ILL .

AT .URBAN - HAMPAI
BIOLOGY

JUL 1 9 198?

•* ELDIANA
zoology

Published by Field Museum of Natural History

New Series, No. 2 December 18, 1979

The Functional Morphology of the
* . Grooming Appendages of
a Palaemonetes kadiakensis Rathbun, 1902

& .A, Bruce E. Felgenhauer

Department of Biology
Florida State University, Tallahassee

Frederick R. Schram

Department of Paleontology
San Diego Natural History Museum

Competition for attachment surfaces is a constant process in the
aquatic environment. Sessile protozoans and various other in-
vertebrates attach to almost any available substrate as epibionts,
and the crustacean exoskeleton is such a substrate.

Aquatic Crustacea are often fouled by epibionts and debris. This
fouling may cause difficulties in locomotion or inhibit sensory recep-
tion depending upon the location and intensity of infestation
(Bauer, 1975). Heavy infestations of epibionts at specific locations
i.e., pleopods, branchiostegites, gill lamellae, and antennae, could
impede normal fluid flow around the animal.

Suspended materials in the water column may clog openings and
cover surfaces through which contact between the organisms and
the external environment must take place, i.e., gill lamellae, chemo-
receptive setation, and antennae (Bauer, 1975). Such epibiont infes-
tation has elicited the development of elaborate cleaning systems.

There are very few reports on crustacean grooming in the
literature. Doflein (1910) described gill and exoskeleton grooming
by the first cheliped of Palaemon xiphias. Needier (1931) observed
Pandalus danae clean its pleopods before laying eggs. Hoglund
(1943) reported cleaning behavior which preceded spawning in

Library of Congress Catalog Card No.: 79-51548
ISSN 0015-0754

Publication 1303

101 BURRILLHAU.

BIOLOGY LIBRARY j J\J\_ ° '"

2 FIELDIANA: ZOOLOGY

Palaemon squilla. Bauer (1975) reviewed some earlier work and
described in detail the relevant morphology of the preening appen-
dages and grooming behavior of Pandalus danae.

This study parallel's Bauer's work, but investigates the morphol-
ogy and grooming activities of a freshwater prawn, Palaemonetes
kadiakensis Rathbun, 1902, and constitutes the first observations
of grooming in freshwater prawns. Comparisons between the mor-
phology and activities of marine prawns and freshwater prawns is
described below.

MATERIALS AND METHODS

Palaemonetes kadiakensis occurs mainly in waters of the central
United States west of the Alleghenies (Holthius, 1949). The prawn
is transparent and ranges up to 54 mm. in total body length.

Collections were made by dip netting in the shallows of Lake
Charleston, Coles County, Illinois. Prawns were placed in aquaria
with a sample of natural substrate and plants. Observations of
grooming behavior were recorded at time intervals around the clock.
Setal structure of the pereiopods were analyzed by light and scan-
ning electron microscopy. For SEM examination, whole prawns
were fixed in 4 per cent glutaraldehyde in .1 molar phosphate buffer.
Then, after a rinsing of the appendages, the specimens were fixed an
additional 4 hr. in 4 per cent glutaraldehyde alone and afterward
rinsed in a .1 molar phosphate buffer. Appendages were dried in a
C02 critical point dryer, sputter coated with carbon, and then sput-
ter coated with 10-15 nm of gold paladium. Observations were made
on a JEOL-JSM-35 SEM at 5 kilovolts. Drawings in Figure 1 were
made with a Wild Camera Lucida and drawings in Figure 2 were
generally made from photographs.

APPENDAGES

The functions of each appendage in grooming were observed and
recorded. The first, second, and fifth pereiopods (fig. lb,c,f), along
with the third maxillipeds (fig. la), are responsible for keeping the
body and sensory areas free from fouling materials. The third and
fourth pereiopods (fig. ld,e) are devoid of any functional grooming
setation, but support the prawn during grooming.

The first, second, and fifth pereiopods were observed to clean
specific locations on the exoskeleton, and are armed with specialized

Fig. 1. A, Third maxilliped; B, First pereiopod; C, Second pereiopod; D, Third
pereiopod; E, Fourth pereiopod; F, Fifth pereiopod; G, Serrate seta; H, Cross-section
of serrate seta showing angle orientation of subsetules to shaft; I, Simple seta; J,
Plumose seta; K, multi-denticulate seta; L, Close-up of multi-denticulate seta show-
ing brush-like nature of subsetules; M, Squat-hair seta.

