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Behavioural Processes, 12 (1986) 383-388 383

Elsevier

Letter

IS THERE "PFIIN" IN INUERTEBRATES?

G. FIORITO
Evolution & Development of Behavior Res. Group
Neurobiology Department, Stazione Zoologica,
Uilla Comunale, 80121 Naples, Italy.
(Accepted 20 IJovenber 1985)
f?BSTRACT

Fiorito, G., 1936. Is there "pain" in Invertebrates?


Eehav. Processes,l2: 383-388.

In contrast to nociception, the perception of pain, or pain


experience, remains a subjective notion applicable to humans, but
untestable with animals. Yet, when defined operationally as a
physiological response induced in an animal by stimuli painful to
humans, and resulting in a protective stimulus avoidance response,
pain is amenable to testing with non-human subjects. This paper
considers a series of examples showing responses to stimuli that
are both painful Cnociceptive) and responsible for eliciting
natural self-preserving behavior in Invertebrates. Consideration
is also given to the evolution and,possible mechanism underlying
the "pain-system" in Invertebrates.

KEY WORDS: Pain; Behavior; Invertebrates; Emotional-processes;


Evolution.

Pain is a variable, subjective experience involving a


specific variety of sensations, called nociception. Its quality
and severity may be strongly modified by factors including
previous experience, non-nociceptive sensory information, and the
perceived significance of the stimulation. Considered as an
objective fact, pain corresponds to the activity of nociceptors as
a consequence of noxious stimulations. Subjective pain is, on the
other side, an empirical fact involving emotion and/or cognition;
it can be defined as an unpleasant sensory and emotional
experience associated with acutal or potential tissue damage
CZayan, 1986!* The unpleasant emotional qualities involved in pain
sensations and strong motivation to remove the source of noxious
stimulation generally appear to comprise the experience widely
known as suf.f.erin~. The occurrence of suffering in animals is
usually inferred from physiological and behavioral changes such as
flexor reflexes, blood pressure increase or vocalizations, all of
which are normal concomitants of severe pain in humans. The main
difficulty is that behavioral and/or hormonal records cannot be
interpreted as specific indicators of pain experience unless
neurophysiological indication of nociception is already available
in a given animal species IZayan, 19663. The very suggestion that
animals can suffer from certain stimulations implies that there is
inference from neural analogy with suffering from pain sensations
in humans. The inference of a pain-sense in animals, however,
appears progressively less defensible as one considers animals

0376-6357/86/$03,50 0 1986 Elsevier Science Publishers B.V. (Biomedical Division)


384

phyletically remote from humans. The hypothesis that Invertebrates


fael pain may be supported by analogies between nociception as it
is known in humans and as it is suggested in (higher1 Vertebrates.
Neural analogies are, however, a necessary but insufficient
condition for inferring that animals suffer CZayan, 1966?. Thus,
looking to the Invertebrates according to the standard reference
work on the structure and function of the nervous system of these
animals CBullock and Horridge, 19651, it appears fundamental to
search for behavioral indicators of p..a.:ln_~ex~er~_e.~.~e.

Although there is no conclusive proof as to whether an


Invertebrate can experience something akin to human pain,
experimental analysis of known examples of Invertebrate behavior
and physiology, may facilitate a rational decision.
For example, the quality and intensity of the motor responses
under conditions of passive touch may be indicative of the
emotional content of mechanical stimulations, e.g. according to
their intensity. In contrast to sea anemones (S.a,ear.tL.a gar_asit.Lc.a.?
and to echinoderms, gasteropod C!?gL~s&.a. d~~i.La.nsJ and cephalopod
cPctopus vu QLsEi?. 1 molluscs show different types of motor
reactions in the two ,conditions of active and passive tactile
stimulation CBuytendijk, 1953): sudden retraction of tentacles or
body appendices, escape responses and immobility with colour
change OF the body after being touched in condition of immobility;
adaptive avoidance and exploration of the same stimulus when
touched on the same tentacle in condition of spontaneous
locomotion. Similar results were obtained with Invertebrates and
Uertsbrates such as crustacean arthropods and blinded fish Esee
Zayan, 1371, for a comparative psychobiological analysisl; the
Fact that blinded octopusss made a difference between touching and
being touched raises the question whether Invertebrates feel pain.
Moreover, from the discharges of the chromatophores and other
responses indicative that cephalopods have emotions, both Pigron
Cl9303 and Buytendijk C19Y3) were of the opinion that octopuses
were sensitive to pain.

0 pain process may result from either internal or external


stimulation; Feeling or perceiving pain may produce a reaction to
minimize the stimulus. Thus, a suffering animal either withdraws
From or neutralizes the causative agent, and acts to protect
wounded parts from further injury; the individual may learn'to
avoid that agent in the future. Several kinds of behavioral
responses are involved in this process, including withdrawal,
aggression, learned avoidance or learned aggression. The potential
adaptive value of such responses is clear, even in Invertebrates.
However, the learning capacity of Invertebrates is considered to
limit the adaptive value of pain-activated learning because of its
high situational speciFicity [Eisemann et al., 19BY).
Uarious responses occur in a wide variety of motile organisms
Cincluding bacteria3 to detrimental stimuli such as heat,
electrical current, chemicals and mechanical compression or
restraint (Table 1). The occurrence of these reactions does not
in itself indicate any pain experience CBullock et al., 19771,
since they can be explained as excessive or abnormally patterned
non-nociceptive sensory input, activating the central nervous
system to produce avoidance or escape outputs CEisemann et al.,
19893. However, avoidance and withdrawal responses often accompany
pain in conscious humans and may be related to emotional sufPering
situations where animals are coping with a noxious stimulus.
The examples reported in table 1 illustrate adaptive
responses in order to minimize damage to the organism. This
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permit5 to consider the pain-system as one related to species-


typical behavior From the withdrawal category, and as a mechanism
related to adaptation, thus providing a continuum from
Invertebrates to Uertebrates, including humans.

