In-Situ Observations of the Deep-sea Goosefish Sladenia shaefersi Caruso and Bullis (Lophiiformes: Lophiidae), with Evidence of Extreme Sexual Dimorphism

Abstract

The deep-sea goosefish Sladenia shaefersi Caruso and Bullis, now known from only six specimens in collections around the world, appears to be more common than once thought, as indicated by recent in-situ observations off the southeastern United States and in the northern Gulf of Mexico. These sightings have provided new information on geographic distribution, behavior, and habitat, plus evidence for an extreme size difference between putative males and females. © 2013 by the American Society of Ichthyologists and Herpetologists.

Full text

In-Situ Observations of the Deep-sea Goosefish Sladenia shaefersi Caruso
and Bullis (Lophiiformes: Lophiidae), with Evidence of Extreme
Sexual Dimorphism
Theodore W. Pietsch
1
, Steve W. Ross
2
, John H. Caruso
3
, Miles G. Saunders
4
, and
Charles R. Fisher
4
The deep-sea goosefish Sladenia shaefersi Caruso and Bullis, now known from only six specimens in collections around
the world, appears to be more common than once thought, as indicated by recent in-situ observations off the
southeastern United States and in the northern Gulf of Mexico. These sightings have provided new information on
geographic distribution, behavior, and habitat, plus evidence for an extreme size difference between putative males
and females.
THE deep-sea goosefish Sladenia shaefersi was described
originally by Caruso and Bullis (1976) on the basis of
two specimens collected by trawl in the Caribbean
Sea: the holotype from off Point Baru, Colombia, and the
paratype from off Aruba Island in the Lesser Antilles, at
depths of 1200 and 850 m, respectively (Caruso, 1985, 2003;
Moore et al., 2003). Since that time, only four additional
specimens have been reported: an individual first reported
by Kukuev (1982), and later described and figured by
Prokofiev and Kukuev (2009), from far to the northeast on
the Angular Rise in the New England Seamount chain; a
fourth reported by Caruso et al. (2007) collected on the
Blake Plateau off South Carolina; a fifth, unpublished
record, from off Cape Canaveral, Florida (see below); and a
sixth specimen from the southern Gulf of Mexico off
Tabasco, Mexico, described by Sepu´ lveda et al. (2013).
Except for routine trawl data, almost nothing has been
known about the biology of this species, although it has
generally been considered rare but widely distributed
(Caruso et al., 2007; Prokofiev and Kukuev, 2009; Sepu´lveda
et al., 2013). Here we describe, for the first time, in-situ
submersible and ROV observations that provide new
information on distribution, abundance, behavior, and
habitat, plus evidence for an extreme size difference
between putative males and females (Figs. 1, 2).
MATERIALS AND METHODS
All fish lengths are standard length (SL). Institutional
symbolic codes follow those provided by Sabaj Pe´rez
(2012). In-situ observations were made during recent
research cruises investigating cold-seeps and deep coral
communities along the outer continental shelves and upper
slopes off the southeastern U.S. and northern Gulf of
Mexico. In-situ observations were recorded with video and,
in some cases, digital still cameras. Parallel lasers spaced
10 cm apart were used to estimate the standard length of
four of the fish observed; but for two, the large putative
female and tiny putative male (ROV Global Explorer, aboard
RV Falkor; Fig. 2), in the absence of laser determination and
any other appropriate scale, only the relative size of the two
could be estimated by comparing standard lengths in pixels.
For methods describing the August 2004 observations via
the submersible Johnson-Sea-Link II (JSL), see Caruso et al.
(2007). For information on the vehicle and dives made in
June 2007 using ROV Jason II, see http://oceanexplorer.
noaa.gov/explorations/07mexico/welcome.html; for those
in October 2011 using ROV Chouest Holiday, see http://
www.chouest.com/subsea.html; for those in April 2012 using
ROV Little Hercules, see http://oceanexplorer.noaa.gov/
okeanos/explorations/ex1202/background/plan/welcome.
html; and for those in November 2012 using ROV Global
Explorer, see http://www.schmidtocean.org/story/show/
1430.
The work was based on six preserved specimens and five
in-situ observations (as numbered in Fig. 3): (1) holotype,
USNM 214477, female, 397 mm, FRV Oregon II, cruise 22,
station 11242, 10.1667uN, 76.2333uW, ca. 52 km west of
Point Baru, Colombia, depth 1200 m, 22 m semi-balloon
trawl, 4 hr tow, 5 November 1970; (2) paratype, USNM
214478, male, 146 mm, FRV Oregon II, cruise 43, station 124
of the Miami Laboratory, 13.0000uN, 70.6667uWto
12.9083uN, 70.4417uW, ca. 47–69 km NW of Aruba Island,
Lesser Antilles, depth 850 m, 12 m flat trawl, 6 hr tow, 24–25
February 1973; (3) ZMMU 16117, sex indeterminate,
280 mm, trawler-freezer Bakhchisarai, trawl 79, 35.5167uN,
51.9667uW, depth 910–1200 m, 29 April 1977; (4) GMBL
5333, female, 301 mm, JSL, aboard RV Seward Johnson,
station JSL 2-3467, by suction device, on coral rubble near
base of a steep 200-m scarp on the Blake Plateau off the coast
of South Carolina, 31.8167uN, 77.5167uW to 31.7500uN,
77.5667uW, depth 909 m, start time 1603 hr, 26 August
2004; (5) NCSM 73401, spent female, 360 mm, JSL, aboard
RV Seward Johnson, station JSLII-2009-Atl-3720, by suction
device, on Lophelia pertusa coral rubble off Cape Canaveral,
Florida, 28.0389uN, 79.6086uW, depth 689 m, video time
segment 18:48:49–18:52:53 hr, 16 August 2009; (6) CNPE-
1
School of Aquatic and Fishery Sciences and Burke Museum of Natural History and Culture, University of Washington, Campus Box 355020,
Seattle, Washington 98105-5020; E-mail: twp@uw.edu. Send reprint requests to this address.
2
Center for Marine Science, 5600 Marvin K. Moss Lane, University of North Carolina Wilmington, Wilmington, North Carolina 28409;
E-mail: rosss@uncw.edu.
3
Department of Ecology and Evolutionary Biology, 400 Lindy Claiborne Boggs Center, Tulane University, 6823 St. Charles Avenue, New
Orleans, Louisiana 70118-5698; E-mail: jcaruso@tulane.edu.
4
Department of Biology, 208 Mueller Laboratory, The Pennsylvania State University, University Park, Pennsylvania 16802; E-mail: (MGS)
mgs190@psu.edu; and (CRF) cfisher@psu.edu.
Submitted: 10 March 2013. Accepted: 4 June 2013. Associate Editor: D. Buth.
F2013 by the American Society of Ichthyologists and Herpetologists DOI: 10.1643/CI-13-023
Copeia 2013, No. 4, 660–665

