2.
Predators of the High Intertidal Harpacticoid Copepod
Tigriopus californicus
Tigriopus californicus, a harpacticoid oopepod, occurs in great numbers
in high rocky tide pools along the Pacific coast from Vancouver Island, British
Columbia, to Baja California (Vittor, 1971). Predation on Tigriopus has not
been previously studied, and as of this date no important predators are known
(Vittor, 1971). The present paper presents an investigation of some possible
predators of Tigriopus.
A preliminary survey of tide pools in the vicinity of the Hopkins Marine
Station of Stanford University at Pacific Grove, California and Natural Bridges
State Park, Santa Cruz, California, beginning in the highest pools and working
down to the lower pools, revealed the following list of possible predators: the
waterboatman Trichocorixia sp. (Insecta, Hemiptera), the crab Pachygrapsus
crassipes, the hermit crab Pagurus samuelis, the barnacle Balanus glandula,
Gammarid amphipods, isopods, the bivalve Mytilus californianus, the sea
anemone Anthopleura elegatissima, the cottid fish Clinocottus analis, and
the shrimp Heptacarpus paludicola.
Materials and Methods
Possible predators and Tigriopus were collected in April and May, 1977,
at Mussel Point, Point Pinos, and Asilomar State Beach, Pacific Grove, Califor-
nia, and maintained in either running sea water or in pans of standing sea water at
temperatures f approximately 15 to 22 90 until they were used in experiments.
Each potential predator species was tested to determine if it fed on
adult Tigriopus or its larvae. The basic experimental procedure for testing
predation on adult Tigriopus involved counting out 75 Tigriopus and placing
them in filtered sea water in a four inch fingerbowl. No gravid females were
used, so no hatching of larvae could occur. One to four
specimens of
the possible predator species being tested, starved for one to two days, were
added to each bowl. Observations were then made on the feeding methods of the
predators. At the end of 24 hours the predators were removed, the number of
living and dead Tigriopus remaining were counted, and the predator's gut contents
and fecal pellets were examined. The control for each set of experiments was a
fingerbowl with 75 Tigriopus in filtered sea water.
Tigriopus larvae were obtained by removing the egg sacs from gravid
females and allowing them to hatch in filtered sea water. Larvae were then
added to fingerbowls containing possible predators and observations were made
to determine the methods, if any, used to capture Tigriopus larvae. After 21
hours the gut contents and fecal pellets of the predators under study were
examined for Tigriopus fragments.
Results and Discussion
The control populations for the earlier experiments occassionally showed
an increase in number. This is due to the separation of copulating pairs which
in these earlier tests were counted as one individual, or possibly due to
inaccurate counting. The predators are considered below in the order of their
distribution in the intertidal zone, starting with those found in the highest
pools.
Trichocorixia
The waterboatman Trichocorixia was found in the flocculant detrital
material of the very high tide pools. In natural situations Trichocorixia
can cling to the bottom. To simulatethis natural condition I placed sterile
sand or cotton in the bottom of the fingerbowl; these materials could be
grasped by the corixids with the tarsal claws of their second legs (Pennak, 1953).
In all of the runs there was a small decline in the number of Tigriopus at the
end of the experiment (Table I). While under observation the corixids did not
feed. Before feeding, the guts of the corixids did not appear red, while
after feeding the guts of some did appear red. An examination of the reddish
gut contents did not reveal any recognizable Tigriopus parts, However, the
reddish-orange oil droplets in the corixids did look similiar to those in
Tigriopus. It is possible that the corixids only suck the internal contents
out of Tigriopus with their stylets. However, no empty Tigriopus exoskeletons
were found at the ends of experiments.
At Hopkins Marine Station Tigriopus are maintained in an outdoor con-
crete pool about h.5 meters in diameter. They are fed "TetraMin" fish food.
In the flocculant material on the bottom of this Tigriopus pool some red
decomposing pieces of the "TetraMin" fish food were found. The corixids used
in most of the feeding experiments were captured in this pool. The gut contents
of many freshly captured specimens was red. Corixids starved for several days
were fed fresh red "TetraMin", or red "TetraMin" which had been allowed to sit
in filtered sea water for two days, to determine if the fish food was responsible
for their red gut coloration instead of Tigriopus. The results of these experi¬
ments (Table II) indicate that the fresh "TetraMin" is not responsible for the
red gut coloration; only one of five corixids tested with the decomposing
"TetraMin" had gut contents similiar to those of corixids just taken from the
concrete pool. The reddish-orange oil droplets were also present in the freshly
collected corixids' guts.
Usinger (1956) reports that corixids do not subsist on the flocculant
bottom deposits but eat animal food such as larvae; the corixids sweep larvae
into their mouths with their first tarsi (Pennak, 1953). Trichocorixia were
not observed eating any larvae, but their gut contents were occassionally red
after feeding. No larval fragments were found in the corixids' guts.
The results of these experiments do not clearly indicate that
Trichocorixia either is or is not a predator of Tigriopus.
5
Pachygrapsus crassipes
This crab is a common inhabitant of high tide pools and one of Tigriopus's
main predators. The crab ate from 2.6 to 36% of the adult Tigriopus presented
to it in feeding experiments (Table III). Fragments of adult copepod exoske¬
letons were found in the crab's feces several hours after the feeding experi¬
ment. Pachygrapsus uses its chelae to pick up Tigriopus and bring them to its
mouth. It also uses its chelae to scoop dead Tigriopus into its mouth. In its
natural environment Pachygrapsus is an omnivore (MacGinitie and MacGinitie,
1968). Its main food source is matted and encrusting algae which it scrapes
from rocks with its chelae; detrital material left by the receding tides, and
living intertidal organisms are its secondary food sources (Hiatt, 1948).
