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Octopus Senescence:
The Beginning of the End
Roland C. Anderson
The Seattle Aquarium
Seattle, Washington
James B. Wood
National Resource Center for Cephalopods
University of Texas Medical Branch
Ruth A. Byrne
Department of XXX
University of Vienna
Senescence is a normal stage of an octopus’s life cycle that often occurs before death.
Some of the following symptoms typify it: lack of feeding, retraction of skin around
the eyes, uncoordinated movement, increased undirected activity, and white
unhealing lesions on the body. There is inter- and intraspecific variability. Senes
-
cence is not a disease or a result of disease, although diseases can also be a symptom of
it. Both males and females go through a senescent stage before dying—the males after
mating, the females while brooding eggs and after the eggs hatch. There are many as
-
pects of octopus senescence that have not yet been studied. This study discusses the
ecological implications of senescence.
A public aquarium or scientist frequently calls one of us about a sick octopus.
For example, a large male giant Pacific octopus (GPO), Enteroctopus dofleini,
held in captivity for 6 months is not eating and is losing weight. The octopus is
acting strange—not going into his lair and moving around the tank in the open
much of the time. As time progresses, his skin develops lesions, and this nonhu
-
JOURNAL OF APPLIED ANIMAL WELFARE SCIENCE, 5(4), 275–283
Copyright © 2002, Lawrence Erlbaum Associates, Inc.
Requests for reprints should be sent to Roland C. Anderson, The Seattle Aquarium, 1483 Alaskan
Way, Seattle, WA 98101. E-mail: roland.anderson@seattle.gov
man animal loses coordination. People notice, and, inevitably, they start asking
about the welfare of the animal. We have seen this pattern before. For example,
at The Seattle Aquarium a GPO named Clyde (in honor of the cephalopod biolo
-
gist Dr. Clyde Roper) weighed 18 kg when he was collected. He thrived in cap
-
tivity for 5 months and grew to a size of 32 kg but then stopped eating. He lost
10 kg over 2½ months, 32% of his body weight, before dying. He crawled all
over his tank, even into stinging sea anemones that he normally avoided. His
eyes were prominent and seemed larger than normal. This animal had the symp
-
toms of octopus senescence, a precursor to his death.
To understand octopus senescence, it is necessary first to understand the life
history of octopuses. We are familiar with the reproductive patterns typical of
mammals; they can reproduce several times during their life span; that is, they are
iteroparous. Almost all octopuses are semelparous, meaning they reproduce once
and then die (Mangold, 1987). Salmon, cicadas, and century plants are other exam
-
ples of semelparous organisms (Stearns, 1992).
Many animals have life spans that last many years. In general, mollusks other
than cephalopods are smaller but often live for many years (Morton, 1967). Powell
and Cummins (1985) reported several gastropods and bivalves who live for more
than 50 years. However, cephalopods “live fast and die young,” a motto O’Dor and
Webber (1986) borrowed from the Hell’s Angels and applied to cephalopods.
Even the GPO, who frequently reach a size of 50 kg, only live about 3 years
(Hartwick, 1983). The very small sepiolid Idiosepius pygmaeus lives for only 80
days (Lewis & Choat, 1993). Most other octopuses only live a year (Hanlon &
Messenger, 1996), although this depends on size at maturity and temperature at
which the species lives. Animals who mature at large sizes and live in colder water
tend to have longer life spans (Wood & O’Dor, 2000).
Octopuses are born, grow rapidly, mature, mate, and—if female—brood eggs.
Then they die. Males generally die about the same time as the females (Hanlon,
1983a; Mangold, 1983a; Van Heukelem, 1983), but male GPOs (Hartwick, 1983)
and O. vulgaris (Mangold, 1983b) may live longer than females. Death may be pro
-
longed into a senescent state, but for most species it is inevitable once an octopus has
reproduced. In the wild, a senescent octopus who is not camouflaged and who is
moving around inordinately is likely to quickly become part of the food chain.
Senescence occurs at the end of a mature octopus’s natural life span and often
lasts for a period of a month or more. However, there are other reasons octopuses
may experience senescence-like symptoms that are animal welfare issues. Poor
water quality (lack of dissolved oxygen, low pH, pollutants), incorrect tempera
-
ture, collecting stress, and disease (Budelmann, 1998) also can cause these symp
-
toms and even death in captive octopuses.
