Abstract
Octopuses
typically have a single reproductive period and then they die
(semelparity). Once a clutch of fertilized eggs has been produced, the
female protects and tends them until they hatch. In most shallow-water
species this period of parental care can last from 1 to 3 months, but
very little is known about the brooding of deep-living species. In the
cold, dark waters of the deep ocean, metabolic processes are often
slower than their counterparts at shallower depths. Extrapolations from
data on shallow-water octopus species suggest that lower temperatures
would prolong embryonic development periods. Likewise, laboratory
studies have linked lower temperatures to longer brooding periods in
cephalopods, but direct evidence has not been available. We found an
opportunity to directly measure the brooding period of the deep-sea
octopus
Graneledone boreopacifica, in its natural habitat. At
53 months, it is by far the longest egg-brooding period ever reported
for any animal species. These surprising results emphasize the selective
value of prolonged embryonic development in order to produce
competitive hatchlings. They also extend the known boundaries of
physiological adaptations for life in the deep sea.
Figures
Citation: Robison B, Seibel B, Drazen J (2014) Deep-Sea Octopus (
Graneledone boreopacifica) Conducts the Longest-Known Egg-Brooding Period of Any Animal. PLoS ONE 9(7):
e103437.
doi:10.1371/journal.pone.0103437
Editor: Erik V. Thuesen, The Evergreen State College, United States of America
Received: May 22, 2014;
Accepted: July 2, 2014;
Published: July 30, 2014
Copyright: © 2014 Robison et al. This is an open-access article distributed under the terms of the
Creative Commons Attribution License,
which permits unrestricted use, distribution, and reproduction in any
medium, provided the original author and source are credited.
Data Availability: The
authors confirm that all data underlying the findings are fully
available without restriction. All relevant data are contained within
the paper.
Funding: This research was funded by the Monterey Bay Aquarium Research Institute (
www.mbari.org) as a research project (#901220) led by author BR; MBARI is funded by the David and Lucile Packard Foundation (
www.packard.org). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Introduction
In
April of 2007 we used a remotely operated vehicle (ROV) to inspect an
isolated rocky outcrop, 1397 m deep, at the sediment-covered base of a
sloping wall in the Monterey Submarine Canyon, off central California.
We had visited the site several times before and knew it to be a
location where females of
Graneledone boreopacifica Nesis 1982,
attach and brood their eggs. On this occasion we found no brooding
individuals on the rock. However, on the sediment nearby we observed a
solitary octopus moving slowly toward the exposed hard substrate.
When
we returned to the site 38 days later, in May, 2007, we found the same
individual octopus, easily identified by characteristic scars, up on the
rock and guarding a clutch of attached eggs (
Figure 1).
Given this singular opportunity to measure the length of a brooding
period from its inception, we returned to the site 18 times over the
ensuing four-and-a-half years. Each time we returned we found the same
octopus (
Figure 2)
clinging to the vertical rock face, arms curled, covering her eggs.
Continuous growth of the eggs provided evidence that it was the same
clutch throughout (
Figure 3).
In general, octopods are believed to cease or to greatly reduce feeding when they brood
[1]–
[4]. For
Graneledone, there is no evidence that females feed while brooding
[5].
Potential prey in the form of Lithodid crabs and Pandalid shrimps were
frequently in close attendance around the brooding female that we
monitored. However, the only interactions we observed were when she
pushed these crustaceans away as they stepped within her watch circle.
In laboratory brooding studies, the deep-living octopus
Bathypolypus arcticus occasionally accepted food that was offered by hand
[2]. But in situ, the brooding
Graneledone ignored pieces of crab when we offered them to her with the manipulator of the ROV.
During
the periods when we had the female under observation, she never left
the eggs unattended; but our presence included only a small fraction of
the protracted brooding period. While the proximity of our ROV was
surely conspicuous because of its lights and vibrations, we never
disturbed the brooder mechanically. On two occasions we used the reverse
water flow of our suction sampler to gently lift the web between her
arms so that we could view some of the eggs for laser-referenced size
measurements. While she occasionally shifted her position slightly, or
uncurled and lifted one or two arms, the female always remained centered
over the clutch of eggs.
Results
The eggs of
G. boreopacifica are elongate vesicles which taper to short stalks that the mother cements to hard substrate
[3].
The chorion tissue comprising the vesicle allows the exchange of oxygen
and thus maternal care is necessary to prevent fouling and suffocation
[6]. Expansion of the chorion during development permits growth
[7]
but its pliability renders the capsule vulnerable to predation unless
the eggs are protected. We measured the size of exposed eggs several
times over the course of the brooding period (
Figure 3).