3

Fig. 2. A, Double-hatched area defines the field of operation of first and second
pereiopod, single-hatched area indicates the field of operation of second pereiopod
only; B, Hatched area field of operation of fifth pereiopod; C, Grooming of second
antenna in carpus-propodus joint of first pereiopod; D, Grooming of second antenna
by the third maxillipeds, arrows indicate direction in which flagellum is pulled; E,
Tongue and groove locking mechanism of second pereiopod of Pandalus danae; F,
Locking mechanism of second pereiopod of Palaemonetes kadiakensis; G, Auto-
grooming of third maxillipeds, arrows indicating movement of appendages; H,
Diagrammatic view of sequential stages in auto-grooming of third maxillipeds; I,
Grooming of pleopods, arrow indicating motion of fifth pereiopod; J, Grooming of
abdomen and telson, large arrows indicate movement of fifth pereiopod, small
arrows indicate movement of first and second pereiopod chelae.

FELGENHAUER & SCHRAM: GROOMING IN PRAWNS S

setae for this purpose (fig. 2a,b). The pereiopods also groom indepen-
dently of each other and frequently reached across to preen opposite
sides of the individual.

Several distinct types of setae are found on the grooming appen-
dages (fig. lg-m): serrate, simple, plumose, multi-denticulate, and
squat-hairs.

Third Maxillipeds

The third maxilliped, composed of four segments, are larger than
the other maxillipeds and have dense patches of serrate setae
medially on the fused propodus and dactylus (pi. I, fig. 1). The
setules lining the setal shaft occur at 45° angles to each other (fig.
lh), and are restricted to the distal two-thirds of the setal shaft.

The third maxillipeds groom the first and second pereiopods and
the antennae. The chelae of the first and second pereiopods are
groomed as a result of numerous passes through the third maxilli-
peds which are held horizontal to the substrate. After these pereio-
pods are groomed, the third maxillipeds remove debris and epizoites
by the mutual rubbing of each other (fig. 2g). The maxillipeds rub
vertically against each other's setae causing the lodged debris to
drop to the substrate (fig. 2h), an activity also noted by Bauer (1975)
in Pandalus.

The first antennae are also groomed by the third maxillipeds in
the following manner: the first antennae are lowered toward the
third maxillipeds; the maxillipeds raise themselves slightly, and
clasp the base of the antennae; the first antennae are then drawn
through the setation of the third maxillipeds as the antennae
resume the normal horizontal resting position. This grooming oc-
curs frequently and is usually coupled with cleaning of the second
antennae, which will be discussed below.

First pereiopods

The first pereiopods of Palaemonetes kadiakensis have locomo-
tory, feeding, and grooming functions. As in most caridean prawns,
the first pereiopod is chelate and is composed of seven segments.
The chelae are used to delicately probe the substrate for food and
tear bits of material apart with the aid of the third maxillipeds.

The propodus and dactylus of the chelae are armed with three
types of setae: serrate, multi-denticulate, and squat-hairs (pi. I, fig.
3), serving various grooming functions.

The dactylus and distal half of the propodus are armed with long
multi-denticulate setae (pi. I, fig. 4), composed of toothed setules

FIELDIANA: ZOOLOGY

lmm

.1mm

Plate I. 1, Third maxilliped; 2, Close-up of serrate setae on third maxilliped; 3,
Chela of first pereiopod; 4, Close-up of subsetules of multi-denticulate seta on first
pereiopod.

along each setal shaft. Each setule has individual subsetules which
give it a comb-like appearance (pi. II, fig. 1). The inner medial sur-
faces of the propodus and dactylus are armed with short, evenly
spaced setae. These setae are termed squat-hairs. The squat-hairs
located medially on the inner surface of the propodus and dactylus
are apparent under light and SEM photography (pi. II, fig. 2), and
are thought to be advantageous in gripping, scraping, and abrading
(Bauer, 1975). Shelton & Laverack (1970) suggested that this type
of setation may also be chemoreceptive.

•1mm

Plate II. 1, Close-up of subsetules of multi-denticulate seta; 2, Terminus of first
pereiopod with arrows indicating a row of squat-hair setae; 3, Carpus-propodus joint
of first pereiopod, with arrow indicating position of antennular flagella in grooming.

