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Refugia in the ‘twilight zone’: discoveries from the Philippines

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Sonia J. Rowley at University of Hawaiʻi at Mānoa
Sonia J. Rowley
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Over the millennia, perpetual geological sea level changes have continuously shaped coral reef environments. Coral reef biodiversity, considered at its peak within the Coral Triangle, is most notable throughout the Philippine archipelago largely due to it having among the highest number of islands (more than 7,100) per geographical area. The origin of such diversity remains the subject of much controversy and investigation generating hypotheses of speciation and migration from within or outside the region. Coral reefs in the ‘twilight zone’ between 40 and 200 m are termed ‘mesophotic coral ecosystems’ (MCEs). MCEs are classified as conservation priority ecosystems (e.g. IUCN). Until recent technological advances, such mesophotic reefs were largely inaccessible. However, exploration using advanced closed-circuit rebreather technology has enabled us to penetrate the mysteries of these little-studied reefs. Here, as part of a collaborative research team, we aimed to discover, document and characterize mesophotic reefs within the Batangas region of the Philippines. The Marine Biologist: http://www.mba.ac.uk/refugia-‘twilight-zone’-discoveries-philippines
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Refugia in the ‘twilight
zone’: discoveries from
the Philippines
Over the millennia, perpetual
geological sea level changes have
continuously shaped coral reef
environments. Coral reef biodiversity,
considered at its peak within the Coral
Triangle, is most notable throughout
the Philippine archipelago largely
due to it having among the highest
number of islands (more than 7,100)
per geographical area. e origin of
such diversity remains the subject of
much controversy and investigation
generating hypotheses of speciation
and migration from within or outside
the region. Nevertheless, central to
determining reef biodiversity and bio-
geographical distributions are species
responses to environmental change,
particularly as human impacts acceler-
ate and/or exacerbate natural processes.
Coral reefs in the ‘twilight zone’
between 40 and 200 m are termed
‘mesophotic coral ecosystems’ (MCEs).
MCEs are classied as conservation
priority ecosystems (e.g. IUCN)
and posited to act as refugia against
environmental disturbances. Until
recent technological advances, such
mesophotic reefs were largely inacces-
sible or overlooked, being too precari-
ous for conventional SCUBA and too
shallow to justify the cost of a deep-sea
submersible. However, exploration
using advanced closed-circuit
rebreather technology
has enabled us
to penetrate
the mys-
teries
of
these little-studied reefs. Here, as part
of a collaborative research team sup-
ported by the Seaver Institute, our mis-
sion as the Bishop Museum rebreather
team was twofold: to test-pilot the
Poseidon next generation rebreather;
and to discover, document and
characterize mesophotic reefs within
the Batangas region of the Philippines.
Descending to depths unexplored,
away from the bustle of the shallows,
is not without risks. As inquisitive
explorers we are caught in peace and
exhilaration between the enticing
attenuation of the deep slope and the
mesophotic reef before us. To me these
reefs are akin to being transported back
in time. Not only do MCEs harbour
a myriad of new species, behaviours
and interactions just waiting to be
discovered, they also hold the keys to
questions of persistence, polyphyly,
and the evolution of structure–func-
tion relationships over geological
time. What fauna and even ora are
present, how do they survive, how
are they benecially connected to the
surrounding habitats if at all, and are
such patterns duplicated in other areas?
With the exception of reefs within
Hawai’i which are often dominated by
members of the zooxanthellate genus
Leptoseris, low-light habitats throughout
the Pacic are typically charac-
terized by gorgonian
sea fans, soft
corals,
sponges
and
As inquisitive explorers
we are caught in peace
and exhilaration
By Sonia J. Rowley
Spring 2014 | e Marine Biologist 19
Science letters
black corals, the majority of which are
unknown to science. e Philippines
are no exception; on this trip alone
we have discovered at least seven new
sh and 20 new gorgonian species at
depth, the latter providing substrate
for sh to lay their eggs. Our diving
experience tells us that it is at around
80 m depth that the temperature
drops, a shelf emerges, and where such
characteristic ‘twilight’ assemblages
begin to be found. Dynamic sea-level
changes produce extreme variations in
shallow water habitats of up to 80–100
m, with these deeper reefs remaining
relatively unchanged, and less than
50% species overlap with shallow taxa.
erefore, gorgonian corals and reef
sh are key taxonomic groups within
deep-reefs with some taxa spanning
considerable depths (e.g. 5–2,000 m).