Egg capsule sizes started at 1.5 cm (length)×0.5 cm (diameter) and
reached 3.3 cm×1.6 cm a month before hatching. By the 40th month the
shapes of the young octopuses inside, were clearly apparent (
Figure 4). Hatchlings of
G. boreopacifica are the largest and most developmentally advanced coleoid cephalopod hatchlings known to date
[7]. They emerge as virtual miniature adults, without a pelagic juvenile phase
[7].
When
the brooding female was first observed on the seafloor adjacent to the
rock outcrop, the skin of her mantle was highly textured and pallid
purple in color; when she began brooding it became pale, almost white.
Indeed, on several occasions as the ROV approached the rock, the first
thing visible was the pale body of the brooder, standing out against the
dark background. Signs of advancing senescence
[3],
[5]
included diminishing size and tumescence of the mantle, loss of skin
texture, cloudy eyes, slack skin, and a loss of pigmentation on the oral
surface of the arms.
In
September of 2011 the brooding female and her eggs were still in place.
When we returned in October of 2011 she was gone and the rock face she
had occupied held the tattered remnants of empty egg capsules (
Figure 5).
Thus the total length of the brooding period we measured was from May,
2007 to September, 2011, or 53 months. From HD video frame grabs of the
empty capsules and the characteristic green cement of their anchor
points
[3] we estimate the clutch size to have been between 155 and 165 eggs.
The
rock shelf that holds the brooding site runs generally east to west,
parallel to the axis of this part of the canyon. The rock face where the
octopus placed her eggs is in the lee of sediment flow down the slope
of the canyon wall, and parallel to but protected from down-canyon
currents. The brooding spot was about one meter above the seafloor
sediment and about three meters below the crown of the rocky shelf. We
never observed sediment build-up within the small, protected alcove
although the canyon is subject to considerable sediment flow
[8].
Exposures of hard substrate are rare in this part of the canyon and
this rock was occupied by a number of other invertebrate species, both
attached and mobile. During the course of our observations the
temperature ranged from 2.8°C to 3.4°C.
Discussion
Aggregations of egg-brooding
G. boreopacifica
have been found elsewhere in the eastern North Pacific, clinging to the
vertical faces of rock outcrops where elevated currents reduce
sedimentation and promote ventilation of the eggs
[3],
[9]. In years prior to the present series of observations, we encountered two specimens of
G. boreopacifica
brooding eggs at different locations on the same outcrop in Monterey
Canyon. These females were observed in place for 8 months and 20 months
but we have no measure of the beginning or end of their full brooding
periods. While brooding females are seen routinely at depths between
1200 and 2000 m, we have never observed unattended clutches of
G. boreopacifica eggs.
Most, if not all incirrate octopods are believed to brood their eggs
[7],
[10]–
[12].
This is part of a holobenthic reproductive strategy that includes
direct development without a larval stage. There is considerable
variability in reproductive behavior among octopod species from
different habitats; but protection of eggs during development is
paramount and universal so far as is known. In shallow-water species the
eggs are often clustered within a den, where they are guarded and
ventilated by the female. In pelagic species, brooding is accomplished
with the female holding the developing eggs, usually within her arms.
Brooding deep-sea squids also hold their eggs with their arms
[13],
[14], apparently without feeding. Compared with shallow-water species, the eggs of
G. boreopacifica
are relatively large, while the clutch size is relatively small; both
traits are characteristic of a strategy that maximizes the production of
developmentally advanced hatchlings
[7].
The 53-month brooding period that we measured considerably exceeds all such records in the literature (Table S1 in
Information S1). Previously, the longest octopus brooding known was 14 months, attributed to
Bathypolypus arcticus on the basis of specimens kept in the laboratory
[2] at 7°C. The longest guarded incubation known for fish eggs is 4–5 months, by the Magellan Plunder Fish
Harpagifer bispinis in Antarctic waters
[15]. For birds, the longest uninterrupted egg brooding is 2 months, by the Emperor Penguin
[16]. Among live-bearing species, elephants gestate for 20 to 21 months
[17], frilled sharks carry their embryos internally for about 42 months
[18], and the internal gestation period of alpine salamanders can reach 48 months
[19] before birth.
The
prolonged brooding period that we measured is a consequence of two
interacting factors, low temperature, and the selective advantage of
producing highly-developed hatchlings. Marine ectotherms typically
exhibit an inverse relationship between environmental temperature and
the duration of embryonic development
[6]. Such a pattern is evident in the semelparous, bathypelagic mysid crustacean
Gnathophausia ingens, which also has a protracted brooding period of 20 months, hatches miniature adults, and does not feed during brooding
[20].
In octopods, development time equates to brooding period and this
brings a third factor into play, the brooding parent. In the deep ocean,
low temperatures are typical, and thus the trade-off within the
reproductive strategy of deep-living octopods is between the mother’s
ability to endure a long brooding period, and the competitiveness of her
hatchlings.
