spp. + - + -

Ulva sp. + - - +

Macroalga filiform green + + + +

Green Macroalgae - - + +

Phaeophyta

Dictyota sp. - - - +

Feldmannia sp. - - - +

33

Lobophora variegata + - + +

Padina sp. - - + +

Sargassum sp. - - - +

Unidentified brown alga - - - +

Filamentous Brown +

+

Macroalga filiform brown + + - +

Lyngbya sp. + - - -

Rhodophyta

Amansia glomerata -

+ -

Amphiroa sp. - + - +

Asparagopsis sp. - + - -

Dichotomaria marginata + - - -

Dichotomaria sp. + - - -

Peyssonnelia sp. + - + +

34

Macroalga filiform red + +

+

Red Macroalgae + - - +

Crustose Coralline Algae (CCA) on hard substrate

+ + + +

CCA on rubble + + + +

Unknown + + + +

Filamentous filiform + + +

Filamentous macroalgae - - - +

Turf on hard substrate + + + +

Turf on rubble + + + +

Corals

Leptoseris hawaiiensis - + - +

Leptoseris sp. - - + +

Montipora capitata + + - -

Montipora patula + - - -

35

Porites evermanni - - - +

Pocillopora eydouxi - - - +

Pocillopora meandrina + - - +

Pocillopora damicornis + - - -

Pocillopora sp.

- - -

Porites brighami + - - -

Porites lobata + + - -

Porites lutea +

- -

Porites rus + + - -

Porites sp. - - + -

Black Coral - - - +

NonCoral Invertebrates

Anemone - - - +

Bryozoan - + + +

36

Diadema antillarum - - - +

Diadema sp. - - - +

Reteporellina denticulata + - - -

Hydroid/Bryozoan - + - -

Linckia sp. + - - -

Sponge + + + +

Orange Sponge - - + -

Red Sponge + - - +

Sarcothelia edmondsoni

- - +

Zoanthus sp. + - - -

37

Table 3. Data on total number of living taxa (S), taxa diversity( H’), and evenness (J’) for each. H’= -pi (ln pi) J’= H’/lnS values in parentheses represent standard deviations.

Community Indices

Nihoa French Frigate Shoals Laysan Kure

Taxa Richness (S)

34 23 21 34

Diversity (Shannon Wiener Index H’)

0.99

1.24 0.74 1.01

Evenness (J’)

0.71

0.68

0.58

0.62

Number of Quadrats 155 60 57 119

38

Table 4. Jaccard Index of Similarity for mesophotic communities in the NWHI from south to north. Numbers represent % similarity. Nihoa French Frigate Shoals Laysan Kure

Nihoa X 36 33 32

French Frigate Shoals 36 X 32 29

Laysan

33 32 X 44

Kure 32 29 44 X

39

Figure 1. Map of the Northwestern and Main Hawaiian Islands.

40

Figure 2. Location of four study sites.

41

Figure 3. This photoquadrat was taken at Kure from transect 2016060501, at a depth of 96m. Random circles were generated by the CoralNet software.

42

Figure 4. Taxa and their average percent cover at four islands/atolls in the NWHI.

Fig. 5. Mean percent cover of the most abundant taxa from all four sites combined.

43

Figure 6A. Mean percent cover of the top ten entities found at Nihoa. Error bars represent standard error of the mean.

Figure 6B. Mean percent cover of the top ten entities found at Laysan. Error bars represent standard error of the mean.

44

Figure 6C. Mean percent cover of the top ten entities found at French Frigate Shoals. Error bars represent standard error of the mean.

Figure 6D. Mean percent cover of the top ten entities found at Kure Atoll. Error bars represent standard error of the mean.

45

Fig. 7. Mean percent cover of coral, non-living entities, and algae on benthic substratum at the mesophotic sites surveyed at Nihoa, French Frigate Shoals, Laysan, and Kure. Error bars represent standard error of the mean.

46

Appendix 1.

Table 1. This table is a combined list of all species present among all the quadrats analyzed.

Nihoa French Frigate Shoals Laysan Kure

Avg % Cover

Standard Deviation

Standard Error

Avg % Cover

Standard Deviation

Standard Error

Avg % Cover

Standard Deviation

Standard Error

Avg % Cover

Standard Deviation

Standard Error

Chlorophyta

Caulerpa

0.035 0.00 0.00

Halimeda sp. 0.18 1.77 0.15 0.09 0.00 0.00 0.211 2.00 0.26

Microdictyon spp.