IBUNAM 16607, female, 208 mm (as measured by us), RV
Justo Sierra, southern Gulf of Mexico, off Tabasco, Mexico,
19.4622uN, 93.0556uW, semi-balloon otter trawl, depth
1144–1152 m, 25 August 2009.
The five in-situ observations include (as numbered in
Fig. 3): (4) a single specimen, GMBL 5333 (listed above); (7)
three closely associated specimens, one approximately
570 mm, another about 615 mm, the third in the same size
Fig. 1. In-situ images of Sladenia shaefersi in the northern Gulf of Mexico: (A–E) 570–615 mm SL, ROV Little Hercules, aboard NOAA ship Okeanos
Explorer, depth 1165 m, April 2012 (framegrab from video); (F) 510 mm SL, ROV C-Innovation UHD, aboard the Chouest Holiday, depth 1092 m,
October 2011 (digital still); (G–H) 790 mm SL, ROV Jason II, aboard NOAA ship Ronald H. Brown, Operation Deep Slope, depth 1002 m, 16 June
2007 (digital stills).
Pietsch et al.—Deep-sea Goosefish, Sladenia shaefersi 661

range but without laser-scale information, ROV Little
Hercules, aboard NOAA ship Okeanos Explorer, Expedition
3, Dive 10, northern Gulf of Mexico, 27.13uN, 90.15uW,
northeastern flank of a salt dome, depth 1165 m, 24 April
2012 (Fig. 1A–E); (8) single specimen, about 510 mm, ROV
C-Innovation UHD, aboard the Chouest Holiday, northern
Gulf of Mexico, 28.9362uN, 88.2022uW, depth 1092 m,
October 2011 (Fig. 1F); (9) single specimen, about 790 mm,
ROV Jason II, aboard NOAA ship Ronald H. Brown, Chemo
III, Operation Deep Slope, northern Gulf of Mexico,
27.1875uN, 92.6386uW,depth1002m,16June2007
(Fig. 1G–H); (10) two specimens, putative male and female,
the assumed female, comparable in size to the largest of the
other females observed in situ, about 10.8 times the length of
the putative male, ROV Global Explorer MK3, aboard RV
Falkor, Dive 13, northern Gulf of Mexico, 27.5858uN,
89.7050uW, depth 1052 m, 23 November 2012 (Fig. 2).
RESULTS AND DISCUSSION
The few known locality records of S. shaefersi indicate a
broad geographic distribution in the western North Atlantic
ranging from seamounts in the open ocean to the conti-
nental slopes of Colombia, Venezuela, South Carolina,
Florida, and the Gulf of Mexico, at depths of 689–1200 m
(Fig. 3). In most cases, the in-situ observations were similar:
solitary individuals lying motionless on hard-bottom or
Fig. 2. In-situ image of Sladenia shaefersi in the northern Gulf of Mexico, putative mated pair, female, with tiny male resting on head just above eye:
ROV Global Explorer MK3, aboard RV Falkor, depth 1052 m, 23 November 2012 (digital still).
Fig. 3. Distribution of Sladenia shaefersi in the western North Atlantic
Ocean. Numbers correlate with locality data given in the text.
662 Copeia 2013, No. 4

coral rubble near relatively small, complex, reef-like out-
crops of exposed carbonates—of which thousands have been
visited and imaged in the northern Gulf of Mexico over the
past 20 years (Fisher et al., 2007)—but never on the much
more abundant surrounding soft-sediment areas. The Okea-
nos Explorer observations in the northern Gulf of Mexico
differ, however, in showing three, closely associated indi-
viduals perched on top of large boulders (most likely
authigenic carbonate rock) near a cold seep ecosystem,
apparently lying in wait and luring for prey. In most of the
images, the illicium (first dorsal-fin spine) can be seen
extended forward in front of the mouth, but the available
videos show no actual luring motion. In fact, during two
continuous video recordings, lasting nearly 4 min (ROV
Jason II) and 7 min (ROV Global Explorer), no movement of
any part of the fish could be detected even when
approached or touched by the underwater vehicle (see
Supporting On-Line Material cited below). These data are
thus consistent with lie-in-wait predators in general and
especially other members of the family Lophiidae (e.g.,
Lophiodes beroe) that are predictable constituents of the
deep-reef fish community of the region (Ross and Quattrini,
2007, 2009; Sulak et al., 2007). Although two of the
preserved specimens from outside of the Gulf of Mexico
were taken at somewhat shallower depths of 689 and 850 m
(NCSM 73401, from off Cape Canaveral; and USNM 214478,
Lesser Antilles), all those imaged by ROV or submersible in
the Gulf were found between 900 and 1200 m, despite
hundreds of submersible hours spent investigating similar
habitats on both sides of this depth range (CRF and SWR,
pers. obs.).
The known specimens of S. shaefersi (both preserved and