At depths greater than 100 m we
work against time, determined by the
ratio between the saturation of our
mortal tissue with dissolved gas and
the safety gas that we carry. Yet no
part of what we encounter is lost; all
digital imagery is synchronized with
the rebreathers’ advanced electronics,
capturing time, depth and specimen
information. I continue to collect
gorgonians as we ascend—intrigued by
their dynamic patterns of diversity with
depth. e swim bladders of sampled
sh are vented with needles as we
ascend (the notorious ‘Pyle’ stop). At
the surface, specimens are catalogued
and preserved, whilst digital imagery is
systematically documented for immedi-
ate dissemination in the web-based
archive Explorers Log. e discovery
of the twilight zone is not exclusive—
everyone can immediately enjoy!
Are shallow reefs being seeded by
deep reefs? Are certain taxa habitat spe-
cialists or bathymetric migrators? ese
questions remain to be elucidated,
but when they are, key evolutionary
mechanisms facilitating survival over
geological time will undoubtedly be
unveiled. So even though as humans
we are challenged to save habitats
from their ongoing destruction,
‘twilight’ reefs of refugia may likely
replenish many of their inhabitants.
Dr. Sonia Rowley (soniajrowley@
gmail.com) is an invertebrate
zoologist at the Bernice Pauahi
Bishop Museum, and the University
of Hawai’i, USA.
Funding and collaborations:
Bernice Pauahi Bishop Museum,
Hawai’i, USA; Hawai’i Institute of
Marine Biology, Hawai’i, USA
California Academy of Sciences,
California, USA; Seaver Institute,
California, USA
Images: Opposite: A typical mesophotic
assemblage from the Solomon Islands with
the deep-reef Griffis’ Angelfish Apolem-
ichthys griffisi. Carlson & Taylor 1981. This
page, from top left: Chromis n. sp.. Plectran-
thias n.sp.. Dr. Luiz Rocha with the pinecone
fish Monocentris sp.. Mesophotic reefs of
gorgonians in the Philippines. Mesophotic
reefs of gorgonians in Fiji. Dr. Brian Bowen.
The PI team: Brian Greene, David Pence,
Dr. Richard Pyle, Joshua Copus, Dr. Sonia
Rowley, Robert Whitton, with Poseidon
prototypes and Inspiration Rebreathers.
... Prior to the introduction of this term, this habitat had been referred to as deep outer reefs, deep-water reefs, the coral reef twilight zone, twilight reefs, or simply deep coral reefs. The reference to the twilight zone, first insinuated by Starck and Starck (1972) and later adopted by others (e.g., Fricke and Knauer 1986;Schlichter et al. 1986;Fricke et al. 1987;Pyle 1992aPyle , 1996aPyle , b, 1998Brokovich 2008;Brokovich et al. 2008;Weinstein et al. 2011Weinstein et al. , 2015Rowley 2014;Tornabene et al. 2016a;Weiss 2017a), is particularly apt in that it references the attenuating light levels across this depth range while simultaneously alluding to the mysterious and largely undocumented nature of the habitat. However, besides this term being associated with the iconic American television series (Stanyard 2007), it has been used to describe other light-transition zones, including terrestrial cave environments (Northup and Welbourn 1997) and deeper portions of the pelagic realm (Earle 1992;Cameron 2018). ...
... Perhaps the most frequently debated topic involving conservation and MCEs is the question of whether MCEs can act as refugia for shallow coral reefs (Glynn 1996;Bongaerts et al. 2010Bongaerts et al. , 2017Hickerson et al. 2012;Bridge et al. 2013;Rowley 2014;Smith et al. 2014;Holstein et al. 2015;Lindfield et al. 2014Lindfield et al. , 2016Laverick et al. 2016Laverick et al. , 2019MacDonald et al. 2016;Smith et al. 2016;Semmler et al. 2017;Bongaerts and Smith 2019;Shlesinger et al. 2019). ...
