Download COMMENSALISM AND REPRODUCTIVE BIOLOGY OF THE

COMMENSALISM AND REPRODUCTIVE BIOLOGY OF THE BRITTLE
STAR OPHIOCREAS OEDIPUS ASSOCIATED WITH THE OCTOCORAL
METALLOGORGIA MELANOTRICHOS ON THE NEW ENGLAND AND
CORNER RISE SEAMOUNTS
By
Celeste V. Mosher
B.S. University of the Virgin Islands, 2002
A THESIS
Submitted in Partial Fulfillment of the
Requirements for the Degree of
Master of Science
(in Oceanography)
The Graduate School
University of Maine
August, 2008
Advisory Committee:
Les Watling, Professor of Oceanography, Advisor
Pete Jumars, Professor of Marine Sciences and Oceanography
Kevin J. Eckelbarger, Professor of Marine Sciences
©2008 Celeste V.Mosher
All Rights Reserved
COMMENSALISM AND REPRODUCTIVE BIOLOGY OF THE BRITTLE
STAR OPHIOCREAS OEDIPUS ASSOCIATED WITH THE OCTOCORAL
METALLOGORGIA MELANOTRICHOS ON THE NEW ENGLAND AND
CORNER RISE SEAMOUNTS
By Celeste V. Mosher
Thesis Advisor: Dr. Les Watling
An Abstract of the Thesis Presented
in Partial Fulfillment of the Requirements for the
Degree of Master of Science
(in Oceanography)
August, 2008
While temperate-water coral ecosystems of seamounts have been gaining more
attention in the last decade, the organisms that live within and rely upon these corals for
survival are studied to a lesser degree. Throughout the New England and Corner Rise
seamounts of the western North Atlantic, several ophiuroid species are conspicuously
epizoic on octocorals. One objective of this study was to investigate the association
between Ophiocreas oedipus and its host octocoral Metallogorgia melanotrichos on these
seamounts. Coral colonies with their brittlestar epibionts were collected from 11
seamounts in 2003, 2004, and 2005 at depths between 1300 and 2200 m via submersible.
O. oedipus is obligately associated with M. melanotrichos, leading a solitary existence on
all octocorals observed. O. oedipus gains feeding and protective benefits while M.
melanotrichos appears to neither benefit nor be disadvantaged by this commensalism. M.
melanotrichos exhibits a distinct developmental pattern that can be categorized into three
growth stages. The positive correlation between size of O. oedipus and growth stage of
its host is highly significant suggesting the brittlestar may grow up with M.
melanotrichos. A further objective of this study was to investigate the reproductive
biology of O. oedipus. Paraffin histology reveals that O. oedipus is gonochoristic and
likely a broadcast spawner with a lecithotrophic larval stage. The gonadal tubules of O.
oedipus occur in pairs of up to four within the proximal arm segments of each arm. The
tubules exhibit synchronous gametogenesis within each pair but asynchronous
development between pairs within the same individual. Findings suggest O. oedipus may
use continuous reproduction throughout the year to maintain its population while limited
by its dependence on M. melanotrichos as a host.
ACKNOWLEDGEMENTS
I would like to thank Les Watling for the opportunity to immerse myself in this
fascinating research, for his advisory contributions, and for his contagious excitement
with all things related to this subject. I cannot thank enough the members of my advisory
committee, Pete Jumars and Kevin Eckelbarger, for their helpful comments and
intriguing discussion. I am grateful to Scott France of the University of Louisiana,
Lafayette, for confirming through genetic analysis the hypothesis that the three growth
stages of M. melanotrichos are indeed the same species, and to Walter Cho of Woods
Hole Oceanographic Institution who provided further molecular insight.
I am indebted
to Tim O'Hara of the Museum Victoria, Melbourne, and Isaac Smirnov of the Zoological
Institute of the Russian Academy of Sciences, St. Petersburg, for their species
identifications of the octocoral-associated brittle star Ophiocreas oedipus. Much
appreciation goes to the graduate students, faculty, and staff of the Darling Marine
Center, without whom this research would have been unsuccessful, and especially to my
fellow lab members, Anne Simpson and Mateja Nenadovic, who were of great help and
continuously supportive. I would like to thank Sheryl Mosher, Nye Mosher, Michelle
Mosher, and Torren Nehrboss for supporting me in my endeavors, past and present.
Finally, I am forever grateful to Jason Nehrboss for his technical assistance, unending
patience, and loving inspiration.
This research was funded by a NOAA Ocean Exploration grant to Les Watling
and research and teaching fellowships from the University of Maine's School of Marine
Sciences.
iii
TABLE OF CONTENTS
ACKNOWLEDGEMENTS
iii
LIST OF TABLES
vi
LIST OF FIGURES
vii
Chapter
1.
INTRODUCTION
1
2.
MATERIALS AND METHODS
5
Study and Collection Site
5
Sample Treatment
7
Commensalism
8
Reproductive Biology
9
3.
RESULTS
11
Growth stages of Metallogorgia melanotrichos
11
Association between Metallogorgia melanotrichos and
4.
Ophiocreas oedipus
13
Predation on Ophiocreas oedipus
15
Ophiocreas oedipus reproductive biology
15
DISCUSSION
21
Commensalism of Ophiocreas oedipus on
Metallogorgia melanotrichos
21
Reproduction in Ophiocreas oedipus
25
iv
REFERENCES
29
BIOGRAPHY OF THE AUTHOR
33
V
LIST OF TABLES
Table 1.
Sampling and morphological data for Metallogorgia melanotrichos hosts
and Ophiocreas oedipus commensals
Table 2.
6
Ophiocreas oedipus estimated fecundity and egg sizes per
gonadal tubule
19
VI
LIST OF FIGURES
Figure 1.
