AMER. ZOOL., 15:13-19 (1975).
Immunity in Decapod Crustaceans
HARRIETTE C. SCHAPIRO
Department of Biology, San Diego State University, San Diego, California 92182
SYNOPSIS. Immunity in the decapod crustaceans is surveyed. Types of immune responses
include encapsulation, phagocytosis with or without the aid of serum factors, bactericidins
active with or without the aid of hemocyte factors, hemagglutinins, hemolysins, agglutinins,
and precipitins. Immunity to gaffkemia in Panulirus interruptus is also discussed.
INTRODUCTION
The origins of investigations into invertebrate immunity are almost as ancient and
honorable as those of vertebrate immunity.
Three early giants in the field have been
most strikingly brought to life by some
comments of Bang (1967a) a few years ago.
"It is claimed that Metchnikov, who was originally an
embryologist, derived his ideas of phagocytosis from
observations on the transparent starfish embryo into
which he had inserted a splinter.
"One of his students, a good many years later, was a
Roumanian bacteriologist Cantacuzene, who loved to
spend his summer at the French seashore and there,
injected all kinds of bacteria into all available invertebrates.
"Another student of Metchnikov was Metalnikov,
who, after years of successful work on insect immunity, seems to have played a trumpet to caterpillars to see
if they changed their reaction to the injected bacteria.
Despite this vigorous start in one way or another, the
study of comparative pathology of invertebrates lost its
impetus."
The invertebrates took a back seat to the
vertebrates for a long time. Only the immune responses of insects continued to be
studied. A renaissance of comparative
pathology and immunity in the past few
years has led to a reevaluation and extension of much of this early work.
The general term invertebrate covers a
great number of phyla. Apparently, there is
a concomitantly wide range of responses
possible to a specific antigen. In fact, as will
be pointed out, different genera within an
order and even species within a genus may
respond differently to the identical antigen.
There have been many excellent reviews
of invertebrate immune reactions in the last
few years (Cushing, 1967; Bang, 19676,
1970, 1973; Rabin, 1970; Sindermann,
1971; Tripp, 1971).
The decapod crustaceans exhibit all of
the major forms of immunity observed in
the invertebrates. Thus, they can serve as a
model system, and this discussion will be
limited to one class—Crustacea—and in
particular, one order—decapoda.
Shrimp, crabs, crayfish, and lobsters are
of particular interest because of numerous
attempts to grow some of them under controlled mariculture conditions. Mariculture
for these organisms includes the use of elevated temperature to enhance growth rates
and crowding to decrease space requirements. Therefore, organisms under intensive culture will be under physiological
stress and more susceptible to disease. A
knowledge of defense mechanisms and
immune responses will be needed to
minimize the lethal effects of pathogens
and to maximize the yield of cultured organisms.
SHRIMP
Penaeid shrimp in the Gulf of Mexico are
This work is a result of research sponsored by heavily infected by trypanorhynchid cesNOAA Office Sea Grant, Department of Commerce, todes, Prochristianella penaei (Kruse, 1959).
under Grant #USDC 04-3-158-22. The U. S. Government is authorized to produce and distribute re- Approximately 90 to 95% of brown shrimp,
prints for governmental purposes, notwithstanding Penaeus aztecus, and white shrimp, P.
any copyright notation that may appear herein.
setiferus, are parasitized to the same extent.
13
14
HARRIETTE C. SCHAPIRO
However, individual brown shrimp consistently show higher concentrations of the
parasite than do white shrimp of comparable size (Aldrich, 1965). White shrimp respond to the presence of parasites in the
hepatopancreas by developing an increasingly dense cyst or capsule around the
parasites. The cyst is composed of numerous hemocytes, fibroblasts, and collagenlike fibers. The parasite is destroyed as the
inner layers of the cyst become necrotic.
Parasites in the hemocoel become encysted
but are not destroyed (Sparks and Fontaine, 1973).
CRABS
sponse seems non-specific since injections
of either erythrocyte type or saline increase
titers to RRBC to approximately 100 within
the first 2 days. Titers then decline to the
normal range (Pauley, 1973).
The shore crab clears Ti bacteriophage
faster on secondary challenge than on
primary challenge suggesting a memory response. The two crabs, surviving the entire
course of the experiment, clear 103 phage
particles in 42 and 70 days respectively.