Mesophotic Coral Ecosystems: Introduction and Overview
Chapter
Full-text available
  • May 2019
Although the existence of zooxanthellate corals in mesophotic coral ecosystems (MCEs; light-dependent coral ecosystems from 30 to 150 m in depth) has been known since the nineteenth century and focused scientific exploration of MCEs began over 50 years ago, more than 70% of all research on MCEs has been published only within the past seven years. MCEs represent approximately 80% of potential coral reef habitat worldwide, yet very little is known about them in comparison to shallow reefs. Many MCE species new to science have been discovered in the past decade, and many more await discovery. The term MCEs has been widely adopted by the scientific community since its 2008 inception; however, there is considerable inconsistency in how it is subdivided into “upper” and “lower” (and sometimes “middle”) zones. Moreover, doing so may lead to artificial boundaries when habitats and ecological communities at different depth zones may blend together. Growing evidence suggests that MCEs harbor proportionally more geographically endemic species than their shallow-water counterparts, and initial indications are that major biogeographic patterns described for shallow reef organisms may not apply to MCEs. Although MCEs may serve as refugia for some shallow species, they are increasingly recognized as unique ecosystems, important in their own right. Future research on MCEs should aim to address gaps in our understanding of the basic physical and biological characteristics of MCEs including geography, taxonomic composition, depth distribution, ecology, physiology, and connectivity. Improving knowledge of MCEs would benefit from combining different technologies to leverage the strengths of each.
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... Istotne znaczenie ma również nieinwazyjne oddziaływanie takich badań na środowisko przyrodnicze, gdzie nie dochodzi do przypadkowego niszczenia biocenoz. Co więcej, już sama obserwacja obiektu pod powierzchnią wody może przynieść wartościowe dane naukowe [1,7]. Ponadto istnieją zjawiska przyrodnicze czy organizmy, które są niemożliwe do obserwacji i zidentyfikowania bez udziału płetwonurka, np.: ryby raf koralowych. ...
... The noninvasive impact of such research on the natural environment is also important, as such methods greatly limit the accidental destruction of biocenoses. What's more, the very observation of the object under the surface of the water can bring valuable scientific data [1,7]. In addition, there are natural phenomena or organisms that are impossible to observe and identify without the participation of a diver, e.g. ...
Scientific diving in natural sciences
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  • Dec 2018
Scientific diving is increasingly being used for numerous studies. Moreover, this form of diving allows for the conduction of interdisciplinary research. The current nomenclature of this type of dive is defined as scuba diving to collect information to support science by using diving techniques. Underwater research is particularly important in the natural sciences where it allows for the non-invasive observations of fauna and flora of aquatic ecosystems in their natural environment. At the same time, the use of diving for scientific purposes avoids mistakes made in random sampling, which is related to the use of classical sampling methods. As a result, such diving is crucial in systematic, ecological and behavioural analysis. Nevertheless, dive techniques, however versatile, require optimisation, separate study and systematisation, depending on the type of research conducted. This article is an attempt to present an outline of the topic, to systematise basic concepts in presenting the principles of legal regulations in Poland and abroad..
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... 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 communities, as well as their connectivity with shallow reefs, are just beginning to be explored. ...
... 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. ...
A comprehensive investigation of mesophotic coral ecosystems in the Hawaiian Archipelago
Article
Full-text available
  • Oct 2016
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 km2 in 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 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.
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... However, technological advances in both smaller, remotely operated submersibles (ROVs) (Fricke and Knauer, 1986;Stewart and Auster, 1989;Love et al., 1994;Lindsay et al., 2012), and in rebreather diving equipment (Stone, 1990;Pyle, 1999Pyle, , 2000, have allowed exploration of these mesophotic ecosystems to expand greatly in scale and frequency. Research in these ecosystems have yielded important new discoveries about marine biodiversity (Erdmann et al., 1998;Pyle, 2000;Kane et al., 2014;Rowley, 2014;Kosaki et al., 2017). However, as seen from both shallow-water and deep-sea work, studies on understudied, or so-called "minor taxa", have lagged. ...