Bathymetric map of the New England and Corner Rise seamounts, NW
Atlantic
5
Figure 2.
Growth stages of Metallogorgia melanotrichos
Figure 3.
Ophiocreas oedipus disc diameters of individuals residing in the three
12
growth stages of M. melanotrichos hosts
14
Figure 4.
Ophiocreas oedipus gonad morphology
17
Figure 5.
Change in gonadal tubule morphology of Ophiocreas oedipus as disc
diameter increases
Figure 6.
18
Transverse histological sections of gonadal tubules of
Ophiocreas oedipus
20
vn
Chapter 1
INTRODUCTION
In the face of habitat destruction by ever more intensive and deeper fishing
methods as well as chemical and thermal changes caused by rising atmospheric C0 2
levels, deep-sea coral communities are in increasing danger of being damaged or
destroyed (Auster et al. 1996; Auster et al. 1998; Koslow et al. 2001; Fossa et al. 2002;
Hall-Spencer et al. 2007; Clark and Koslow 2007; Probert et al 2007; Waller et al. 2007).
Deep-sea organisms have been proposed as important bio-indicators of climate change
(Guinotte et al. 2003; Danovaro et al. 2004; Barnett et al. 2005) and as sources of natural
products for pharmaceuticals (Faulkner 2001). Seamount communities in particular have
been characterized as sites of higher endemism (de Forges et al. 2000; Stone et al. 2004),
possible hot spots of biodiversity (Worm et al 2003; Samadi et al 2006), and areas of
higher productivity (Genin 2004; Samadi et al 2006). Such characterizations imply that
these communities may be at an elevated risk of ecological damage and perhaps,
extinction events.
While cold-water coral communities of deep seamounts have been gaining more
attention in the last decade, the organisms that live within and rely upon these corals for
survival are studied to a lesser degree. Many of the "associates" hosted by the octocorals
are thought to live symbiotically upon their hosts either as commensals or as parasites
(Buhl-Mortensen and Mortensen 2004). For example, of the known symbiotic
associations on deep-sea cnidarian taxa, Buhl-Mortensen and Mortensen estimate that
35% are obligately associated with their hosts. Obligate coral symbionts are even more
1
at risk than other associates as they depend on their hosts for survival (Buhl-Mortensen
and Mortensen 2004), but the degree to which associates rely on their hosts is relatively
unstudied for most seamount symbioses. Although conservation efforts are underway,
more progress is needed towards the protection of seamount ecosystems (reviewed in
Probert et al 2007). It is especially crucial to assess the interspecific relationships of
these octocoral associations.
Echinoderms dominate the non-sessile megafauna in the deep-sea (Gage and
Tyler 1991). Throughout the New England and Corner Rise seamounts of the North
Atlantic, several ophiuroid species are conspicuously epizoic on the octocoral
assemblage. The prominence of organisms perched in arborescent corals has been related
to food availability (Gage and Tyler 1991). Particulate matter is resuspended from the
bottom within the benthic boundary layer (Jumars and Nowell 1984) and corals tend to
align perpendicular to the prevailing current, providing food for the suspension-feeding
corals themselves and also their symbionts. Climbing a small distance above the bottom
provides access to higher fluxes because any decrease in suspended particle concentration
is generally more than offset by the steep velocity gradient in the lowermost bottom
boundary layer. There are likely further benefits to the organisms that reside in coral
hosts, such as protection from predators and/or increased gamete dispersal for freespawning species.
Asteroschematid brittle stars (Ophiuroidea: Euryalida) are one of the least studied
families of ophiuroids, likely because most known species occur in the deep sea. Many
are found associated with colonial cnidarians. There have been some studies of the
feeding characteristics and basic biology of asteroschematid species (Stewart and
2
Miadenov 1997, Grange 1991, Fujita and Ohta 1988, Emson and Woodley 1987, Hendler
and Miller 1984) yet the ecological dynamics of brittle star-host associations within the
family are poorly known. Brittle star host fidelity ranges from specific to a single host
species in a particular geographic location (Grange 1991, Emson and Woodley 1987) to
occurrence on many different coral species (pers. obs.). The only asteroschematid
association studied in detail is that of Astrobrachion constrictum, a euryalid living in
association with a gorgonian in the fjords of New Zealand (Grange 1991, Stewart and
Miadenov 1997, Stewart 1998). A. constrictum is an asteroschematid species found at
SCUBA-accessible depths. The New Zealand fjords, however, are subject to diel cycles
of light penetration and nutrient-rich run-off, neither of which is found in the more stable
environment of the deep-sea. A. constrictum lives upon an antipatharian octocoral,
Antipathes fiordensis, in what has been described as an obligate symbiosis (Grange
1991). They appear to remain on their hosts year after year and, when transplanted from
their perches in A. fiordensis. to the seabed, individuals will rapidly find the nearest A.
fiordensis and climb up the colony (Stewart and Miadenov 1997). Other arborescent
features and protective niches are apparently not deemed suitable. In addition, there
appear to be elements of mutualism (Grange 1991) as the host coral is cleaned by the
brittle star that feeds on the detritus settled onto its branches.
The asteroschematid ophiuroid Ophiocreas oedipus Lyman, 1879, has been found
on the octocoral Metallogorgia melanotrichos Wright and Studer, 1889, on the New
England and Corner Rise seamounts. The major objective of this study is to begin a basic
investigation of this association and the biology of the two species. It is hypothesized
3
that the brittle star settles onto the young M. melanotrichos and the two species then grow
up and live together their entire lives.
As part of this study, the reproductive biology of O. oedipus was also examined.