After complete clearance and rechallenge
with 103 phage, clearance of the second
challenge is more rapid, 14 and 42 days
respectively. This is a 3- and 1.6-fold increase in the titer, respectively. The enhanced clearance occurs in the absence of
any neutralizing activity which suggests a
cellular mechanism of clearance (Taylor et
al., 1964; Nelstrop et al., 1968).
A naturally occurring, well-studied disease in crabs develops from an invasion of
the hemolymph of the shore crab, Carcinus
maenus, by a ciliate, Anophrys magii (Poisson,
1930). The ciliate becomes numerous and
CRAYFISH
replaces the hemocytes, and at death, the
hemolymph of the crab appears turbid due
Phagocytosis has been studied in the Auto high concentrations of ciliates. The stralian crayfish or "yabbie," Parachaeraps
serum of the spider crab, Maia squinado, bicarinatus. The only organs to contain visinormally contains an agglutinin which im- ble accumulations of carbon, following inmobilizes the ciliate; the agglutination reac- jection of carbon into the ventral abdomition is protective in some way. The aggluti- nal sinus, are the gills and hepatopancreas.
nin is lost from the serum of the spider crab In the gills, the carbon is not associated with
just before a molt, such that spider crabs cells but appears to be suspended in the
without the agglutinin are killed by ciliate vascular spaces. In the hepatopancreas,
infections as are shore crabs (Bang, 19676). carbon is taken up by cells in the vessel walls
In this case, the physiological state of an of the digestive diverticula as soon as 1 min
animal with respect to the molt cycle affects after injection. Three hours after injection,
its susceptibility to disease.
all of these cells are tightly packed with
Both natural and inducible hemaggluti- carbon. By 24 hr, when phagocytosis is virnins have been found in crabs. Can- tually complete, the carbon is aggregated
tacuzene reported the presence of into rounded masses near the nuclei of cells
hemagglutinins in the spider crab (1920) in the vessel walls of the digestive diverticuand the hermit crab, Eupargurus prideauxii la. Three months after injection, the ex(1913). Serum of the coconut crab, Birgo travascular spaces are crowded with dislatio, contains strong hemagglutinins for crete aggregates of carbon. No other norhuman erythrocytes of all blood types. This mal cells appear to take up carbon. Howhemagglutinin seems to be dependent on ever, one animal in the study had an enthe age of the animal; young individuals are cysted parasite in its tail muscle; the large
devoid of the hemagglutinin (Cohen, mononuclear cells which formed the cyst
1968). The blue crab, Callinectes sapidus, actively phagocytosed carbon (Reade
contains a natural hemagglutinin for both 1968).
chicken (CRBC) and rabbit red blood cells
Crayfish, Cambarus virilis, have been
(RRBC). Normal titers range from 16 to 64 studied for immune clearance of 131 Iwith a mean of approximately 40. The re- labeled human serum albumin (HSA) and
IMMUNITY IN DECAPOD CRUSTACEANS
bacteriophage. Following intracardiac injection of 131I-HSA, the radio label
disappears from the circulation at a nearly
constant rate after secondary and tertiary
challenge. There is evidence for the rapid
catabolism and reutilization of the radiolabeled protein. Primary clearance of
</>X174 phage shows no accelerated clearance in the 34 days of observation (Teague
and Friou, 1964).
Further studies with the Australian
crayfish or "yabbie," P. bicarinatus, revealed
the presence of hemagglutinins of limited
specificity which appear to act as opsonins,
enhancing adhesion of heterologous
erythrocytes to hemocytes (McKay et al.,
1969) and phagocytosis (McKay and Jenkin, 1970a).
The "yabbie" may be immunized by injection of either alcohol-killed vaccines or
endotoxin from Pseudomonas CP, a crayfish
pathogen. The response is not entirely
specific, a variety of vaccines from gramnegative bacteria or lipopolysaccharide endotoxins, antigenically unrelated to the
pathogen, increase resistance to the
Pseudomonas infection. The development of
protection proceeds optimally at 26 C
(McKay and Jenkin, 1969). Phagocytes, cultured in vitro, from immunized animals
show greatly enhanced phagocytosis of
sheep erythrocytes only if the erythrocytes
are first treated with hemolymph. There is
no apparent increase in opsonin content in
immunized hemolymph compared with
nonimmunized hemolymph (McKay and
Jenkin, 1970c). There is no apparent production of bactericidins (McKay and Jenkin, 19706). The immunization, therefore,
seems to consist of an increase in the
number of phagocytic cells.