Exploring the Biodiversity of Understudied Benthic Taxa at Mesophotic and Deeper Depths: Examples From the Order Zoantharia (Anthozoa: Hexacorallia)
Article
Full-text available
  • Jun 2019
Research on so-called “minor taxa” at mesophotic depths has lagged behind that of more commonly researched groups such as fish or hard corals. Exemplar taxa include species of the order Zoantharia, benthic colonial anemones that are cosmopolitan in distribution but understudied in many ecoregion and ecosystems. In this study, we examine the results of rare mesophotic to deep sea surveys (one rebreather, one remotely operated submersible (ROV) + net survey, two ROV surveys) from Japan and Israel. We examined the collected images and video data to provide a first estimate of Zoantharia diversity at mesophotic depths. Zoantharians were observed in all surveys, indicating their ubiquitous presence in mesophotic and deeper ecosystems. Additionally, specimens (n = 12) acquired via these surveys were phylogenetically analyzed with three DNA markers. Phylogenetic results showed the presence of undescribed species based on the uniqueness of acquired DNA sequences, including one specimen belonging to the family Abyssoanthidae, previously only reported from depths below 2000 m. Other specimens belong to groups that inhabit shallower and deeper depths (Antipathozoanthus, Epizoanthus, and Parazoanthidae). These results depart from surveys of mesophotic coral ecosystem fishes and crustaceans, which indicate affiliations almost exclusively with shallow genera and families. We hypothesize that mesophotic depths are an ecotone for zoantharian diversity, with links to both deeper and shallower ecosystem diversity. Future surveys in mesophotic depths should incorporate phylogenetic methods to better catalog so-called “minor taxa” (not only including Zoantharia) and enhance the scientific foundation for conserving the biodiversity of these threatened ecosystems.
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... An effective technique for safe and efficient data gathering is to develop simple routines that can be repeated multiple times during a dive. For example, when collecting gorgonian specimens from MCEs, Sonia Rowley has implemented an efficient protocol: she identifies the target specimen, takes a photograph of the gorgonian in situ, collects a sample and places it in a prenumbered bag, and photographs the rebreather computer display to document the environmental parameters (Rowley 2014). Such carefully designed protocols both maximize the efficiency of data collection and ensure the integrity of the collected data. ...
Advanced Technical Diving
Chapter
Full-text available
  • May 2019
Effective exploration of mesophotic coral ecosystems (MCEs) has been limited primarily by available technology. Although research targeting MCEs led to the development of the first electronically controlled, closed-circuit rebreather in the late 1960s to the early 1970s, it wasn’t until the 1990s that the technology was utilized extensively for MCE research. Over the years, diving techniques and technologies have gradually advanced from conventional SCUBA to open-circuit, mixed-gas diving to closed-circuit rebreathers, each progressively increasing diver safety and bottom time at depth. Over the past decade, the application of closed-circuit rebreathers for use in MCE research has increased dramatically, enabling research activities that are impractical or impossible using other technologies. When conducting advanced diving operations to study MCEs, many logistical and practical considerations must be taken into account. Trained and experienced divers and support personnel are required and must have access to appropriate equipment. Contingencies both during dives (e.g., bailout options) and in response to emergencies must be clearly defined and understood. Insights and guidelines for conducting MCE research using rebreathers are recommended based on over three decades of field experience. As scientific diving programs at more institutions continue to establish support for advanced technical diving operations, the application of this approach to MCE research will help scientists conduct work efficiently and safely.
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... & Sonia J. Rowley srowley@hawaii.edu Gorgonian corals (Cnidaria: Anthozoa: Octocorallia) are conspicuous, diverse and often dominant components of benthic marine environments, notably tropical shallow reefs, deep-sea habitats and mesophotic habitats (Cerrano et al. 2010;Rowley 2014b;Sánchez 2016). Numerous gorgonians are conservation 'flagship' species (e.g., Eunicella verrucosa Pallas, 1766;Tinsley 2005, Paramuricea clavata Risso, 1826; Linares et al. 2008a;Cerrano et al. 2010), being ecologically diverse, long-lived engineering taxa that maintain habitat heterogeneity and provide secondary space to other organisms (Buhl-Mortensen et al. 2010). ...