The physiological processes by which senescence occurs are fairly well known
(Tait, 1986, 1987). The process is driven by secretions from the optic gland (Tait,
1987; Wodinsky, 1977) that elicit ripening of the reproductive organs, inactivation
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ANDERSON, WOOD, BYRNE
of the posterior salivary and digestive glands, and cessation of appetite, which nor
-
mally causes death by starvation after reproduction. Activation of the optic gland
appears to be affected by environmental factors such as light, temperature, and nu
-
trition that, thus, ultimately control reproduction and life span (Van Heukelem,
1979). The behavioral aspects of senescence have been less remarked on but have
been casually known for millennia. Aristotle stated, “[T]he females after giving
birth … become stupid, and are not aware of being tossed about in the water, but it
is easy to dive and catch them by hand” (cited in Balme, 1991, p. XXX).
The purpose of this article is to document the indicators of senescence, both
physical and behavioral, that we have observed in several cold, temperate, and
tropical octopuses. We hope that knowledge of the senescence phenomenon will
help aquarists and researchers understand what is happening to their animals as
they grow old. We cite what is known about octopus senescence. Such knowledge
is perforce limited, and we draw on our own observations to expand the knowledge
of its occurrence.
SYMPTOMS OF SENESCENCE
Four conditions or activities are all indicators of octopus senescence. These are
(a) loss of appetite and lack of feeding leading to weight loss, (b) retraction of
the skin around the eye, (c) undirected or uncoordinated activity, and (d) the oc-
currence of white lesions on the skin.
Many researchers and aquarists have noted the loss of appetite in both male
and female octopuses at this stage, and it is fairly well documented (Cortez, Cas-
tro, & Guerra, 1995; Hanlon, 1983a, 1983b; Joll, 1983; Mangold, 1983; Tait,
1986, 1987; Van Heukelem, 1977, 1979; Wodinsky, 1977, 1978). It has been
posited that such fasting is what inevitably leads to the animal’s death by starva
-
tion (Tait, 1987).
The eyes of octopuses stay the same size while the body shrinks as the animal
loses weight. This causes the skin around the eyes to retreat, making the eyes more
visible.
The increased activity at the start of senescence is undirected activity (particu
-
larly in males). It is not hunting, foraging, or performing other activities with a pur
-
pose. O’Dor and Wells (1978) showed that both starved and senescent female
octopuses used dissolution of muscle tissue as fuel, which kept the metabolic rate
at an unnaturally high level. A study on activity patterns of Octopus vulgaris at the
Konrad Lorenz Institute showed that senescent males were statistically more ac
-
tive than normal males (Meisel, 2002). The undirected activity of senescent males
should not be confused with perseverating activity (“pacing”) of bored octo
-
puses—this may be alleviated with proper environmental enrichment (Anderson
& Wood, 2001; Dickel, Boal, & Budelmann, 2000; Wood & Wood, 1999) as it is
THE BEGINNING OF THE END 277
in other animals (Shephardson, 1998). This undirected activity may be related to
mate searching. It is not known whether senescent males can still successfully
mate a female, whether they still have spermatophores, or whether they have the
“mental capacity” to mate.
The occurrence of white lesions on a senescent octopus has been the subject of
controversy and discussion (Budelmann, 1998; Reimschuessel & Stoskopf, 1990).
A young octopus, in good condition and in good water quality, can sustain an in
-
jury that may cause such lesions. However, Hanlon (1983a) remarked that the skin
deteriorates during the 2- to 4-week senescence of both male and female O.
briareus. “Skin damage usually leads to infection only in old animals” (Mangold,
1983b, p. 359). Van Heukelem (1977) stated that the healing processes of octo
-
puses are shut off during senescence, so skin injuries may become secondarily in
-
fected with Aeromonas, Vibrio, and Staphylococcus bacteria (Reimschuessel &
Stoskopf, 1990).
MALE SENESCENCE
A male octopus’s senescent condition begins after maturity. A male may mate
more than one female and may mate the same female more than once (Mangold,
1983b). There is evidence that both sexes are promiscuous and that there is
sperm competition among males (Cigliano, 1995; Mangold, 1987). Males may
use their spatulate ligulas on their third right arms to remove another male’s
stored sperm in a female (Hanlon & Messenger, 1996). A male’s supply of sper-
matophores (sperm packets he passes into the female) may be limited. Whether
they can make more and how long it would take them to do so if they can is un
-
known, but “mating is highly unlikely to exhaust males (referring to Octopus
vulgaris)” (p. XXX), according to Mangold (1983b).
Other octopus species have a very limited number of spermatophores at any one
time, which may limit their chance to mate successfully. GPOs have only 10 sper
-
matophores (Mann, Martin, & Thiebsch, 1970), and the deep-sea octopus
Bathypolypus arcticus typically has only 3 or 4 (O’Dor & Macalaster, 1983) avail
-
able for use. Although it has been reported that there is permanent production and
release of spermatophores in male Octopus vulgaris (Mangold, 1983b), it is not
known if this is true for other species or if it occurs after the onset of senescence.