8 FIELDIANA: ZOOLOGY

The third setal type seen on the first pereiopods is serrate, found
densely packed in the joint between the carpus and propodus (pi. II,
fig. 3). This serrate setal type has rows of teeth laterally along the
shaft and serrations that are not opposite on the shaft, but usually
within 45-120° of each other (fig. lg,h). The serrate setae have also
been suggested to be chemoreceptive (Farmer, 1974). The proximal
portion of the propodus is lined with rows of stiff, short, serrate
setae which are individually set into sockets. The brush-like nature
of this setation is presented by SEM stereo pairs (pi. Ill, fig. la,b).
These serrate setae on the carpus are longer and denser than the
more uniformly spaced serrate setae on the propodus (pi. Ill, fig. 3).
Serrate setae are brush-like in appearance and their dense nature
forms a network of combs which provide a surface area for grooming
the antennae when the joint is flexed.

The first pereiopods groom primarily cephalic structures (fig. 2a),
and also parts of the telson. The chelae pick and preen at the
crevices of the exoskeleton, vigorously pulling and digging at the
arthrodial membranes. The chelae open and close rapidly while pass-
ing across the carapace and rostrum during grooming periods. The
squat-hairs, located medially on the inner surface of the propodus
and dactylus, may act as scraping devices during the rapid move-
ment of the chelae over the exoskeleton. These serrate setal bundles
on the distal end of both the propodus and dactylus are used as
brushes to clean the gill lamellae and the lining of the branchial
chamber.

The telson is simultaneously groomed by the first and second
pereiopods. The prawn is supported by the third and fourth pereio-
pods as the telson is then brought anteriad and ventrad under the
carapace. The first and second pereiopods pick at the uropods and
the chelae rapidly open and close while passing across the surface of
the telson (fig. 2j). The pereiopods of Palaemonetes kadiakensis are
quite flexible at the joints, enhancing their grooming efficiency.

The second antenna of the prawn is groomed with greater frequen-
cy than any other part of the prawn. The second antenna is brought
anterior as the carpus-propodus joint of the first pereiopod hooks
onto the base of the second antennular flagellum (fig. 2c). Each
antenna is then pulled ventrad by the first pereiopod toward the
third maxillipeds. In the process of lowering the antennular flagel-
lum the carpal-propodal joint slides down the length of the antenna.
The third maxillipeds then clasp the base of the flagellum, where-

FELGENHAUER & SCHRAM: GROOMING IN PRAWNS

1mm

1mm

Plate III. la, b, Stereo SEM of serrate setae on proximal third of propodus of
first pereiopod; 2, Second pereiopod; 3, Close-up of serrate setae in carpus-propodus
joint of first pereiopod.

upon the antenna is pulled through stiff grooming brushes of the
third maxillipeds as it resumes its normal horizontal position (fig.
2d). Following this antennular grooming, the third maxillipeds also
autogroom. The antennular flagella are actually double-groomed by
this elaborate process. The carpus-propodus joint of the first pereio-

10 FIELDIANA: ZOOLOGY

pod is heavily armed with dense serrate setae, which, when flexed
around the antennae, form a network of brushes that encloses the
entire flagellum as it moves through the joint (pi. II, fig. 3).

The first pereiopod setal groups are cleaned by rubbing the distal
portion of the leg through the stiff serrate setae of the third maxilli-
peds. Following this action, the chelae are often autogroomed by
brushing against each other for short periods, thus removing any
additional debris from the serrate setae.

Second pereiopods

The second pereiopods behave in a manner similar to the first
pereiopods. The chelae of the second pereiopods are more slender
and pointed than those of the first pereiopods (pi. Ill, fig. 2). The
distal portion of the chela is armed with multi-denticulate setae set
into deep sockets with many setae per socket (pi. IV, fig. la,b).
There is sparse multi-denticulate setation of the distal end of the
propodus and dactylus (pi. Ill, fig. 3). There are no setal groups on
the carpus of the second pereiopod, as is seen on that of the first
pereiopod, but as in the first pereiopod the second also has squat-
hairs lining the medial surface of the propodus and dactylus.

The second pereiopod has a locking mechanism on the tip of the
chela. The propodus and dactylus have large terminal tooth-bearing
movable setae that fit together tightly when the chela is closed (pi.
IV, fig. 3). Bauer (1975) observed that the second pereiopod of Pan-
dalus danae had a tongue and groove locking mechanism (fig. 2e).
Palaemonetes kadiakensis has a locking mechanism on both the
first and second pereiopods which lock much like the clasps on a
purse, (fig. 2f).