observed in situ) are, for the most part, large, ranging in
standard length from 146–790 mm (average length 418 mm),
roughly comparable to the adults of most other members of
the family Lophiidae (Caruso, 1981, 1983). Of those
individuals available for dissection (six preserved specimens,
146–397 mm), the smallest is a male, all remaining
specimens are females. In one in-situ observation (ROV
Global Explorer), however, there is a relatively tiny individ-
ual (less than one tenth the standard length of its
conspecific partner), which we believe is a male, resting on
top of the head of a much larger presumed female (its length
estimated as comparable to the largest of the specimens
observed in situ), the two together possibly representing a
mated pair (Fig. 2). The smaller individual is obviously
conspecific, the morphology and distinctive color pattern
closely matching that of the larger specimen. That the
smaller specimen might be a juvenile associated with a
parent or other large adult seems unlikely—lophiids are
broadcast spawners, their eggs spawned encapsulated within
a non-adhesive mucoid mass (often referred to as an egg raft)
that serves to distribute a large number of small eggs over
great geographical distances (Pietsch and Grobecker, 1987).
While juveniles might conceivably settle near the adults,
doing so would invite conspecific predation, and juveniles
of most other deep-reef associated fishes generally occur in
habitats away from the adults (Ross and Quattrini, 2007).
Furthermore, there is some precedent in lophiiform fishes
for sexual size differences, the ultimate condition exemplied
by the deep-sea Ceratioidei in which females may be more
than 60 times the length and about a half-a-million times as
heavy as the males (Pietsch, 2009). Less extreme examples,
however, are found in antennariids (Antennarius spp.) and
other lophiids (Lophiodes spp.). In the latter, the size
differences appear to be relatively small, but in all taxa
available for examination, the largest individuals were
female (Table 1).
Sexual size differences observed in antennariids, however,
are nearly comparable to the putative example described
here. Between June 2003 and May 2012, underwater
photographer Ellen Muller of Imagine Bonaire documented
18 spawning events in several species of Antennarius in which
the males in all cases were significantly smaller than the
females (see http://www.pbase.com/imagine/frogfishspawn;
Fig. 4A–C). Moreover, in many of these examples the male
was observed resting on top of the female. Another example,
recorded in August 2002 in the Lembeh Strait, North
Sulawesi, Indonesia, by Marna Zanoff and Chuck Boxwell
of Fish Tales Photography, shows an even greater size
difference between male and female, in this case the male
resting between her body and arm-like pectoral fin
(Fig. 4D). While definitive evidence is lacking, the available
data thus support a similar sexual dimorphism in Sladenia
shaefersi.
The habitat described here for Sladenia shaefersi may be
characteristic of the genus as a whole. Similar in-situ
sightings of Sladenia (probably S. gardineri) on hard bottoms
near hydrothermal vents have been recorded from the
central North Pacific Ocean. Several images, dating back to
2003, are available on the Internet, taken on Kingman Reef
in the Northern Line Islands and off the Hawaiian Islands.
The most recent photographs were taken near the summit of
the active submarine volcano Loihi Seamount about 35 km
off the southeast coast of the island of Hawaii in a depth
range of 1000–1500 m, and on the flanks of the island itself,
as shallow as 300 m. These images, taken during Woods
Hole Oceanographic Institution cruise TN-293, using ROV
Jason II aboard the R/V Thomas G.Thompson, 16 March–1
April 2013, are very similar to those reproduced here.
Surprisingly, researchers have ‘‘been seeing them for over
20 years while working at Loihi Seamount’’ (Craig L. Moyer,
pers comm., 3 May 2013).
SUPPORTING ONLINE MATERIAL
In-situ video of Sladenia shaefersi in the northern Gulf of
Mexico, ROV Jason II, 16 June 2007: http://oceanexplorer.
Table 1. Sexual Size Differences in Three Species of the Lophiid Genus Lophiodes.
Taxon Lophiodes caulinaris Lophiodes kempi Lophiodes reticulatus
Sex Males Females Males Females Males Females
n15 24 12 16 40 25
Maximum SL (mm) 224 240 129 202 177 246
Mean SL (mm) 133 171 113 139 128 131
Pietsch et al.—Deep-sea Goosefish, Sladenia shaefersi 663