Graneledone boreopacifica produces hatchlings that are very highly developed, which gives them the advantage of a high potential for survival
[7].
The ultimate fate of a brooding female octopus is invariably death, but
in this first example from the deep-sea, brooding also confers an
extension of adult life that greatly exceeds most projections of
cephalopod longevity.
Most
previous attempts to model the duration of embryonic development of
cephalopods at colder temperatures failed to predict the extended
brooding period demonstrated here (Table S1 in
Information S1).
Interspecific models accounting for variation in egg size and
temperature predict anywhere from 2.8 to 75 months for development when
applied to
G. boreopacifica. We show here that much of the interspecific variation in development time can be attributed to temperature (
Figure 6).
Egg size is also linked to temperature, with longer development
yielding larger eggs and more completely developed hatchlings (
Figure 7). However, with one exception (Table S1 in
Information S1), extrapolation of existing models to 3°C still underestimates measured development in
G. boreopacifica by nearly a year.
The
principal question now remaining is how does the mother survive for so
long? Low temperatures and inactivity help by keeping metabolic demand
low. We saw no evidence of feeding during brooding. The only examination
of a brooding female in the literature showed an empty gut
[5].
It is certainly possible that the mother feeds on the surrounding fauna
or that in the course of protecting her eggs she feeds on would-be egg
predators like Lithodid crabs. Resorption of unlaid eggs is known in
other species, as is feeding on unfertilized or diseased eggs
[2],
[3],
[21],
[22].
Among deep-sea squids, species that brood their eggs rely on digestive
gland lipid stores to meet their extended nutritional needs
[13],
[14], but octopods are not known to store lipid as extensively. Regardless of how their nutritional needs are met, female
G. boreopacifica spend a long time brooding. The entire lifespan of most shallow-water cephalopod species is less than 2 years
[1],
[11]. If
G. boreopacifica conforms to the general rule among octopods, that brooding comprises about a quarter of the lifespan
[10],
[23], then it, and possibly other deep-sea species, may be among the longest-lived of all cephalopods
[24].
While
the discovery of a 53-month brooding period is remarkable, this
reproductive strategy is not unusual, it is common and is clearly
successful because
G. boreopacifica is one of the most abundant deep-living octopods in the eastern North Pacific
[9],
[25],
[26].
These results only seem extraordinary when compared with well-studied
shallow-water species; which indicates how little we really know about
the deep sea.
This
study did not involve endangered or protected species. The location of
the study site was 36° 42′ N, 122° 03′ W, at a depth of 1397 meters.
Field work was conducted under NOAA Office of Marine Sanctuaries permit
MBNMS 2005-010-A3, and California Department of Fish and Wildlife
scientific collecting permit D-0004069542-0; no specimens were
collected.
Supporting Information
Information_S1.docx
Table S1, Measured and predicted development time for Graneledone boreopacifica
using published models. Hatching mass used in some models comes from
Voight and Drazen, 2004. Egg length (15 mm) and temperature (3°C) were
measured in situ. Table S2, Egg development and morphometric data for species of the family Octopodidae.
Table S1, Measured and predicted development time for Graneledone boreopacifica
using published models. Hatching mass used in some models comes from
Voight and Drazen, 2004. Egg length (15 mm) and temperature (3°C) were
measured in situ. Table S2, Egg development and morphometric data for species of the family Octopodidae.
doi:10.1371/journal.pone.0103437.s001
(DOCX)
Acknowledgments
We
thank MBARI’s ROV pilots and the officers and crews of the research
vessels Point Lobos and Western Flyer. We also thank Kim Reisenbichler,
Rob Sherlock and Kris Walz for their assistance at sea and ashore. We
thank J. Voight, V. Laptikhovsky and R. Villanueva for their helpful
reviews of the manuscript.
Author Contributions
Conceived
and designed the experiments: BR BS JD. Performed the experiments: BR.
Analyzed the data: BR BS JD. Contributed reagents/materials/analysis
tools: BR. Contributed to the writing of the manuscript: BR BS JD.
References
- 1.
Hanlon RT, Messenger JB (1996) Cephalopod Behavior. New York: Cambridge University Press. 256p.
- 2.
Wood JB, Kenchington E, O’Dor RK (1998) Reproduction and embryonic development time of Bathypolypus arcticus, a deep-sea octopod (Cephalopoda: Octopoda). Malacologia 39: 11–19.
- 3.
Voight JR, Grehan AJ (2000) Egg brooding by deep-sea octopuses in the North Pacific Ocean. Biol Bull 198: 94–100.
doi: 10.2307/1542807
- 4.
Nesis KN (1999) The duration of egg incubation in high-latitude and deep-sea cephalopods. Biolog Morya Vladivostok 25: 499–506.
- 5.
