AMER. ZOOL., 35:20-27 (1995)
Physiological Adaptations in the Gastrointestinal Tract of Crayfish1
P A U L B. BROWN
Department of Forestry and Natural Resources, Purdue University, 1159 Forestry Building,
West Lafayette, Indiana 47907-1159
SYNOPSIS. Crayfish are the dominant macrocrustacean in many aquatic
ecosystems and are the largest crustacean aquacultural industry in the
United States, yet we know relatively little about their preferred and
nutritionally important foods, as well as their ability to utilize those foods.
This review focuses on the ability of crayfish to detect foods, reduce food
particle size, digest macronutrients and the control of those functions. Of
particular interest are the enzymatic capabilities of crayfish, especially
trypsin, an alkaline protease, cellulase, muramidase, and possibly chitinase and chitobiase. The coordinated neural control of crayfish food location, ingestion and movement has been well documented, while hormonal
control mechanisms have not. The conclusion we must draw from our
current state of knowledge is that crayfish have ample abilities to taste
and locate potential foods and enzymatic adaptations developed in crayfish that allow use of many of the foods they encounter in a benthic aquatic
environment; other adaptations are lacking or have not been elucidated.
INTRODUCTION
Food habits and the physiology of the gastrointestinal tract of crayfish have fascinated scientists for many years. F. H. King
(1883) wrote "Crayfish feed on worms, small
mollusks, insects that fall in their way, small
fish, and in general any kind of animal food,
especially carion." That description of food
habits remains largely intact today, but has
been expanded to include plant material
(Norton, 1942; Gaevskaya, 1969; Capelli,
1980; Brown et ai, 1990; Huner and Barr,
1991; McClain et ai, 1992a), detritus, and
microorganisms associated with plants or
detritus (Anderson and Sedell, 1979; Wiernicki, 1984; Hessen and Skurdal, 1987;
McClain et ai, 19926; Brown et ai, 1992).
Therefore, the potential foods of crayfish
include virtually all possible taxonomic
groups within the plant and animal kingdoms as well as prokaryotes; crayfish could
be characterized as one of the early aquatic
generalists. In this review, I point out several of the pertinent points in morphological
and physiological adaptations in the gastro1
From the Symposium Physiology and Adaptations
in Crayfish presented at the Annual Meeting of the
American Society of Zoologists, 26-30 December 1993,
at Los Angeles, California.
20
intestinal tract of crayfish, but conclude that
the basic structure and function of the gut
is simple. Although physiology of the gastrointestinal tract will be the focus of this
paper, a few words about food identification
and morphological adaptations seems
appropriate.
TASTE
It could be argued that animals who consume a wide variety of food items have
underdeveloped or limited food sensing
capabilities. This is not the case with crayfish; indeed, their ability to chemically detect
acceptable food is one of their specialized
adaptations. Bell (1906) differentiated
between several compounds that, when
placed in water, elicited either a positive or
negative response in crayfish. Since that
time, the receptor sites of crayfish have been
identified (Ameyaw-Akumfi, 1977; Huner
and Barr, 1991) as well as more specific
modes of action of those receptors (Ache
and Sandeman, 1980; Hatt and Franke,
1987). Receptors are located on the antennae, anntennules, second maxilla, and first
through third maxillipeds (Huner and Barr,
1991). Further, crayfish distinguish among
foods in laboratory settings (Covich, 1978;
Tiernay and Atema, 1986; Brown et ai,
GUT PHYSIOLOGY IN CRAYFISH
1986, 1989). Thus far, crayfish seem to
exhibit preferences for feedstuff's of plant
origin (soybean meal, peanut meal, rice bran,
etc.), while fish and shrimp meals have been
poorly consumed. Tissues from intact animals are generally considered palatable
foods; thus, processing of fish and shrimp
into meals may remove the detectable flavor components. Taken together, those
studies clearly indicate that crayfish, like
other animals, have preferences for certain
food items and that sensory attributes are
important in identifying foods.
FOOD ACQUISITION AND
REDUCTION IN PARTICLE SIZE
Crayfish feeding habits vary considerably
between species. However, there is a clear
relationship with stages of the molt cycle
(Nakamura, 1980) and low environmental
pH affects food consumption (Allison et al.,
1992); these factors probably cross species
boundaries. Other environmental factors
may affect food consumption, but have not
been elucidated.
Once a food item has been identified, specialized food gathering appendages facilitate
acquisition. The first through third walking
legs, and associated chelae or claws are wellknown appendages capable of acquiring and
holding food items. Reduction in food particle size begins with these appendages aided
by the mandible, the maxillae and maxillipeds. Perhaps the most interesting morphological adaptation in crayfish is the gastric mill (Parker, 1876), which is a calcified
accessory grinding organ located in the fore
gut, or cardiac sac, that grinds foods once
ingested. Reduction in food particle size,
either prior to or after ingestion, is generally
considered an important aspect of digestion
and absorption of nutrients. Crayfish appear
to have ample capability of reducing food
particle size.