While studies of reproductive periodicity and general anatomical structure have been
conducted on the shallow water A. constrictum (Stewart and Mladenov 1994, 1995),
similar research has not been conducted on deep-sea asteroschematids. We know
characteristics of the reproductive biology of some deep-sea ophiuroids collected from
muddy bottom, bathyal and abyssal regions (Tyler and Gage 1980, Sumida et al 2000,
Gage et al 2004), however these species represent much more distant taxonomic groups.
4
Chapter 2
MATERIALS AND METHODS
Study and Collection Site
The New England Seamounts form a chain from New England, USA, extending
from Bear Seamount (located at approximately 39°50 N, 67°20 W) southeasterly to
Nashville Seamount (34°30 N, 56°50 W). The Corner Rise complex clusters around 34°
N,49° W (Figure 1). The summits of these undersea mountains range from ~1.3 to 3.5
km water depth. Temperatures at these depths fall between 3°C and 4°C.
New England and Corner Rise Seamounts
Figure 1 Bathymetric map of the New England and Corner Rise seamounts, NWAtlantic.
As part of the NOAA Ocean Exploration program, research cruises to the Corner
Rise and New England seamounts were conducted in July 2003, May 2004, August 2005,
and October 2005. The submersible Alvin and support ship Atlantis was used in 2003 and
during the October cruise of 2005. The ROV Hercules was deployed from the NOAA
5
ship Ronald H. Brown in 2004 and August 2005. Sixty-six coral colonies were collected
at depths between 1300 and 2200 m from 13 seamounts in the New England and Corner
Rise chains (Table 1). In addition, over 500 h of video and -30,000 high-definition
frame-grabs taken during the submersible and ROV dives were used to supplement the
other data for this study.
Table 1 Sampling and morphological data for Metallogorgia melanotrichos hosts and
Ophiocreas oedipus commensals. (NES = New England seamounts, CRS = Corner Rise
seamounts, DD = disc diameter)
Specimen Collection
ID
BAL101
BAL107-1
BAL107-2
BAL107-3
BAL110-2
BAL208-2
BAL210-1
BEA401-2
BEA506-1
MIL103-2
MIL105-1
GOO103-1
GOO106-1
GOO107-1
GOO109-1
KUK209-1
KEL103-1
KEL107-1
KEL201-2
KEL203-3
KEL301-2
KEL301-3
KEL301-4
KEL607-1
KEL610-1
MAN 706-2
MAN 710-1
date
5/21/04
5/22/04
5/22/04
5/22/04
5/22/04
9/2/05
9/2/05
5/11/04
5/12/04
8/17/05
8/17/05
8/20/05
8/21/05
8/21/05
8/21/05
8/22/05
7/15/03
7/15/03
7/16/03
7/16/03
5/18/04
5/18/04
5/18/04
8/31/05
9/1/05
5/15/04
5/15/04
Seamount
Lattitude
N
Balanus, NES
39°21.30
Balanus, NES
39°21.51
Balanus, NES
39°21.51
Balanus, NES
39°21.51
39°22.30
Balanus, NES
39°24.88
Balanus, NES
Balanus, NES
39°24.88
Bear, NES
39°57.10
Bear, NES
39°53.02
Caloosahatchee, CRS 34°48.92
Caloosahatchee, CRS 34°48.91
Corner, CRS
35°23.61
Corner, CRS
35°23.59
Corner, CRS
35°23.58
Corner, CRS
35°23.57
Corner, CRS
35°33.40
Kelvin, NES
38°47.33
Kelvin, NES
38°47.31
Kelvin, NES
38°51.60
Kelvin, NES
38°51.51
Kelvin, NES
38°49.20
Kelvin, NES
38°49.20
Kelvin, NES
38°49.20
Kelvin, NES
38°45.88
Kelvin, NES
38°45.92
Manning, NES
38°08.93
Manning, NES
38°08.78
6
Longitude> Depth
i M. melanotrichos 0. oedipus
W
(m)
growth stage
DD (mm)
65°21.52 1912 3
65°21.82 1767 3
65°21.82 1767 3
65°21.81 1767 3
65°22.31 1562 1
65°24.66 1802 2
65°24.56 1717 3
67°24.60 1559 1
67°28.32 1491 2
50°30.35 1601 3
50°30.36 1592 3
51°15.93 2135 2
51°15.99 2082 3
51°16.00 2076 2
51°16.05 2051 3
51°48.89 1829 3
64°07.91 2029 3
64°07.83 1949 1
63°54.85 2173 3
63°54.85 2047 3
63°57.54 1773 1
63°57.54 1773 3
63°57.54 1773 3
64°05.41 2171 3
64°05.43 2144 3
61°06.13 1847 2
61°06.92 1668 3
12.26
12.64
11.57
11.90
7.25
10.13
12.15
6.29
10.21
10.19
11.81
8.87
11.85
7.95
12.17
12.66
12.05
6.61
10.19
13.8
6.50
12.41
12.36
13.74
9.97
8.02
10.69
MAN703-1
MAN706-1
MAN708-1
MAN708-2
MAN801-1
MAN803-2
NAS104-1
NAS105-1
NAS110-3
NAS203-1
NAS203-2
5/15/04
5/15/04
5/15/04
5/15/04
5/16/04
5/16/04
8/25/05
8/25/05
8/25/05
8/26/05
8/26/05
10/28/05
PIC101-3
REH 203-1 8/29/05
REH105-1 8/29/05
REH 112-3 8/29/05
REH212-1 8/30/05
REH215-1 8/30/05
LYM210-1 8/14/05
Manning, NES
Manning, NES
Manning, NES
Manning, NES
Manning, NES
Manning, NES
Nashville, NES
Nashville, NES
Nashville, NES
Nashville, NES
Nashville, NES
Picket, NES
Rehoboth, NES
Rehoboth, NES
Rehoboth, NES
Rehoboth, NES
Rehoboth, NES
Yukatat, CRS
38°08.93
38°08.93
38°08.09
38°08.09
38°08.84
38°08.83
34°34.92
34°34.88
34°34.77
34°28.81
34°28.81
39°39.12
37°33.67
37°27.63
37°27.60
37°33.48
37°33.37
35°11.63
61°06.14
61°06.13
61°06.97
61°06.97
61°05.87
61°05.86
56°50.59
56°50.59
56°50.51
56°44.15
56°44.15
65°56.50
59M8.43
59°57.08
59°56.99
59M8.18
59M8.13
47°40.60
1867
1847
1718
1718
1692
1674
2233
2221
2136
2103
2103
2084
1678
1907
1820
1438
1372
2143
3
3
3
3
3
3
3
3
3
3
3
3
2
3
3
3
3
3
13.41
12.24
12.06
14.86
12.90
12.63
12.85
12.31
11.46
11.37
12.24
13.61
9.16
11.34
11.95
11.71
11.08
12.03
Sample Treatment
After removal from the submersible or ROV bioboxes, the M. melanotrichos and
associated brittle stars were briefly held in cold seawater until processed on-board the
research vessel. Processing each octocoral began by photographing each one with its
associates and making preliminary identifications if possible. Small portions of the
corals were removed for future use in molecular studies as was one arm of each brittle
star. The specimens were then fixed in a 5% formalin/seawater bath for approximately 812 h. Most brittle stars were extricated from the coral colonies before fixation, although
some especially small individuals were left on the host throughout the preservation
process. Following the formalin bath, all specimens were transferred to 70% ethanol for
long-term storage.