Environmental gradients structure gorgonian assemblages on coral reefs in SE Sulawesi, Indonesia
Article
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  • Jun 2018
  • CORAL REEFS
Indonesian coral reefs are the epicenter of marine biodiversity, yet are under rapid anthropogenically induced decline. Therefore, ecological monitoring of high diversity taxa is paramount to facilitate effective management and conservation. This study presents an initial report from a comprehensive survey of shallow-water (0–15 m) gorgonian assemblage composition and structure across sites with varying habitat quality within the Wakatobi Marine National Park (WMNP), SE Sulawesi, Indonesia. Current estimates of over 90 morphospecies from 38 genera and 12 families within the calcaxonian, holaxonian and scleraxonian groups are reported. This extensive survey confirms high local gorgonian abundance, diversity and species richness in the absence of anthropogenic influence and increasing with depth. Notably, morphological variants of the zooxanthellate species Isis hippuris Linnaeus, 1758, and Briareum Blainville, 1830, drive site and habitat assemblage differences across environmental gradients. Azooxanthellate taxa, particularly within the Plexauridae, drive species richness and diversity with depth. Of the 14 predictor variables measured, benthic characteristics, water flow and natural light explained just 30% of gorgonian assemblage structure. Furthermore, zooxanthellate and azooxanthellate taxa partitioned distinct gorgonian communities into two trophic groups—autotrophs and heterotrophs, respectively—with contrasting diversity and abundance patterns within and between study sites. This study strongly supports the WMNP as an area of high regional gorgonian abundance and diversity. Varying ecological patterns across environmental clines can provide the foundation for future research and conservation management strategies in some of the most biodiverse marine ecosystems in the world.
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... It is not the purpose of this paper to provide a full list of all the studies that have employed CCRs, but many applications exists in behavioural sciences such as: Collette (1996) looking at fish behaviour; Lobel (2009) studying underwater acoustic ecology; and Tomoleoni et al. (2012) and Tinker et al. (2007) who used CCRs to facilitate the capture or recapture of sea otters. Moreover, Hinderstein et al. (2010), Sherman et al. (2009) and Rowley (2014 used the advantages provided by CCR deep mixedgas diving to study mesophotic coral ecosystems. ...
The closed circuit rebreather (CCR): Is it the safest device for deep scientific diving?
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Full-text available
  • Nov 2016
The closed circuit rebreather (CCR) is not a new diving technology. From the late 1990s CCR units were commercially available in Europe, and increasingly more divers, and among them scientific divers, have been trained to use them. Even if many benefits exist for using CCR for all diving depth ranges, it is in the deep diving zone ranging from 50 m to 100 m of sea water where the main advantages to using this equipment exist. Using rebreathers does carry additional risks, and these must be mitigated to ensure safe usage. A standard for CCR scientific diving has existed for many years in the USA, and the levels of expertise within the European scientific diving community are now sufficient for a European standard to be established. National legislation for occupational scientific diving in many cases excludes CCR diving, which can limit its use for scientific purposes. This paper suggests that, where possible, legislations should be allowed to evolve in order to include this type of equipment where and when its use has direct advantages for both the safety and the efficiency of scientific diving. This paper provides a brief description of the fundamentals of closed circuit rebreather diving and outlines the benefits that its use offers diving scientists. Special attention is given to safety issues with the assertion that the CCR concept is, if strictly applied, the safest available technique today for autonomous deep scientific diving purposes. © 2016, Society for Underwater Technology. All rights reserved.
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The Hawaiian Archipelago
Chapter
Full-text available
  • May 2019
The Hawaiian Archipelago is one of the largest and most isolated island chains in the world, and its marine ecosystems are well-studied. Research on Hawaiian mesophotic coral ecosystems (MCEs) began in the 1960s and has intensified during the past decade. In Hawai‘i, rich communities of macroalgae, corals and other invertebrates, and fishes inhabit MCEs and are associated with increased water clarity and decreasing average current strength with depth. Extensive calcified and fleshy macroalgal beds are found both in discrete patches, dense beds, and meadows over both hard and soft substrates. Several species of corals typical of shallow reefs extend to depths of ~60 m. The dominant corals below 60 m are in the genus Leptoseris, which can form extensive coral reefs spanning tens of km². Few octocoral species inhabit shallow reefs and upper MCEs (30–70 m) but are diverse at the deepest range of MCEs (>130 m). Sponges do not represent a major structural component of MCEs. Many species of fishes occur on both shallow reefs and MCEs, but MCEs harbor more endemic species (up to 100% endemism). Several new species of macroalgae, corals and other invertebrates, and fishes have recently been documented. Over 60% of the territorial waters surrounding the archipelago are protected as the Papahānaumokuākea Marine National Monument; however, no specific protections exist for MCEs. Generally, threats affecting Hawai‘i’s shallow reefs also affect MCEs to varying degrees. MCEs may be more insulated from some threats but more vulnerable than shallow reefs to others (e.g., water clarity).
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