MORPHOLOGY OF THE
GASTROINTESTINAL TRACT
The gastrointestinal tract of crayfish is a
relatively simple, straight tube without significant areas for storage and microbial degradation, although the stomach is divided
into two distinct areas (the fore gut, or cardiac sac, and the posterior stomach or pylo-
21
rus), with a cardio-pyloric valve separating
the two areas (Claiborne and Ayers, 1987).
Additional descriptions can be found in
Komura and Yamamoto (1968), Kawaguti
et al. (1961) and Grahame (1983). Esophageal glands have been an area of relatively
intense interest. Condoulis (1967) provided
strong evidence for the function of these
glands. Not surprisingly, esophageal glands
exhibit salivary, lubrication and fecal binding capabilities in Orconectes immunis.
Those functions are consistent with esophageal glands in vertebrates and probably
consistent among crayfishes. Additional
descriptions of cell types in the gastrointestinal tract can be found in MalaczynskaSuchitz and Klepke (1960) and Miyawaki
and Tsuruda (1984).
The gastrointestinal tract is generally considered to not act as a site of excretion of
nutrients of endogenous origin (Parry, 1960).
This is in direct contrast to vertebrates; further studies in this area may modify this
generalization. Once food has been identified, acquired, and ingested, several physiological factors enhance catabolism and
eventual absorption of nutrients.
ENZYMES AND P H
Enzymatic catabolism of ingested foods
is well known in crayfish and has been summarized on a regular basis (Vonk, 1960;
Kooiman, 1964; O'Connor and Gilbert,
1968; Dall and Moriarty, 1983). Of particular interest has been trypsin and its differences with mammalian trypsin and the lack
of chymotrypsin and pepsin (Kleine, 1967),
although other decapod crustaceans synthesize chymotrypsin (Fang and Lee, 1992; van
Wormhoult et al., 1992).
Trypsin has been carefully studied in a
number of crayfish, but always with an active
form of the enzyme; a zymogen, or inactive
form, has not been identified (Bunt, 1968).
Schoch and DeVillez (1982a) incubated mid
gut tissue from O. virilis and Cambarus sp.
for up to four hours and recorded an increase
in trypsin activity at the 1 and 1.5 hour
samplings. They concluded that either trypsin was being activated from a zymogen form
or deinhibited, possibly released from a
storage site. Based on the previous research,
the deinhibition argument appears to be the
22
PAUL B. BROWN
better of the two. The amino acid composition of trypsin from crayfish is different
from mammalian trypsin in that the number of arginine and lysine residues are lower
in crayfish (Muller and Zwilling, 1975). The
primary catalytic sites of trypsin are the basic
amino acids, lysine and arginine. Thus, the
decreased number of basic amino acid residues reduces the possibility of autocatalysis
and a zymogen form may not be as important in crayfish as in animals with more
basic amino acid residues. The lack of a
zymogen form of trypsin and the differences
in amino acid composition between crayfish
and mammals have been important points
in the discussion of the evolution of the
serine proteases (Muller and Zwilling, 1975;
Zwilling et al., 1975; de Haen and Teller,
1977). The other interesting aspect of trypsin from crayfish is that it is completely
inactivated below pH 4-6 (Dall and Moriarty, 1983).
Given the lack of chymotrypsin and pepsin in crayfish, scientists have explored the
possibility of other proteinases that might
compensate for the lack of the more commonly known digestive enzymes (DeVillez
and Lau, 1970; DeVillez, 1975). A low
molecular weight (LMR) proteinase (Mr
11,000-12,000) was identified in O. virilis
by DeVillez (1965) and characterized as
having an alkaline pH optimum (DeVillez,
1968). A similar proteinase was subsequently identified in Astacus and termed
"niedermolekular" enzyme because of its
small mass (Pfleiderer et al, 1967). Armstrong and DeVillez (1978) found the
enzymes to be similar, but isolated by different methods. Subsequent studies found
the enzyme to be of larger mass (Mr 22,000)
than originally thought (Zwilling et al, 1981;
Titani et al, 1987). The enzyme is interesting in that it has relatively broad specificity for amino acid residues (leucine, phenylalanine and tyrosine) and is completely
inactivated below pH 4.
The occurrence of cellulase in the gastrointestinal tract and hepatopancreas of crayfishes is another distinct difference between
crayfish and other animals (Yokoe, 1960;
Yasumasu and Yokoe, 1965). While bacterial production of cellulase from gut flora
is a common occurrence in many animals,
cellulase in crayfish originates in the hepatopancreas. The pH optimum is 5.8 (Yokoe,
1960). Thus, crayfish have the ability to utilize ingested cellulose as a source of dietary
energy.