The second pereiopods supplement the first pereiopods in groom-
ing the cephalic regions and have virtually the same field of activity.
The second pereiopods, however, do not groom the antennae nor
much of the rostral area, and they reach farther posterior on the
carapace (fig. 2a). The second pereiopods preen the edges of the
branchiostegites and the peduncle of the eyestalks more than the
first pereiopods do. Since the chelae of this second pereiopod are
armed with setae of the multi-denticulate type, they also may have
important chemoreceptive functions.

Third and fourth pereiopods

The third and fourth pereiopods are the principal walking appen-
dages of the prawn and are long and pointed at the tip (fig. ld,e).

.1 mm

■imm

j.1 mm ,

Plate IV. la, b, Stereo SEM of lateral view of second pereiopod; 2, Carpus-
propodus joint of fifth pereiopod; 3, Oblique view of second pereiopod chela showing
interlocking terminal setae.

11

12 FIELDIANA: ZOOLOGY

The setal structures of these pereiopods indicate that these appen-
dages are not morphologically designed for grooming, as they are
devoid of complex setation. Most of the setae are simple, with soli-
tary shafts lacking the subsetules or serrations of the grooming
pereiopods (fig. lb,c,f).

The main functions of these two pereiopods during grooming
periods are support and balance. Removal of the first, second, and
fifth pereiopods does not impair locomotion and maneuverability.

Fifth pereiopods

The fifth pereiopods are the longest and most flexible of all the
walking legs and groom the abdomen and tail fan of the animal. Ser-
rate setae extend ventrally between the carpal-propodal joint (pi.
IV, fig. 2).

The fifth pereiopods groom the dorsum of the abdomen. This is
accomplished as the prawn shifts its weight forward on the third
and fourth pereiopods as the telson is flexed forward, forming an
inverted "U." The fifth pereiopod then runs its serrate setae dorsal-
ly down the entire length of the abdomen, beginning with the
posterior edge of the carapace and ending at the tip of the telson
(fig. 2j). The serrate setae on the fifth pereiopod are extremely dense
and groom the entire dorsum of the abdomen (pi. V, fig. 1).

The prawn remains in this flexed position for extended periods of
time as the fifth pereiopod repeatedly sweeps the abdominal region.
This behavior is frequently coupled with the preening of the telson
by the first and second pereiopods (fig. 2j).

The fifth pereiopods are important in the grooming of the abdo-
men in both prawns. Heavy bundles of serrate setae are seen in the
carpal-propodal joint of both species. The behavioral patterns of
cleaning the abdomen are somewhat different. Palaemonetes kadia-
kensis brings its abdomen beneath the carapace as the fifth pereio-
pods stroke the dorsum of the abdomen. Bauer also reported this
behavior in Pandalus, but noted this species more typically
groomed a straightened abdomen with brushing and scratching
movements of the fifth pereiopods.

Grooming is an integral part of the activities of Palaemonetes
kadiakensis. It is evident in this study that elaborate morphological
and behavioral adaptations have been developed for the removal of
fouling organisms and debris, and that a large proportion of time
and energy is expended in the process of cleaning. The Infraorder
Caridea has successfully radiated into marine, brackish, and fresh-

Plate V. 1, Brush-like serrate setae on fifth pereiopod; 2, Appendix interna on
pleopods; 3, Close-up of terminus of appendix interna showing the mushroom setae
for interlocking with opposing appendix interna; 4, Light micrograph of plumose
setae on pleopod, arrows indicating bent or broken setae.

13

14 FIELDIANA: ZOOLOGY

water habitats. One factor that may have contributed to this suc-
cess is the development of efficient grooming patterns.