7
Commensalism
Of the 66 M. melanotrichos colonies collected, 45 of the associated ophiuroids
were brought to the Darling Marine Center for this study (Table 1). The rest were placed
in collections at the Smithsonian National Museum of Natural History, Yale-Peabody
Museum, and Woods Hole Oceanographic Institution. At the Darling Marine Center, the
ophiuroid specimens were digitally photographed using a dissecting microscope taking
care to capture defining characters for species identification. Disc diameter was recorded
as the distance across the aboral surface from the point between the radial shields above
one arm to the opposing interradius. Number of arms with macroscopically visible signs
of regeneration per individual was recorded. The brittle star arms were tightly coiled
around the branches of M. melanotrichos and data from arms that were broken and/or
missing after extraction from the host, as well as those that had been taken for molecular
studies, could not be included in this study.
M. melanotrichos colonies of a wide range of sizes were collected. They were
divided into three growth stages. Stage 1 is the youngest juvenile stage, Stage 2 is
intermediate, and Stage 3 is the full-grown adult stage, as more fully characterized in the
Results.
Observational data recorded from the video and frame grabs of submersible dives
included the number of brittle stars on each of the 66 M. melanotrichos colonies,
presence/absence of non-ophiuroid fauna associated with the octocorals,
presence/absence of O. oedipus brittle stars on other corals and/or on the seabed, location
of the brittle stars on the octocoral, and behavior of the brittle stars. Also, the number
and species of brittle stars associated with uncollected M. melanotrichos were recorded.
8
The observations were made before and during collection while great care was taken to
discern abnormal behavior caused by the submersible or ROV. The video was also used
to ascertain that the brittle stars were on their respective hosts when collected and identify
those few that traveled from their hosts after being stored in the bioboxes.
Reproductive Biology
In many asteroschematids the gonads develop as tubules in the proximal part of
the arms. In O. oedipus, this portion of the arms becomes swollen as the brittle star
matures to accommodate the expanding gonad tubules. The number of modified arm
segments was recorded from one arm of each brittle star. This sampling was deemed
sufficient because the number of modified arm segments was seen to be approximately
equal among the arms of each individual. Gonadal portions from multiple arms of each
individual were dissected microscopically to examine gross morphology. The swollen
proximal portion of one arm was removed from each individual for examination by
paraffin histology. These gonadal portions were hydrated and allowed to decalcify in
Hollande's fixative for approximately two weeks. The portions were then dehydrated in
ethanol, cleared with toluene, and embedded in paraffin. Serial transverse sections (1214 jxm thick) were hydrated and stained with Gomori's trichrome (aniline blue) before
finally dehydrating and mounting for microscopy. Histological sections of O. oedipus
gonads were examined under a compound microscope to determine the sex of each
specimen. The number of eggs within one of each pair of gonadal tubules of the
sectioned arm was counted by counting the distinct nucleoli. This number was multiplied
by 10 to estimate the standing fecundity of an individual. Fecundity of four individuals
9
with different disc sizes was estimated. The minimum and maximum egg sizes were
taken from the tubules examined for fecundity. Many eggs were nonspherical due to
packing within the gonads. Egg size was estimated as an average of two diameters
measured perpendicular to one another. Digital images were captured of the male,
female, and immature gonads and examined further for details of reproductive anatomy
and evidence of reproductive mode and periodicity.
in
Chapter 3
RESULTS
Growth Stages of Metallogorgia melanotrichos
Juvenile M. melanotrichos do not look like adults. The juvenile form (Stage 1)
consists of a single stalk with axial polyps arising from the central axis and a single
terminal polyp at the apex of the stalk. This juvenile develops branches along the central
axis that give rise to more polyps (Figure 2 a,b). As the colony matures, the polyps
disappear from the central axis, and a cluster of terminal branches replaces the terminal
polyp (Stage 2). This cluster forms a burgeoning "parasol" of polyps while the axial
branches are retained along the stalk (Figure 2 c). Finally, the axial branches disappear
and the adult form (Stage 3) is fully manifested as a solitary stalk with a full crown of
polyp-covered terminal branches (Figure 2 d,e). As the colony ages further, branches in
the crown continue to subdivide until the crown is densely branched.