Male and female octopuses both go into senescence, but females typically
brood fertile eggs during this time, an activity with a clear and necessary reproduc
-
tive purpose. Unlike in females, senescence in male octopuses occurs without as
clear a sign that they are at the end of their lives. The best sign that males are be
-
coming senescent is their lack of appetite. They stop eating, and their bodies begin
to deteriorate. They can survive a surprisingly long time without eating. At The Se
-
attle Aquarium, male GPOs (N = 7) stopped eating a mean of 48 days (range = 14
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ANDERSON, WOOD, BYRNE
to 76 days) and lost a mean 17.4% of their body weight (range = 4.3% to 32.1%)
before dying. Gabe’s (1975) male GPO died 54 days after mating.
At the Konrad Lorenz Institute, senescence was monitored in three male O.
vulgaris. They stopped eating a mean of 131 days (range = 79 to 188 days) before
dying. They did not stop eating suddenly but gradually ate less and less. Two of the
O. vulgaris had small white lesions for 248 and 257 days before their deaths; these
lesions increased in number and size prior to death. An O. macropus died 165 days
after his last mating. During this time, he rarely ate the food given, and was never
seen during the day, but was very active at night, mostly swimming and jetting.
Undirected activity of a senescent male octopus is likely to get him in trouble by
exposing him to predators. Senescent males are much more likely to escape from
captivity because of their increased activity (personal observation), and senescent
male GPOs and Octopus rubescens are frequently found crawling out of the water
onto the beach. Senescent males have been found even in river mouths, going up
-
stream (personal observation).
A study on the biorhythms of O. vulgaris showed that a senescent male animal
spent 80% of his time active, compared to three subadult males who spent an aver-
age 41% of their time active (Meisel, 2002).
Undirected movement of senescent male octopuses is also frequently observed
with uncoordinated activity. They look as if they have forgotten how to crawl or
swim properly; they lose their balance and appear to “trip” over their own arms,
and they do not seem to control their own bodies. Senescent octopuses may even
eat their own arms. Again, this is different from the bacteria-caused disease that
causes autophagy in previously healthy octopuses of any age (Budelmann, 1998).
In a study of visual control of arm movements in O. vulgaris, it was possible to
see the progression of one animal toward senescent behavior (U. Griebel, personal
communication, May 1, 2002). The animals were presented a transparent plexiglas
T-maze. The octopuses had to learn to look first and then make the right choice for
the reward. Before senescence, one male performed 68% of the right choices; af
-
terward, however, he fell back to chance level (48%). Not only did the animal’s
performance decrease, but so did his willingness to perform the trials.
FEMALE SENESCENCE
Although the term senescence typically is used in referring to the condition in
male octopuses, females also may develop signs of senescence. Senescence in
females is especially apparent in those who are brooding eggs, have survived af
-
ter the eggs hatched, or are removed from their eggs. While brooding eggs, fe
-
males do not leave them, and they reduce or stop feeding (Mangold, 1987). They
guard the eggs from predators and clean and oxygenate their eggs (Cosgrove,
1993; Gabe, 1975). To provide the energy to do this, they metabolize their own
THE BEGINNING OF THE END 279
bodies. In the wild, female GPOs lost 50% to 71% of their body weight while
brooding eggs (Cosgrove, 1993). In captivity, female Octopus mimus lost 25%
of their body weight (Cortez et al., 1995); O. cyanea, 36% (Van Heukelem,
1976); and O. vulgaris, 50% (O’Dor & Wells, 1987). At The Seattle Aquarium,
female GPOs lost a mean of 49.5% of body weight, whereas female O.
rubescens lost a mean 50.3% of their body weight before dying.
If a female survives after her eggs have hatched, she will be senescent. She
probably will not eat, she may not shelter in a den, and she will not behave like a
healthy octopus because she is dying. There are a few exceptions to this general
pattern. Several female GPOs have been reported to continue to eat during the first
part of egg guarding as have a few Octopus vulgaris (Mangold, 1983b). Tait
(1987) exclaimed, “There is no such thing as a ‘typical octopus!’” (p. XXX). There
are a few species like O. chierchiae who lay more than one batch of eggs and con
-
tinue to feed and grow between batches of eggs (Rodaniche, 1984). However, the
typical pattern is for females to die when their eggs hatch. They already show some
symptoms of senescence similar to males while they are brooding, and those who
survive past brooding act in the same way as senescent males.