Voight JR (2008) Observations of deep-sea octopodid behavior from undersea vehicles. Amer Malacol Bull 24: 43–50.
doi: 10.4003/0740-2783-24.1.43
- 6.
Boletztky Sv (1994) Embryonic development of cephalopods at low temperatures. Antarctic Sci 6: 139–142.
- 7.
Voight JR, Drazen JC (2004) Hatchlings of the deep-sea octopus Graneledone boreopacifica are the largest and most advanced known. J Moll Stud 70: 406–408.
doi: 10.1093/mollus/70.4.400
- 8.
Paull
CK, Mitts P, Ussler W, Keaten R, Greene HG (2005) Trail of sand in
upper Monterey Canyon. Geo. Soc Amer Bull 117: 1134–1145.
doi: 10.1130/b25390.1
- 9.
Drazen
JC, Goffredi S K, Schlining B, Stakes DS (2003) Aggregations of
egg-brooding deep-sea fish and cephalopods on the Gorda Escarpment: a
reproductive hot spot. Biol Bull 205: 1–7.
doi: 10.2307/1543439
- 10.
Boletzky Sv (1987) Embryonic phase. In: Boyle PR, editor. Cephalopod Life Cycles, Vol. II. London. Academic Press. 5–31.
- 11.
Calow P (1987) Fact and theory. In: Boyle PR, editor. Cephalopod Life Cycles, Vol. II. London. Academic Press. 351–365.
- 12.
Rocha
F, Guerra A, Gonzalez AF (2001) A review of reproductive strategies in
cephalopods. Biol Rev Cambridge Philos Soc 76: 291–304.
doi: 10.1017/s1464793101005681
- 13.
Seibel BA, Robison BH, Haddock SHD (2005) Post-spawning egg care by a squid. Nature 438: 929.
doi: 10.1038/438929a
- 14.
Bush SL, Hoving HJT, Huffard CL, Robison BH, Zeidberg LD (2012) Brooding and sperm storage by the deep-sea squid Bathyteuthis berryi (Cephalopoda: Decapodiformes). J Mar Biol Assoc UK. 92: 1629–1636.
doi: 10.1017/s0025315411002165
- 15.
Daniels RA (1979) Nest guard replacement in the Antarctic fish Harpagifer bispinis: possible altruistic behavior. Science 205: 831–833.
doi: 10.1126/science.205.4408.831
- 16.
Kirkwood R, Robertson G (1997) The foraging ecology of female emperor penguins in winter. Ecol Monogr 67: 155–176.
doi: 10.2307/2963511
- 17.
Corse J (1799) Observations on the manners, habits and natural history of the elephant. Philos Trans 1799: 31–35.
doi: 10.1098/rstl.1799.0006
- 18.
Tanaka S, Shiobara Y, Hioki S, Abe H, Nishi G, et al. (1990) The reproductive biology of the frilled shark, Chlamydoselachus anguineus, from Suruga Bay, Japan. Jap J Ichth 37: 273–291.
- 19.
Miaud
C, Andreone F, Riberon A, De Michelis S, Clima V, et al. (2001)
Variations in age, size at maturity and gestation duration among two
neighbouring populations of the alpine salamander (Salamandra lanzai). J Zool Lond 254: 251–260.
doi: 10.1017/s0952836901000760
- 20.
Childress JJ, Price MH (1978) Growth rate of the bathypelagic crustacean Gnathophausia ingens (Mysidae: Lophogastridae). I. Dimensional growth and population structure. Mar Biol 50: 47–62.
doi: 10.1007/bf00390541
- 21.
Barratt
IM, Johnson MP, Allcock AL (2007) Fecundity and reproductive strategies
in deep-sea incirrate octopuses (Cephalopoda: Octopoda). Mar Biol 150:
387–398.
doi: 10.1007/s00227-006-0365-6
- 22.
Ibanez CM Keyl F (2010) Cannibalism in cephalopods. Rev Fish Biol Fisheries 20: 123–136.
doi: 10.1007/s11160-009-9129-y
- 23.
Mangold K (1987) Reproduction. In: Boyle PR, editor. Cephalopod Life Cycles, Vol. II. London. Academic Press. 157–200.
- 24.
Saunders WB (1984) Nautilus growth and longevity: Evidence from marked and recaptured animals. Science 224: 990–992.
doi: 10.1126/science.224.4652.990
- 25.
Pereyra
WT, Alton MS (1972) Distribution and relative abundance of
invertebrates off the Oregon coast. In: Pruter AT, Alverson DL, editors.
The Columbia River Estuary and Adjacent Ocean Waters. Seattle:
University of Washington Press. 444–474.
- 26.
Voight
JR (2002) When octopus abundance does not reflect prey availability:
Implications for gene flow. Bull Mar Sci 71: 1142–1143.
end quote from:
http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0103437