The M. melanotrichos hosts of the 45 brittle stars used in this study were
categorized into growth stages as follows: four Stage 1 juveniles, six Stage 2
intermediates, and 35 Stage 3 adults (Table 1).
11
Figure 2 Growth stages of Metallogorgia melanotrichos. Note the Ophiocreas oedipus
(O) associated with each colony. (White scale bars = 5 cm) a Stage 1 M. melanotrichos
12
characterized by a single terminal polyp (tp) and axial polyps (ap) arising from a central
axial stalk. Axial branches (ab) are present in the more mature Stage 1 colonies, b Stage
1 colony illustrating the terminal polyp that defines this stage, c Stage 2 M.
melanotrichos. Terminal branches (tb) have replaced the terminal polyp. The axial
branches still arise from the stalk but the axial polyps are no longer present, d In situ
image of Stage 3 M. melanotrichos with a full crown of terminal branches. A single O.
oedipus is curled around the branches in the center of the crown, e Stage 3 M.
melanotrichos. Axial polyps and branches are no longer present in the adult colony.
Association Between Metallogorgia melanotrichos and Ophiocreas oedipus
All collected M. melanotrichos hosted one individual O. oedipus. In addition,
there were 94 M. melanotrichos definitively seen to host a single brittlestar resembling O.
oedipus in the frame grabs. The dive tracks did not coincide on repetitive visits to
seamounts, therefore multiple observations of the same individual did not occur. O.
oedipus was found on no other coral in our explorations nor was it observed on the
seabed via submersible/ROV video camera and frame grabs. No other ophiuroid species
was found on living M. melanotrichos across the New England and Corner Rise
seamounts. Other brittle star species were observed around the base of M. melanotrichos
colonies and sometimes hanging from the detritus-covered base of the stalk. In addition,
no other macroscopic species were observed on this coral, with the exception of one
octocoral on Balanus Seamount. This M. melanotrichos was swathed with numerous
non-stalked crinoids and other brittle star species were hanging off the stalk that appeared
13
to be covered with dead tissue. One O. oedipus was present even though the octocoral
appeared to be in poor health.
There is a strong correlation between the disc diameters of O. oedipus and the
growth stage of the respective octocoral hosts (Figure 3, Kruskal-Wallis H = 22.24, p <
0.001, n = 45). Disc diameters ranged from 6.29 to 14.86 mm (Table 1) with a mean of
11.23 mm. O. oedipus does not exhibit external sexual dimorphism (Mann-Whitney U =
270, p = 0.95, n = 43). Females had a mean disc diameter of 12.86 mm and males, 11.04
mm. The disc diameter of brittle stars perched on Stage 1 M. melanotrichos is 6.66 mm.
The mean diameter of those residing on Stage 2 hosts is 9.06 mm and the mean size of
those on Stage 3 octocorals is 12.13 mm.
1
2
3
Growth stage of host octocoral
Figure 3 Ophiocreas oedipus disc diameters of individuals residing in the three growth
stages of M. melanotrichos hosts. (Circles = outliers, t-bars = range, solid bars =
medians, boxes = 25th to 75lh percentiles)
14
O. oedipus was found with its arms coiled around the branches in the center of an
M. melanotrichos host (Figure 2 d, 4 d) and often the outer lengths of up to all five arms
were extended into the surrounding water. O. oedipus did not appear to take care to
avoid contact with the stinging polyps of M. melanotrichos as it waved its arms about.
Brittle stars stopped any activity or feeding postures when disturbed physically by the
submersible/ROV arm. O. oedipus resided always in the full crown of branches of an
adult host or coiled around the axial stalk of hosts without crowns. (Figure 2 a-e). Of the
six brittle stars on Stage 2 hosts, four were found in the young parasol of branches at the
apex of the stalk and the other two were coiled around the stalk below the parasol.
Predation on Ophiocreas oedipus
Although there were 45 O. oedipus available for the analysis of regeneration, only
82.7% of their arms were available and intact enough to make a confident assessment of
regeneration. Of them, 15.1% showed macroscopic signs of regeneration (Figure 4 d).
All but one of the regenerating individuals were on Stage 3 host colonies. Only one
specimen had 3 arms regenerating and the rest had 2, 1, or none.
Ophiocreas oedipus Reproductive Biology
O. oedipus is gonochoristic. Of the 45 specimens examined histologically, 22
were female, 21 were male, and two immature individuals could not be sexed with
paraffin histology. Thus, the sex ratio appears to approximate unity.
Male and female gonads consist of paired tubules that extend into the arms of O.
oedipus from the bursae of the central disc. The gonadal tubules lie aboral to the
15
vertebral ossicles (Figure 4 a,b) and occur in pairs of up to four per arm (Figure 4 a-c).
Two of the 45 brittle stars contained unpaired gonadal tubules, both having one tubule on
one side of each arm. The other side of the arms housed three and four tubules within the
two individuals.
The growth of the gonadal tubules causes a modification of the surrounding
calcified arm structures so that the area that houses the gonads is visible externally
(Figure 4 d). The number of arm segments modified by the growth of the gonads within
one arm of each specimen ranged from zero to 14. Of the five individuals with no
modified arm segments, three were sexually immature with no gonads at all and two had
one pair of gonadal tubules just beginning to grow. There is a sexual dimorphism in the
size of gonads as estimated by the number of arm segments modified. Male gonadal
tubules modify more arm segments than female tubules (Mann-Whitney U = 290.5,0.01
< p < 0.02, n = 40). The number of arm segments modified in females averaged 5.14 and
in males, 7.74. These means do not include those immature but sexed individuals with no
modified segments.
The number of gonadal tubule pairs per arm weakly depends on the disc diameter
of the brittle star while the number of segments modified is more strongly dependent on
disc diameter (Figure 5). The gonadal tubules may continue to grow farther out the arms
as the brittle star ages, but the number of tubule pairs does not exceed four.