Most cephalopods held in captivity who do not have a chance to mate will not
spawn normally (Boyle, 1991). Most researchers do not keep adult octopuses to-
gether as they are cannibalistic (Hanlon & Forsythe, 1985); under such conditions,
females are much more likely to lay infertile eggs or not lay eggs. Egg-bound fe-
males do not appear to have a longer life span (Boyle, 1991). We have observed that
the unmated females of some species (Enteroctopus dofleini, Octopus briareus, O.
vulgaris, and Bathypolypus arcticus) lay infertile eggs and also become senescent.
They stopped eating; laid scattered, infertile eggs (unlike the dense egg mass of a
normal female); or laid and brooded infertile eggs. If they are not brooding, they of
-
ten are more active, out in the open, and noticeably physically deteriorating.
DISCUSSION
The life history stage of senescence prior to dying is typical for many cephalo
-
pods but not other mollusks. Senescence is likely part of an adaptive program
that is hormonally regulated in this class (Tait, 1986). Hormonal control of octo
-
puses’ life cycles has been fairly well studied (Mangold, 1987), and senescence
is a direct result of such control (Tait, 1986). Wodinsky (1977) found that re
-
moval of optic glands in female Octopus filosus made them cease brooding, start
feeding again, and live longer than normal. This experiment has not yet been
performed on male octopuses. If it were, it might be possible to grow a
“supermale” who lives longer and grows larger than normal. Such features
would be valued by public aquariums where octopuses are popular display ani
-
mals (Carlson & Delbeek, 1999).
280
ANDERSON, WOOD, BYRNE
Many aquarists have observed and remarked on the increased activity of some
senescent male octopuses (Anderson, 1987; Anderson & Martin, 2002). Such ac
-
tivity may lead to a greater propensity to escape an enclosure. We do not know if
senescent males still (a) can mate, (b) possess viable sperm and spermatophores,
and (c) can produce more spermatophores—and, if so, for how long once they
have reached senescence. Their activity during senescence may be related to an in
-
creased urge to mate. Because senescent males will soon die, they may have little
to lose, and their best strategy to pass on their genes may be to seek further oppor
-
tunities to mate by being more active.
At the end of life, the brooding behavior of females is clearly a necessary com
-
ponent of reproduction for octopuses. Female octopuses likely must balance en
-
ergy allocated to both producing eggs and maintaining enough energy to brood
their offspring until they hatch. In an uncertain world, the potential loss of an entire
brood likely has a much stronger effect on evolutionary strategy than the lost
chance for producing a few more eggs. This would select female octopuses to err
slightly on the side of having too much energy resources, which would lead them
to survive occasionally past the brooding period. However, we have observed that
brooding females who are removed from their eggs act senescent but still are able
to brood if replaced back on them.
A few species of octopuses are iteroparous (Rodaniche, 1984) as are Nautilus
(Ward, 1987) and many other species of mollusks (Morton, 1967). However, most
octopuses are constrained to a semelparous life cycle that may end in senescence.
Such a pattern may be adaptive. Semelparity has the benefits of producing more
offspring and producing them quickly, both of which increase fitness (Stearns,
1992). Young octopuses are particularly capable of efficient assimilation of in-
gested food and very fast growth rates (Mangold, 1983b). Therefore, they are able
to reach maturity quickly. Thus, senescence and death at a young age are the costs
of such a strategy.
There is still much we do not know about octopus senescence, and there are many
opportunities for future research. The onset and duration of senescence need to be
documented in other species. The condition of naturally dying animals, state of in
-
ternal organs, number of spermatophores in males, ability to mate, and the correla
-
tion with hormonal systems need to be further researched. The factors that cause
somefemalestocontinue eatingafter egg-layingor egg-hatchingneed tobe studied.
There are implications for aquarium husbandry of senescent octopuses. It is im
-
portant for those who keep octopuses and work with them to understand that these
cephalopods are short-lived animals and that the senescence stage is a significant
part of their life cycle. It is critical to recognize the symptoms of senescence and be
able to differentiate them from other husbandry problems related to diseases, in
-
fections, injuries, and the effects of poor water quality. Research on octopus physi
-
ology, growth, and behavior will be confounded if senescent animals are used in
experiments.
THE BEGINNING OF THE END 281
Senescent octopuses in the wild probably do not live long due to the added risk
of predation, but senescence may be extended in the laboratory or public aquarium
(the so-called laboratory artifact). Senescent animals are acting normal for their
life stage, but this behavior is not normal relative to the rest of their lives. Octopus
keepers need to realize this and make amends for it. Senescent male octopuses may
make good public aquarium displays (Anderson, 1987). They are active and do not
require much, if any, food. However, octopus keepers need to realize that such ac
-
tivity and lack of appetite of a large, old octopus is the beginning of the end.
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