Fig. 4. Spawning pairs of antennariids showing small males associated with larger females: (A) male nudging female swollen with eggs, 8 March
2005; (B) about an hour before spawning, March 2012; (C) moments before spawning, March 2012; (D) tiny green male beneath gravid female,
moments before spawning, March 2012; (E) male prodding female, moments before spawning, 5 June 2009; (F) female with tiny male resting
between her body and arm-like pectoral fin, August 2002 (A–E: Antennarius multiocellatus, Bonaire, Netherlands Antilles, E2003–2012 Ellen Muller,
Imagine Bonaire, http://www.pbase.com/imagine/profile; F: Antennarius commerson, Lembeh Strait, North Sulawesi, Indonesia, E2002 Chuck
Boxwell, Fish Tales Photography, www.fishtalesphoto.com).
664 Copeia 2013, No. 4

noaa.gov/okeanos/explorations/ex1202/logs/dailyupdates/
media/movies/highlights0424_video.html
In-situ video of spawning of Antennarius multiocellatus,
Bonaire, Dutch Antilles, 4 September 2006, courtesy of Ellen
Muller: https://www.youtube.com/watch?v5MKBo05GoY5w
ACKNOWLEDGMENTS
We thank the following for ship support and underwater
vehicle time: Schmidt Ocean Institute and the Gulf of
Mexico Research Initiative ECOGIG program (Falkor cruise),
NOAA Office of Ocean Exploration and Research and the
Bureau of Ocean Energy Management (Ronald H. Brown and
Okeanos Explorer cruises), NOAA Deep-Sea Coral Research
and Technology Program (2009 Seward Johnson cruise). We
also thank W. Anderson and A. Harold (GMBL), A. Prokofiev
and K. Vasilieva (ZMMU), M. Rhode (UNCW), D. Sepu´ lveda
(CNPE-IBUNAM), and J. Williams and D. Pitassy (USNM) for
help with preserved specimens. Special thanks to Ellen
Muller (www.pbase.com/imagine/profile) and Marna Zanoff
and Chuck Boxwell (www.fishtalesphoto.com) for permis-
sion to reproduce their photos of antennariids.
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