An agglutinin has been found and
characterized in the hemolymph of the
crayfish, Procambarus clarkii. Results indicate that the agglutinin is sensitive to high
and low extremes of/?H, heat denaturation,
and extraction with phenol and 10%
trichloroacetic acid. It is apparently a high
molecular weight, protein containing, macromolecule; the molecular weight is above
150,000, demonstrable by exclusion on
Sephadex (Miller et al., 1972).
A form of encapsulation has been ob-
15
served in vitro in the hemolymph of two
species of crayfish, Pacifastacus lenuisculus
and Astacus astacus. When hyphae of the
crayfish plague fungus, Aphanomyces astaci,
are in contact with a stream of hemolymph,
the hemocytes clump rapidly around the
hyphae. Particles originating from the
hemocyte granules are specifically attached
to and "encapsulate" the hyphae. Melanization could be observed on the hyphal surface within a few hours (Unestam and
Nylund, 1972). Both in vitro and in vivo
melanization is heavier in blood from resistant crayfish (Unestam and Weiss, 1970).
LOBSTERS
A series of natural heteroagglutinins
have been identified and characterized as
one of the minor protein components in the
hemolymph of the California spiny lobster,
Panulirus interruptus. Absorption tests demonstrate ten separate agglutinins which
seem to be class specific (Tyler and Metz,
1945; Tyler and Scheer, 1945).
A natural hemolysin system has been described in the West Indian spiny lobster,
Panulirus argus. The hemolytic system is relatively specific for sheep erythrocytes and
may be completely absorbed by packed
human and sheep erythrocyte stroma. The
reaction is strongly temperature dependent; no hemolysis occurs at 0 C. This implies an enzymatic type of reaction somewhere in the multistep hemolytic system.
The hemolysin is heat labile, nondialyzable
when assayed in the presence of Ca2+ and
Mg 2+ and is inhibited by EDTA
(Weinheimer et al., 1969a). It is not known
if the hemolysin and hemagglutinin systems are related.
American lobsters, Homarus americanus,
clear fluorescein-labeled bovine serum albumin (BSA) at an accelerated rate compared with clearance of fluorescein-labeled
lobster serum proteins. Labeled lobster
protein levels decline rapidly for the first 2
hr and then remain nearly stable for the
next 6 days. The labeled BSA concentration falls rapidly. Almost all labeled BSA is
gone in 72 hr. The clearance rate is related
to the initial concentration of BSA and to
temperature; faster clearance occurs at
16
HARRIETTE C. SCHAPIRO
higher concentrations and temperatures.
Lobster serum in contact with BSA forms
a precipitin ring in 16 hr and a precipitate
after 36 hr. The precipitin titers range
from 2 to 4 and do not increase after exposure of the lobsters to BSA. The precipitin
is nondialyzable and heat labile. There is no
evidence of pinocytosis of the labeled BSA
nor of other foreign proteins. It is
suggested that precipitation may be a prime
mechanism for clearance of foreign proteins (Stewart and Foley, 1969).
An inducible bactericidin has been found
in the West Indian spiny lobster, Panulirus
argus (Evans et al., 1968), the California
spiny lobster, P. interruptus (Evans et al.,
1969a), and the American lobster, H.
americanus (Acton et al., 1969). EMB-1, a
gram-negative bacillus isolated from the
gut of P. argus, is the main organism used
for induction and assay of the bactericidin.
Injections of 109 live or formalin-killed bacteria induce the production of a nondialyzable, heat-labile bactericidin which reaches
maximum titer 24 to 48 hr after the injection. The bactericidin declines slowly, with
activity persisting for as long as 2 weeks in
P. argus. In P. interruptus and H. americanus
the time course of the response and the
titers vary; however, the three species were
all held at different temperatures, and
these differences in temperature probably
caused altered responses. In P. argus secondary and tertiary responses showed
higher maxima than the preceding response. Titers persisted for many days or
weeks without further antigenic stimulation (Evans et al., 19696).
Specificity of the bactericidin is limited.
Animals injected with EMB-1 show bactericidin activity to Salmonellatyphosaand
Escherichia coli (Evans et al., 1968).
Hemolymph of animals injected with
Pneumococcus Type II reacts with EMB-1.
However, heterologous reactions are of
lower titer than homologous reactions. Dilute (0.3%) formalin exhibits a mild adjuvant effect when injected with EMB-1
(Weinheimer et al., 19696).