16
Figure 4 Ophiocreas oedipus gonad morphology. (Scale bars = 1 mm) a Image of one
pair of aboral gonadal tubules extending into the arm of a female O. Oedipus. The
oocytes are visible within the gonad coelom. b Three pairs of male gonadal tubules.
Male tubules are longer and more slender than female tubules, c Female gonadal tubules
removed from one arm to show all four pairs. The maximum number of pairs found in
any individual arm, male or female, is four, d The heavily calcified arm structure is
modified to accommodate the gonadal tubules. The enlarged proximal arm portion is
visible externally (white ^ ) . Note evidence of regeneration on missing arm (black ^ ) .
Also, note the posture of the brittle star curled around the branches of the octocoral
seemingly heedless of the stinging polyps. (Brittle star disc diameter =13.8 mm)
17
10.0
12.0
Disc diameter ( m m )
10.00
12.00
Disc diameter ( m m )
Figure 5 Change in gonadal tubule morphology of Ophlocreas oedipus as disc diameter
increases, a Number of arm segments modified by tubule growth generally increases with
disc diameter, b Number of gonadal tubule pairs within one arm is less dependent on disc
diameter.
Of the four female specimens examined, the smallest individual with three tubule
pairs per arm had an overall standing fecundity of 1750 while the largest individual had
an estimated 15,230 eggs (Table 2). Another large individual had one tubule pair per arm
18
and an estimated 9,840 overall fecundity. The number of eggs within a tubule pair differs
between pairs in the same individual. Egg size also differs between pairs (Table 2). The
diameters of eggs range from 39.0 to 604.5 ^m. Tubules with the most eggs have the
smallest eggs because females have many small immature eggs within a single tubule
pair (hereafter referred to as the primary pair). If there are more pairs within each arm,
larger, more mature eggs are seen (Figure 6 b) over the entire length of these tubules.
Gametogenesis appears synchronous between both tubules of pairs, with the
exception of the primary pair. Within the primary tubule pair, eggs closer to the disc are
smaller and less mature than eggs at the distal end. Each pair of tubules develops
asynchronously to other pairs in the same arm. This is the case for both males and
females (Figure 6 a,b) and was exhibited by O. oedipus collected at all four time periods:
mid May, mid July, end of August/beginning of September, and the one female
individual collected at the end of October.
There is no evidence suggesting reproductive periodicity in the present study.
Table 2 Ophiocreas oedipus estimated fecundity and egg sizes per gonadal tubule.
Disc diameter Total estimated Gonad tubules No. eggs Min. egg size
(mm)
fecundity
(pairs/arm) per tubule
(|jm)
50.7
9.16
1750
3
161
10
230.1
4
421.2
11.34
4040
4
283
27.3
315.9
45
40
397.8
36
124.8
984
39.0
12.66
9 840
1
13.41
15 230
4
1285
39.0
401.7
87
83
292.5
218.4
68
19
Max. egg size
(pm)
198.9
300.3
444.6
136.5
604.5
479.7
331.5
109.2
222.3
436.8
409.5
292.5
Figure 6 Transverse histological sections of gonadal tubules of Ophiocreas oedipus. The
vertebral ossicles (O) lie along the oral surface of the arms. (Scale bars = 0.5 mm) a Male
gonadal tubules at varying stages of gametogenesis within a single individual. One pair of
tubules (Tl) has spawned more recently than the others and is spent. The germinal
epithelium has many invaginations ( ^ ) , and there is a lack of spermatozoa. Another
tubule pair (T2) contains spermatozoa. The germinal epithelium is thickened but still
invaginated. The tubule T3 has lost the invaginations of the epithelium and is packed
with spermatozoa, b Female gonadal tubules at varying stages of gametogenesis within a
single individual. Tl is the tubule at the youngest stage of development in this female.
These small, early-vitellogenic oocytes stain darker than the more mature gametes. A
second tubule pair (T2) has larger, mid-vitellogenic oocytes. A third tubule pair (T3) are
at a stage close to the remaining tubule pair (T4). In these gonadal tubules, the cytoplasm
of the late-vitellogenic oocytes stains lighter with a grainy appearance.
20
Chapter 4
DISCUSSION
Commensalism of Ophiocreas oedipus on Metallogorgia melanotrichos
This study of the relationship between O. oedipus and M. melanotrichos offers a
unique opportunity to peer into the lives of some of the most elusive deep-sea brittle stars
and cold-water corals. O. oedipus appears to be different from other deep-seamount coral
associates, many of which are generalists using any coral as a means to gain height in the
benthic-boundary layer (Buhl-Mortensen and Mortensen 2004). The commensalism of
O. oedipus on M. melanotrichos is species-specific and appears obligate on the part of O.
oedipus. A mutualistic relationship is not suggested since no benefit to the coral has been
seen and, is difficult to infer.
Until molecular work was completed after the 2004 cruise, the Stage 1 and Stage
2 host colonies could not be positively identified as M. melanotrichos. Their difference
in external morphology from the adult Stage 3 caused some initial ambiguity. However,
the development of the polyps along the stalk and the branching patterns illustrate the
progression from a juvenile colony to an adult. The strong correlation between brittle star
size and growth stage of the host suggests that O. oedipus matures on - and with - its host
M. melanotrichos. Instances of obligate associations between brittle stars and octocorals
have been seen before (Emson and Woodley 1987, Grange 1991, Pearse et al. 1998,
Metaxas and Davis 2005), but the phenomenon of growing up together has not been
previously observed.
21
The high fidelity between O. oedipus and M. melanotrichos has many
implications. O. oedipus appears to need M. melanotrichos for survival on the New
England and Corner-Rise seamounts. If anthropogenic influences in the deep sea
continue to put seamount coral communities at risk, the organisms that live on the corals
are equally at risk if they are not able to thrive in other habitats such as on the seabed.