TABLE 1
Behavioral effects of noxious stimulations on several Invertebrate
animals.

SPECIES REFERENCES STIMULI RESPONSES

E!eLY.~i..a
sP * mechanical Gill-withdrawal
Arahogs sP * Fl mechanical Leg-autotomy
SgulLlla !Ilant_is_ c electrical Body-flexion
CaCci.I!.ys.
med.Lt_eE.FlaneYs d mechanical Alarm-display
%_ag~a.W&z~a. b_i.o.g~&&.a e electrical Deimatic-reaction
!%z.& r?s.L_l.~re_r.a f electrical Autotomy

a - Kandel, 1979;
b - Eisner and Camazine, 1983;
c - Maldonado and Miralto, 1982;
d - Fiorito, 1985;
e - Zabala et al., 19B!t;
f - Nufiez et al., 1983;

Another continuum may be seen at the neurochemical leval. The


existence in Vertebrates of neuropeptides was discovered a long
time ago, and the chemical structures of some of them have been
known for about thirty years. Others, however, such as
morphinomimetic peptides were discovered only recently. Of all the
neuropeptides, it was the discovery of the qndogenous opioid
peptides that excited the greatest attention, and quite rightly
because it seemed likely that their action might be related to
pain mechanisms, in view of the analgesic role of opioid peptides
in humans. Discovery of endogenous peptides and their receptors in
various Invertebrates (Table 21 would seem to encourage the belief
that these animals can experience and modulate painful sensations.
Peptides OF the opioid family occur in species ranging From human
to TetEa-hymena CLe Roith et al., 19821. Uarious functions
regulating physiological and behavioral activities unconnected
with pain are mediated by endorphinergic system in Uertebrates.
The occurrence of such peptides in Invertebrates suggests that the
endogenous opioid system in Invertebrates may similarly function
in behavioral activities possibly related to pain.

It should be noted, however, that several experiments have


indicated a role for an opioid-like system in pain control and
modulation in Invertebrates. Crustaceans C%~.y.i.,lla ~zI3ti.s.and
Carcinus madi,te_~ra,n_~.u.sl
are opioid-sensitive; they show a decrease
in the threshold of a stereotyped response to an electrical
current when applied to the mouth, in the case of ZgyiAla.
(Maldonado and tliralto, 1982) or, as in Carcinus _, show loss of
reactivity to mechanical stimulation when injected with opioids.
Insects and other Invertebrates also show opioid sensitivity, as
indicated in table 2. So, it may be simplistic to state that
Invertebrate neurobiology does not involve a pain system in the
Uertebrates sense.
Flnother class of biochemicals, venoms, f qund in many taxa,
386

TABLE 2
Distribution of opioid-like activity in Invertebrates

TQXA REFERENCES

PROTOZOA
COELENTERATA
PLATYHELMINTES
EN
SP
EN-NX
z
c
MOLLUSCA SP-EN-OG d
ANELLIDA EN e
CRUSTACEA SP-EN-NX d,e
INSECTA SP-EN-OG d,e,f,g
UROCHORDATA SP d

EN - Enkephalin or Endorphin activity


SP - Substance P activity
NX - Naloxone sensitivity
qG - Opioid general sensitivity

a - Le Roith et al., 1982;


b - Grimmelikhuijzen et al., 1981;
c - Uenturini et al., 1981;
d - Greenberg and Price, 1983;
e - Fiorito, 1985;
f - Nufiez at al., 1983;
g - Zabala et al., 1989

also supports the evolutionary characteristic of the pain sense.


Uenom used for incapacitation of prey probably does not inflict
pain, as it may be disavantageous because pain may increase
struggling on the part of the prey: it is indeed when venoms are
painful that they can function in defense.

Pain sense may be involved in another class of defensive


mechanism. Leg autotomy has bean noted to occur in spiders when a
leg is pulled or injursd. Crabs exposed to a hot plate show leg
autotomy, probably to reduce the stimulation CFiorito, 19651. The
autotomy occurs consistently at the level of the coxa-trochanter
Joint near the base of the leg. A special mechanism provides for
minimization of bleeding at the side of leg detachment. Eisner and
Camazine (1983) showed that in some insects, such as Argiope,
autotomy is induced by honeybee venom and wasp venom as well as by
several venom components (serotonin, histamine, phospholipase A23
known to be responsible for the pain
characteristically elicited by venom inJections In humans.
Therefore, the sensing mechanism by which spiders detect injected
harmful chemicals such as venoms may be fundamentally similar to
the one that is coupled with the perception of pain in humans
CEisner and Camazine, 19831.

The evidence available until now from the neural organization


and behavior patterns in Invertebrates does not allow us to draw a
conclusive picture about the existence of a pain-system in these
animals. However, the role of opioid peptides in the regulation of
nociception, in the control of reactions produced by painful
stimuli, and in procuring analgesia as well as behavioral
responses (such . _ .,...
as escape , defenc.e , mobbing , avoidar?ce) to itI
makes it possible to conclude that some pain system has appeared
in Invertebrates.
387

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