0.09 4.62 0.38 0.070 0.00 0.00 3.19 18.72 1.87

Ulva sp. 0.01 0.00 0.00

1.38 5.05 0.51

Macroalga filiform green

0.12 1.10 0.09 1.36 4.24 0.59 0.386 7.57 1.00 0.45 3.31 0.33

Green Macroalgae

0.035 0.00 0.00 0.07 1.15 0.12

Phaeophyta

Dictyota

0.02 0.00 0.00

Feldmannia sp.

2.76 0.00 0.00

Lobophora variegata

0.56 3.09 0.25 0.246 1.10 0.15 0.49 3.72 0.37

Padina sp.

0.035 0.00 0.00 0.66 11.08 1.11

47

Sargassum sp.

0.92 8.72 0.87

Brown Macroalgae

0.32 2.60 0.26

Filamentous Brown

0.02 2.31 0.19 14.63

2 26.88 3.56

0.00

Macroalga filiform brown

5.90 12.46 1.02 4.73 11.28 1.58 0.82 4.42 0.44

Lyngbya spp 0.26 22.63 1.85

Rhodophyta

Amansia glomerata

0.351 5.03 0.67

Amphiroa sp. 0.09 0.00 0.00

0.22 1.97 0.20

Asparagopsis sp. 0.55 0.00 0.00

0.00

Dichotomaria marginata

0.01 0.00 0.00

0.00

Dichotomaria sp. 0.01 0.00 0.00

0.00

Peyssonelia sp. 0.14 5.77 0.47 1.158 6.40 0.85 12.76 22.54 2.25

Macroalga filiform red

3.60 3.46 0.28 1.55 5.40 0.76 0.08 4.24 0.42

Red Macroalgae 0.04 0.00 0.00

0.29 3.63 0.36

CCA on hard substrate

12.62 10.95 0.90 8.91 9.41 1.32 0.737 3.69 0.49 33.33 26.23 2.62

CCA on rubble 0.12 3.79 0.31 3.45 6.49 0.91 0.596 2.73 0.36 14.82 28.65 2.86

Unknown 13.30 12.48 1.02 17.91 17.93 2.51 0.667 3.11 0.41 2.39 6.37 0.64

48

Filamentous filiform

0.03 0.00 0.00 1.09 8.49 1.19 13.158

22.86 3.03 0.00

Filamentous macroalgae

0.00

0.03 0.00 0.00

Turf on hard substrate

36.34 24.96 2.04 36.82 22.93 3.21 15.088

21.02 2.78 5.18 8.49 0.85

Turf on rubble 2.01 16.10 1.32 8.18 19.24 2.69 0.246 1.91 0.25 0.24 1.57 0.16

Corals

0.00

Leptoseris hawaiiensis

0.09 0.00 0.00

3.38 7.65 0.76

Leptoseris sp.

0.070 0.00 0.00 0.05 0.00 0.00

Montipora capitata

8.10 14.69 1.20 1.27 2.58 0.36

0.00

Montipora patula 1.79 15.93 1.30

0.00

Porites evermanni

0.02 0.00 0.00

Pocillopora eydouxi

0.03 0.00 0.00

Pocilliopora meandrina

0.35 8.88 0.73

0.03 0.00 0.00

Pocillopora damicornis

0.01 0.00 0.00

0.00

Pocillopora sp.

0.00

Porites brighami 0.22 5.87 0.48

0.00

Porites compressa

0.00

Porites lobata 1.65 8.58 0.70 0.36 0.00 0.00

0.00

49

Porites lutea 0.01 0.00 0.00

0.00

Porites rus 0.29 11.31 0.93 0.09 0.00 0.00

0.00

Porites sp.

0.035 0.00 0.00 0.00

Black Coral

0.02 0.00 0.00

NonCoral Invertebrates

0.00

Anemone

2.46 0.00 0.00

Bryzoan 1.36 10.58 1.48 0.035 0.00 0.00 7.03 24.60 2.46

Diadema antillarum

0.05 0.00 0.00

Diadema sp.

0.07 5.48 0.55

Reteporellina denticulata

0.06 1.00 0.08

0.00

Hydroid/Bryozoan

0.09 0.00 0.00

0.00

Linckia sp. 0.04 0.00 0.00

0.00

Sponge 0.03 0.00 0.00 0.09 0.00 0.00 0.105 0.00 0.00 0.72 2.53 0.25

Orange Sponge

0.035 0.00 0.00 0.00

Red Sponge 0.04 1.41 0.12

0.03 0.00 0.00

Sarcothelia edmondsoni

0.00 0.02 0.00 0.00

Zoanthus sp. 0.03 0.00

0.00

0.00

50

Other

0.00

0.00

Sand 13.68 15.10 1.24 5.91 9.73 1.36 47.965

40.00 5.30 10.10 11.06 1.11

Rubble 0.42 1.89 0.16 0.09 0.43 0.06 1.193 3.85 0.51 0.47 1.44 0.14