Monitoring the external environment is vital to the success of any
animal. The caridoid escape reaction of Palaemonetes kadiakensis is
its primary defense mechanism against predators and it is probably
largely triggered by sight, vibrations, or chemoreception. If sensory
sites are fouled, information from the environment could be lost.
Olfaction in Palaemonetes kadiakensis is accomplished at sites of
aesthetascs (extensions of the exoskeleton). They are found on the
base of the first antennae in Palaemonetes kadiakensis. The fre-
quent and repeated groomings of the antennae keeps the aesthe-
tascs free of fouling organisms and debris, allowing olfaction to be
constant and accurate. Without regular grooming, vital information
from the environment could be lost due to the inhibition of water
currents through the rows of aesthetascs (Bauer, 1975). Chemo-
reception of the antennae, pereiopods, and maxillipeds aid in the
securing of food, consequently fouling of such sites could hinder the
receptivity and hence the locating of food sources (Barber, 1960;
Shelton & Laverack, 1970). The third maxillipeds are heavily armed
with serrate setae and are constantly accepting and rejecting possi-
ble food. The serrate setae of the first and second pereiopods also
select and reject materials from the substrate. Clogging of these
chemoreceptive setae may limit the prawn's ability to locate food.
The eyestalks of Palaemonetes kadiakensis are constantly twitch-
ing and are groomed by the first and second pereiopods to
discourage fouling.

In the genus Palaemonetes, males respond only to females which
have recently molted to breeding condition. The recognition of at-
tractiveness by the male occurs with contact of his antennae with
any surface of the female; thus sex recognition would appear to be
determined by a non-diffusible coating of the integument of the
female (Burkenroad, 1947). The mating stimulus initiating the
palaemonid mating behavior suggests that recognition of a recep-
tive female by the male has an important visual component (Nouvel
& Nouvel, 1937; Hoglund, 1943). Regardless of which interpretation
of palaemonid sex recognition is correct, be it visual or chemical, if
sensory sites are fouled, mating would be hindered.

The caridean respiratory and feeding current is an anteriad
stream of water drawn under the posterior and lateral edges of the
carapace and discharged anteriorly on either side of the mouth. This
important flow would be interrupted by debris and epibionts which

FELGENHAUER & SCHRAM: GROOMING IN PRAWNS 15

aggregate along the edges of the branchiostegites if they were not
removed in some manner.

Setation plays an important role in locomotion in Palaemonetes
kadiakensis. Swimming is accomplished in this prawn by the appen-
dix interna locking the pairs of pleopods. The tips of these struc-
tures, which are found on all but the first pleopods, hold the
elements together while the prawn is swimming (pi. V, fig. 2). The
appendix interna is armed with mushroom-shaped setae which serve
to hook the pleopods together (pi. V, fig. 3). The plumed setae, which
have smooth shafts inserted into sockets and have numerous
setules, are located on the pleopod margins (fig. lj). These setae ex-
tend the surface area of the pleopod and form "paddles" which pro-
pel the prawn through the water. If these setae were not groomed
regularly, they would soon become fouled and eventually break,
causing the resistance between the water and the pleopods to be
weakened, thus hindering locomotion (pi. V, fig. 4).

Molting is one of the most important aspects of crustacean physi-
ology. The normal physiology of prawns is continuously concerned
with the successive stages of the molt cycle. Between molts, Palae-
monetes kadiakensis keeps its integument free of fouling organisms
and debris by grooming. Whereas ecdysis frees the crustacean body
of its old cuticle and any fouling debris, it can be interrupted period-
ically by hibernation, ovarian maturation, and carrying of develop-
ing eggs (Passano, 1960). It is during these intermittent periods
that grooming is extremely important.

Temperature influences molting (Passano, 1960). Crustaceans
exhibit increased molting activity during periods of higher tempera-
tures and significantly reduced activity (anecdysis) during times of
low temperatures (Hiatt, 1948; Balesdent-Marquet, 1955). Palae-
monetes kadiakensis is subjected to low temperatures for two to
five months of the year. During this time, molting seems to cease
and grooming is needed to remove fouling organisms and debris
until the molt cycle resumes in warmer weather.

An effective grooming mechanism in these crustaceans is essen-
tial. Such elaborate grooming mechanisms have undoubtedly
played a role in the relative success of the carideans as natant
decapods.

ACKNOWLEDGEMENTS
The authors wish to thank Miss Nancy Graham who contributed

16 FIELDIANA: ZOOLOGY

greatly to the art work of this paper and Mr. Ted Odom for his help
in making the SEM photographs. Special thanks must be expressed
to Dr. R. MacLeod, Director of the Center for Electron Microscopy,
University of Illinois, Champaign, Illinois. Drs. R. T. Bauer and
J. W. Hedgepeth reviewed and commented on the manuscript, but,
of course, defects of presentation remain our own.

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FELGENHAUER & SCHRAM: GROOMING IN PRAWNS 17

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