Natural and induced bactericidins are
produced to several nonpathogenic bacteria isolated from the intestinal tract of//.
americanus. Specificity of the bactericidins is
high with little cross reactivity. The bactericidins are heat labile and more active at
pH's lower than physiological. Elevated
temperatures lead to earlier production of
the bactericidins. Activity is a product of the
interaction of plasma components with
material contained in the hemocytes. Apparently, it is the plasma component that is
enhanced by immunization (Stewart and
Zwicker, 1972).
H. americanus hemolymph inhibits the
growth of a Vibrio sp. (Rabin, 1965),
Pseudomonas perfectomarinus, Achromobacter
thalassius, and Micrococcus sedentarius (Cor-
nick and Stewart, 1968a). In the case of the
latter three bacteria, growth in vitro is inhibited for 24 hr followed by an increase in
viable bacterial counts to nearly the original
numbers within 72 hr. Inhibition of growth
of P. perfectomarinus and A thalassius is re-
moved by heating the hemolymph. These
same studies show that H. americanus
hemolymph is stimulatory for the growth
of Pediococcus homari (formerly Gaffkya
homari), the causative agent of a lethal bacteremia.
TYPES OF IMMUNE MECHANISMS
Several crustaceans challenged with a
wide range of antigens have been reviewed.
Responses have included encapsulation,
phagocytosis with or without the aid of
serum factors, bactericidins active with or
without the aid of hemocyte factors,
hemagglutinins, hemolysins, agglutinins,
and precipitins. Many of these responses
are complex mixtures of cellular and
humoral elements. The humoral portions
of the responses lack the precise specificity
of vertebrate immunoglobulins. The cells
involved in the responses are not well
characterized. Many of the hemocytes of
crustaceans are extremely labile. They rupture or, at the very least, release material
from their cytoplasmic granules when in
contact with foreign substances. This extreme fragility of hemocytes makes it difficult to evaluate the relative contributions
of humoral and cellular elements.
At any rate, it is clear that most decapod
crustaceans are capable of an immune response to many substances including
IMMUNITY IN DECAPOD CRUSTACEANS
17
pathogens. One exception to this seems to initial strain apparently lost virulence.
be the apparent inability of//, americanus to Normally, virulence is maintained by pasrespond to Pediococcus homari.
sage through H. americanus (Cornick and
Stewart, 1968a). When the attenuated
strain began to give anomalous results, it
was compared to a new virulent strain. The
IMMUNITY TO GAFFKEMIA
avirulent strain at high doses could be
The genus Homarus is subject to a lethal cleared within a few days by P. interruptus. A
of P. interruptus were injected with
bacteremia, gaffkemia, caused by Pediococ- group
7
cus homari (formerly Gaffkya homari) 10 avirulent P. homari; 2 days later they
(Snieszko and Taylor, 1947; Editorial Sec- had effectively cleared the injected 5 dose.
retary, 1971). As few as five bacteria per They were then challenged with 10 viruAmerican lobster is sufficient to kill 90% of lent bacteria/ml hemolymph. An unimthe lobsters in 17 days at 15 C. Mean time to munized, control group received the same
death is virtually constant regardless of virulent dose. Control, unimmunized
dose. The bacterium is resistant to aggluti- lobsters died with an MTD of 6 days. The
nation by hemolymph. Its growth is stimu- immunized group lived more than 20 days
lated by hemolymph and although it is with only 3 of 12 animals dead after 28
phagocydzed, the bacteria can overcome days. This is the first reported protection of
this effect and multiply in the hemolymph a crustacean by immunization with a live
(Cornick and Stewart, 1968a). The disease attenuated bacterial pathogen (Schapiro et
has been completely reviewed by Stewart al., 1974). We have tried this attenuated
strain on H. americanus. This strain is still
and Rabin (1970).
virulent
for H. americanus. However, addiThe pathogenicity of P. homari for the
tional
strains
are under investigation. The
crab, Cancer irroratus, has been investigated.
Mean times to death are greatly extended occasional recovery of H. americanus from
over those observed in H. americanus. In- natural infections (Stewart et al., 1966;
terestingly enough, the crab hemolymph Rabin and Hughes, 1968) and the successenhances in vitro growth of the bacteria to ful immunization of P. interruptus make it
the same extent as H. americanus appear that immunization of//, americanus
hemolymph (Cornick and Stewart, 19686). may be feasible.
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IMMUNITY IN DECAPOD CRUSTACEANS
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