The presence of species-specific associations may be an indicator of higher biodiversity
on seamounts (McClain 2007), however, biodiversity may be only slightly elevated as
obligate associations are rare (Buhl-Mortensen and Mortensen 2004).
Moore et al. (2003) explored the biodiversity of a single seamount in the New
England chain in which associations were not recorded. However, such studies should be
cautiously interpreted since artifacts of sampling on seamounts are easily overlooked
(Stocks and Hart 2007). There is a dire need for further sampling of seamounts to assist
management strategies since it is well-accepted that the ecological communities on
seamounts, although often distinct from seamount to seamount, are different from the
surrounding deep-sea and so are usually not characterized by the larger biogeographic
region (Probert et al. 2007).
Such a tight association would seem limiting and is likely to have persisted for
thousands of years in the stable environment at these depths. It is worth noting that
commensal associations between euryalids and other invertebrates can be found in the
fossil record as early as the late Carboniferous. Ancestors of the Asteroschematidae, the
Onychasteridae, are known as fossils coiled around the anal cone of stalked crinoids,
300-325 million years ago (Clark 1908, Wachsmuth and Springer 1897).
22
The exact mechanism that allows O. oedipus to recognize its host is unknown.
Chemical cues likely signal the brittle star larvae to settle either directly onto a young
coral or onto the seabed. Recently settled O. oedipus would not have been visible on the
seabed at the resolution of our video. However, the cost of settling on the seabed and
then searching for a particular host species would be very high because the corals are
rare. If the number of settling larvae is high enough to sustain the population under such
conditions, a settle-then-search mechanism could be maintained. O. oedipus larvae
apparently travel long distances between seamounts (Cho pers. com.) and presumably
larval density is not high over one specific seamount. It is more likely that the larvae
settle onto the juvenile coral from the water column after encountering a chemical cue in
the surrounding water.
No other ophiuroids are found on M. melanotrichos despite the presence of many
other ophiuroid species on the surrounding benthos and hosted by nearby corals. Also,
only one O. oedipus resides on a single octocoral. When the coral is young, it is possible
that its defensive polyps and chemicals are not as toxic to the settling brittle star and the
brittle star develops a resistance to the coral as it grows. Other possible associates, brittle
stars or any other commensals, may not be able to withstand the defense mechanisms of
M. melanotrichos, thus explaining the lack of other associations. This hypothesis could
be tested through in situ manipulations. Pelagic larvae likely recognize the
presence/absence of O. oedipus on a young coral. Alternatively, territorial aggression
could maintain O. oedipus' solitary lifestyle but this is unsupported by any video
observations. The lack of regenerating arms on young brittle stars may be evidence that
physical aggression is not taking place; rather a chemical signal may indicate that a host
23
is already occupied. Another possibility is that the resident brittle star may remove
potential competitors when they are in a younger, post-larval stage. Finally, the
phenomenon of growing up together may simply be a result of host octocorals being rarer
than newly settling O. oedipus. On the Corner Rise and New England seamounts, it may
be that young M. melanotrichos without a current resident represent the only options
available to settling O. oedipus. If the brittle stars live as long as the hosts and fatalities
from predation are low, few adult M. melanotrichos would ever become available.
The brittle stars on intermediate Stage 2 hosts were either in the burgeoning
parasol of polyps or curled around the stalk. At some point in the development of the two
species, O. oedipus ascends into the crown to live. This likely happens when the
octocoral's crown becomes large enough to protect the brittle star and/or when the brittle
star achieves a state of maturity that allows it to withstand the density of stinging polyps
found in the complex of branches of the M. melanotrichos crown.
The evolutionary advantage of maintaining a uniform, solitary population
distribution over hosts is not obvious. Food availability may play a role, but nearby
arborescent corals hosting many brittle stars would seem to dispel that conclusion. Since
there appear to be many possible dwelling locations within the larger adult M.
melanotrichos, one colony could, in theory, host several O. oedipus. The population
uniformity of one brittle star per coral is likely to have persisted since both coral and
brittle star were young. When the coral colony was no more than an axial stalk with a
few polyps, there were fewer places for the young brittle stars to perch and take
advantage of the available currents. That no other larval O. oedipus settles on the coral
may be the result of an evolved survival mechanism. In addition, a single ophiuroid
24
perched and protected within the center of a M. melanotrichos crown of polyp-covered
branches is less likely to be harmed by predators than multiple ophiuroids located nearer
the outer limits of the coral's crown. If there is a predatory attack, damage is not likely to
be fatal if arms are clipped off as opposed to the whole ophiuroid being removed from the
coral. Of the 15% incidence of regenerating arms among those arms analyzed, in most
cases only one arm was damaged. As the brittle stars wave their arms into the prevailing
current for food, an arm could be bitten off and the brittle star would have a chance to
curl into the interior of its host's protective crown. The in situ observations of O. oedipus
suggest such a defense mechanism as the brittle stars were seen extending their arms out
into the water and retracting them upon being disturbed.
Reproduction in Ophiocreas oedipus
Up to four gonadal tubule pairs were found per arm of O. oedipus. This differs
from the single pair per arm that is more common among the asteroschematids (Hendler
1991; Byrne 1994; Stewart and Mladenov 1994). The two specimens that did not have
matching pairs in each arm are likely developmental anomalies; unmatched tubules in
pairs are uncharacteristic of the population as a whole.