Chitinase and chitobiase have been isolated from the gastrointestinal tract of
marine crustaceans (see Dall and Moriarty,
1983); however, these enzymes have not
been studied in crayfish. Wetzel (1993) found
that juvenile O. virilis gained more weight
when fed glucosamine as a carbohydrate
source instead of dextrin. Thus, crayfish have
the ability to utilize the catabolic products
of chitin as a source of dietary energy. Given
this fact and the propensity for consuming
exuvia, lack of chitinase and chitobiase in
crayfish would be surprising. We recently
recorded lysozyme (muramidase, EC
3.2.1.17) activity in the gastrointestinal tract
of O. rusticus, O. virilis and Procambarus
clarkii (unpublished data). Activity was
present in the cardiac sac when crayfish were
fed Daphnia and unidentified bacteria grown
from pond water, but was not present when
crayfish were fed Tubifex. There was no
lysozyme activity in any of the foods evaluated. Lysozyme is one of the few enzymes
capable of catabolizing bacterial cell walls
and can occur with or without chitinase
activity. This indicates that crayfish have
the ability to digest bacteria and use those
as sources of nutrients. We have not examined chitinase activity in conjunction with
muramidase activity.
Acidity of the fore gut of crayfishes is
thought to be in the range of 5-7 as in other
crustaceans (van Weel, 1970). This range is
in agreement with values for O. rusticus
shown in Figure 1 (unpublished data from
my laboratory). Those values do not
decrease below 5 after a meal of Daphnia
magna. Therefore, the acidity of the fore
gut of crayfishes does not appear to exceed
the pH values that would inactivate digestive enzymes. Additional pH measurements
of the mid- and hind gut of crayfishes found
values in the range of 6-7 after a meal
(unpublished data). These data indicate that
acidity of the stomach of crayfish plays a
less important role in digestion than in some
23
GUT PHYSIOLOGY IN CRAYFISH
other animals. For example, stomach pH of
tilapia (a tropical, fresh water fish) is in the
range of 2-3 (Bowen, 1983).
HEPATOPANCREAS
The hepatopancreas, or midgut gland, is
one of the important sites of synthesis and
secretion of digestive enzymes (Bradley,
1908; DeVillez and Fyler, 1986) and other
proteins (Durliat and Vranckx, 1982), and
is the target tissue of several hormones
affecting digestion and absorption of nutrients (Yamamoto, 1953, 1960; Wang and
Sheer, 1963; Zerbe et al, 1970; van Herp,
1970; Keller and Andrew, 1973; Miyawaki
and Tsuruda, 1985; Sedlmeier, 1987). The
use of the term hepatopancreas was questioned by van Weel (1970) and Phillips et
al. (1977). Regardless of the term used to
describe this organ, it has several functions
similar to mammalian and avian hepatic
tissue (Denuce, 1967; Hartenstein, 1971;
Watabe et al, 1985; Almar et al., 1987).
Both absorptive and secretory cells have
been identified and lipid storage occurs in
that organ (Bunt, 1968; van Herp, 1970).
Dall and Moriarty (1983) provided an
excellent description of the cell types found
in the hepatopancreas. Additionally, heavy
metal storage has been documented, and
accumulation of minerals impairs metabolism (Fingerman et al., 1965; Bunt, 1968;
Roldan and Shivers, 1987). Thus, the hepatopancreas appears to be more similar to
vertebrate liver than not.
NEURAL AND HORMONAL CONTROL
Neurological studies with crayfish are well
known and an intense area of investigation.
This review will not focus a proportionate
amount of space to that control, but will
alert the reader to the published literature.
Spirito (1975), Wales (1982), Claiborne
and Ayers (1987), and Govind and Lingle
(1987) summarized the published literature
on neural control of the mouthparts and
gastrointestinal tract of crayfish. Both proprioceptors, mechanoreceptors, and presumptive chemoreceptors have been identified. The presence of chemoreceptors in
the cardiac sac may explain the finding from
my laboratory in which lysozyme activity
4.8
30
60
90
120
TIME (Minutes)
150
180
FIG. 1. Change in mean stomach pH in Orconectes
rusticus after a meal otDaphnia magna.
was present in the fore gut when crayfish
were fed certain foods, but not others. The
gastric mill has two subsystems of neural
control, one for the lateral and one for the
medial aspects, which function independently, but in a coordinated manner. The
cardio-pyloric valve is under neural control
and acts to meter food particles into posterior portions of the stomach. Rhythmic
movements of the musculature result in
peristaltic waves and movement of ingesta,
which are also under neural control. Thus,
there is a coordinated movement of ingesta
once consumed. Stepushkina et al. (1977)
hypothesized that this coordination begins
with location of food. While there has been
considerable research in neural control of
the gastrointestinal tract, there have been
very few studies of hormonal control (Fingerman, 1987).