Pairs of tubules were at varying maturity levels from other pairs within each
individual that had more than one tubule pair. That this was the case at all four collection
times, and in both males and females, implies that spawning is likely to happen in one of
two different ways: either O. oedipus spawns multiple times per year, or it is a dribble
spawner. Gonad morphology suggests that O. oedipus combines these two mechanisms
by spawning at multiple times per year only a portion of an individual's gametes, one
25
tubule pair in all five arms at a time. In other words, a spawning individual releases
gametes from 10 gonadal tubules at one time while other tubule pairs are continuing to
mature. Whether the population spawns synchronously or timing differs at the level of the
individual is unknown, but considering their dioecious, solitary lifestyle, synchronous
spawning across the population would be more likely to result in successful fertilization.
That the number of gonadal tubule pairs per arm appears to not depend on disc diameter
implies this number does not progressively increase to four as the individual grows and
then four pairs are maintained through the remainder of an individual's lifespan. Tubule
pairs may be resorbed after the contents are released and then a new pair begins to
develop.
With the exception of the primary pair in females, each gonadal tubule pair
contains a cohort of gametes developing synchronously. The oocytes in the primary pair
are all less mature than those found in other pairs, however, oocytes are distinctly smaller
and less mature at the ends of the tubules proximal to the disc. Oocytes are likely formed
initially near the central disc where the tubules attach and are pushed more distally as
they mature. This phenomenon has been seen before in ophiuroids (Smith 1940; Patent
1976; Byrne 1994) and is evidence that the source of gamete-producing germ cells is the
genital rachis (Hendler 1991). The distinct pattern of one tubule pair being fairly
immature or recovering from a recent spawning event and other tubule pairs being more
mature within each individual implies that these brittle stars do not spawn all their
gonadal contents at the same time.
Reproductive periodicity thought to be associated with the annual plankton
blooms of the North Atlantic as seen in other deep-sea ophiuroids (Tyler and Gage 1980,
26
Tyler et al. 1982, Sumida et al. 2000, Gage et al. 2004) was not evident in this study. The
maturity-stage index method (Patent 1969) commonly used to evaluate periodicity could
not be used because each individual manifested up to four stages of gametogenesis. A.
constrictum represents the closest relative of O. oedipus for which reproductive studies
have been completed. This species exhibited an annual breeding pattern at depths
between 18 and 21 m in a New Zealand fjord (Stewart and Mladenov 1995) and it
follows the general reproductive anatomy of the Asteroschematidae described by Hendler
(1991). But this species, although closely related, is located in an environment with light
penetration and nutrient run-off, a very different environment than that found on the
seamounts. Deep-sea species for which reproductive periodicity has been supported are
more distantly related, bottom-dwelling brittle stars. Further studies are necessary, yet
the reproductive timing of O. oedipus, with its long, persistent association in the deep sea,
may be phylogenetically constrained as suggested by Eckelbarger and Watling (1995),
and the gonadal morphology described previously supports continuous reproduction.
Fecundity increases dramatically with size of the female and less so with number
of gonadal tubules. This weaker dependence is partly because one gonadal tubule pair
holds the majority of the oocytes regardless of the number of pairs within an individual
(Table 2). The oocytes within this pair are the least mature and smallest of the oocyte
cohorts within any individual housing more than 1 tubule pair per arm. Successive tubule
pairs hold considerably fewer oocytes, although these oocytes are larger and more
developed. An oosorption mechanism is likely responsible for this developmental pattern
and is common in echinoderm species. It is believed that the oosorbed material may be
used for the development of other healthy oocytes (Hendler 1991; Byrne 1994). Oocyte
27
abortion and oogenesis occur simultaneously in continuously reproducing species (Byrne
1994). In the case of O. oedipus, most of the oocytes within the least developed gonadal
pair may be oosorbed to supply nutrients for the remainder of the oocytes in this
developing cohort. If so, the total fecundity estimated for the individuals in this study is
much greater than the number of oocytes that will reach maturity to be released. The
number of oocytes spawned would depend upon the rate of gametogenesis as well as the
rate of oosorption.
The mature oocytes of O. oedipus attain sizes greater than 600 ptm, indicative of a
lecithotrophic larval stage. Molecular studies are underway assessing the genetic
connectivity within the population of O. oedipus across the New England and Corner
Rise seamounts. Findings indicate high connectivity (Cho pers. com.) despite the
thousands of miles of open sea between some of these octocoral communities. A longlived larval stage would be necessary to reach such distances. A pi an kto trophic larval
stage would assist this species in maintaining its high connectivity. Fertilization success
may be low because O. oedipus is restricted to its habitat in colonies of M. melanotrichos
and host octocorals can be found in clusters in only some locales. The brittle stars may
be hundreds of meters apart in other spots. It appears that M. melanotrichos hosts are a
limiting resource for larval O. oedipus because we did not find any of these octocorals
without its resident brittle star. Populations of O. oedipus are likely sustained by a longlived larval stage that can travel far to find an unoccupied juvenile host on which to
settle.
28
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BIOGRAPHY OF THE AUTHOR
Celeste Virginia Mosher was born in Rumford, Maine, on November 4 , 1974.
She was raised in Wilton, Maine, and graduated from Mt. Blue High School in 1993.
Celeste was awarded a Bachelor of Science degree in Biology from the University of the
Virgin Islands in 2002 where she graduated summa cum laude. After her undergraduate
career, she gained marine laboratory and field experience while working with researchers
from the Center for Marine and Environmental Studies, St. Thomas, VI, Harbor Branch
Oceanographic Institution, Ft. Pierce, FL, and Woods Hole Oceanographic Institution,
Woods Hole, MA. She has participated in numerous research cruises conducting
physical and biological oceanographic investigations throughout the Caribbean and
Northwest Atlantic.
Celeste returned to Maine to begin her graduate career at the School of Marine
Sciences at the University of Maine in the summer of 2005. Celeste is a candidate for the
Master of Science degree in Oceanography from the University of Maine in August,
2008.
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