Catecholamines have been difficult to
locate in crustaceans, but Elofsson et al.
(1968) indicated their presence in the hind
gut ofAstacus astacus, associated with nerve
fibers. This could be an indication of the
typical stress response in vertebrates that is
known to affect movement of ingesta in the
gastrointestinal tract. Denuce (1982) injected
porcine cholecystokinin-pancreozymin into
O. virilis and observed a selective response
on amylase and two unidentified proteases.
Schoch and DeVillez (1982ft) reported a significant increase in trypsin activity in O.
rusticus when injected with caerulein (ceruletide). Crustacean hyperglycemic hormone (CHH) most likely has an effect on
24
PAUL B. BROWN
glucose transport from the gastrointestinal
tract. Shibata et al. (1986, 1987) observed
a 15 fold increase in cyclic GMP levels in
intestinal cells of crayfish injected with
CHH, implicating the intestine as a target
tissue of CHH and its effect mediated by
cGMP. Hormonal control of the gastrointestinal tract and associated organs is poorly
understood and may deserve further
research efforts.
ABSORPTION OF NUTRIENTS
The function of the gastrointestinal tract
is catabolism of ingested food and absorption of nutrients. The factors discussed
above aid in the catabolism of macromolecules to subunits that can be absorbed;
however, there are apparently no reports of
nutrient transport mechanisms from the
gastrointestinal tract of crayfish. There are
estimates, though, of the percentages of
radioactively labeled nutrients remaining
intact through the intestinal cells to the
hemolymph. Those estimates ranged from
a low of 20% for glucose to a high of 3040% for amino acids and palmitate (Speck
and Urich, 1972). Thus, the absorbing cells
within the gastrointestinal tract utilize a significant proportion of nutrients in crayfish
as they do in vertebrates.
Gross measures of nutrient absorption
have been developed in the past few years
and those values indicated crayfish absorb
relatively high percentages of ingested macronutrients (Wiernicki, 1984; Brown et al,
1986; Ellis et al., 1987; Brown et al, 1989).
COORDINATION BETWEEN GUT AND GILL
Freshwater animals require regular mineral intake for normal physiological and
biochemical processes. These inputs can be
provided by either the gastrointestinal tract
or across the gill. There have been a number
of studies with freshwater fish indicating this
is the case. However, there have been relatively few studies of this nature with crayfish.
Toxicity of elements in the environment
of crayfish has received a significant amount
of research effort. If elements dissolved in
solution are toxic to crayfish, then there must
be a site of entry into the animal, probably
the gill. Zinc, copper, potassium, magne-
sium and sodium have all been identified
as causing mortality in crayfish when
exposed to selected concentrations in the
environment (Helf, 1931; Hubschman,
1967a, b; Bryan, 1967; Ehrenfeld, 1974).
Those studies were conducted with external
concentrations well above those likely
encountered in most natural situations.
However, those elements are considered
essential minerals in all animals. At sublethal concentrations of these elements in the
water, there may be an interaction of environmental and dietary absorption mechanisms, which has not been explored in crayfish.
CONCLUSIONS AND FUTURE PROSPECTS
Crayfish encounter a wide variety of
potential food items in the benthic environment and several morphological and
physiological adaptations have evolved that
allow use of those foods. The gastric mill is
a specialized food grinding organ that facilitates reduction in food particle size. Crayfish synthesize several enzymes not found
in most other animals that allow use of those
potential nutrients. The pH of the stomach
is relatively alkaline. The gastrointestinal
tract is a simple, straight tube and is not
unique. Thus, the physiological adaptations
in crayfish are largely the enzymatic capabilities; other adaptations await elucidation.
Crayfish are the dominant macrocrustacean in many aquatic ecosystems and are
the largest crustacean aquacultural industry
in the United States; however, relatively little progress has been made in our understanding of certain key aspects of their biology. This review focuses on our knowledge
of gut physiology. It is clear there are large
gaps in our knowledge of important aspects
such as preferred foods, digestion and
absorption of nutrients, control of feed
intake, and metabolic fate of absorbed
nutrients. If aquatic biologists are to fully
understand the flow of nutrients through
aquatic food chains, then a better understanding of crayfish and their role seems
important. Also, aquaculturists have been
operating with relatively little quantitative
information on important foods. Thus, there
are several relatively applied reasons for
studying crayfish nutrition and gut physi-
GUT PHYSIOLOGY IN CRAYFISH
ology. The important discussions of serine
protease evolution point to a more basic
interest in invertebrates and their role in the
evolution of vertebrates. Aquatic biologists,
aquaculturists and evolutionary scientists
could all benefit from further research efforts
with this important crustacean. Perhaps, as
the co-organizer of this symposium pointed
out, the "marriage of science and industry
(could) be beneficial to (all three) camps"
(Fingerman, 1987).
25
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