Pachygrapsus is able to ingest some Tigriopus larvae. Fragments of
larval exoskeletons were found in the feces. However, the larger the crab gets,
the more difficult it is for the crab to pick up the larvae. The reverse
respiratory current created by the bailers on the second maxillae and used to
clean the gills may carry the larvae directly to the mouth, allowing the crab
to feed without the use of its chelae.
After a feeding experiment the crabs involved were placed in 702
alcohol and their bodies and the alcohol searched for adult Tigriopus. Of
those copepods found, some appeared to have been inside the gill chamber,
current.
possibly sucked in with the respiratory/ Others were apparently clinging to
the hairs on the legs of the crabs. Pachygrapsus often visits high tide pools
and is responsible for transportingat least a few Tigriopus from one pool to
another.
Pagurus samuelis
This hermit crab is a scavenger of the high tide pools (MacGinitie and
MacGinitie, 1968) and is another predator of Tigriopus. (Table IV). Adult
Tigriopus exoskeletons and fragments were found in the feces after the feeding
experiments. Pagurus was seen to pick Tigriopus off the bottom and the sides
of the fingerbowls with its left cheliped and then bring them to its mouth.
Here they are passed to the maxillipeds (Makaro, 1938). Pagurus is unable to
pick up the larvae with either cheliped; no larval exoskeleton fragments are
found in either the fecal pellets or the gut.
Tigriopus was observed to crawl all over Pagurus's body and sometimes
to go under the shell covering the gill chamber of the crab. In some cases
Tigriopus came out after the hermit crab was placed in 70% alcohol. Pagurus
could provide another means of transport for Tigriopus between tide pools, but
it does not move between high tide pools as much as Pachygrapsus.
Balanus glandula
This barnacle was collected on the shells of the mussel, Mytilus
californianus. Preliminary experiments showed that adult Tigriopus are too
large for the barnacle to catch with its branched cirri. The barnacles were
observed while in a fingerbowl with larvae, or with a mixture of larvae, the
diatoms, Phaeodactylum tricornatum and Nitzschia longissima, and the flagellates,
Monochrysis lutheni and Isochrysis galbara. The phytoplankters were added to
stimulate filter feeding. The barnacles used in feeding experiments were
placed in fingerbowls after they had been out of water for 18 hours. A small
current was created with a pipette to induce them to feed. The cirri occassion¬
ally caught a Tigriopus larvae and retracted into the shell. However, examin-
ation of the gut contents of barnacles exposed to copepod larvae did not reveal
any larval Tigriopus exoskeleton fragments. Possibly the larvae are rejected
at the mouth and released. At any rate, Balanus glandula is not a predator of
Tigriopus.
Gammarid Amphipods and Isopods
Preliminary observations showed that gammarid amphipods could be
predators of Tigriopus while the isopods are not. The amphipods and isopods
were too scarce in the high tide pools to use in feeding experiments, and are
not common enough to be major predators of Tigriopus.
Mytilus californianus
Preliminary experiments with Mytilus californianus revealed that it is
incapable of capturing adult Tigriopus (Table V). Mussels feed by a ciliary-
mucoid mechanism on the gills. The small frontal cilia on the gills move the
food particles and mucus down the lamelleof the gills bringing them to the
ciliated food grooves where both the food and the mucus are moved foward to
the palps for sorting. The palps reject the larger and heavier particles
which go to form pseudo-feces, while they accept the smaller or lighter parti¬
cles and pass them to the mouth (Meglitsch, 1972).
Dissected living specimens of Mytilus with one valve removed were made
to determine if the gills could pick up and transport the larvae. The larvae
were pipetted directly onto the gill surface and observed to be transported
down the gill lamella to the food groove and then carried to the palps.
Following this, the same preparation of diatoms, flagellates and Tigriopus
larvae that was used to feed Balanus was presented to several healthy Mytilus
from 2.6 cm to 7.6 cm long. After the mussels had been allowed to feed for
at least 24 hours, their pseudo-feces, fecal pellets, and gut contents were
all examined for Tigriopus fragments. The pseudo-feces contained both live
Tigriopus larvae (struggling in the mucus), and some empty larval exoskeletons
which could have been molted exoskeletons. Larval exoskeletons were found in
the stomach and feces of Mytilus. When Mytilus was fed only Tigriopus larvae,
live larvae were found in the psuedo-feces and larval parts were found in the
feces.
Anthopleura elegatissima
Anthopleura elegatissima captures Tigriopus with the nematocysts of
its tentacles. Once the Tigriopus are stung with the nematocysts, they stick
firmly to the tentacles or the tentacles wrap around them. The anemone slowly
transports the tentacles with the Tigriopus to the mouth where they are
ingested. Anthopleura consumed from 5 to 87% of the Tigriopus presented to it.
Tigriopus exoskeletons were found in the anemone feces.
Once Tigriopus became acclimated to the experimental environment with
the anemones, they generally avoided contact with the anemone tentacles; they
climbed around the base and the mouth areas of the anemones without being caught
by the tentacles. Their behavior suggested they were receiving chemical cues
from the anemone.
Anthopleura is able to catch larvae only if they are suspended in the
water column. The anemone itself does not create a current that suspends the
Tigriopus larvae in the water. The larvae are small and the anemone is not
able to sting and grasp them as well as they catch the adult Tigriopus.
Clinocottus analis
These cottid fish are voracious predators on Tigriopus. They fed rapidly
by sighting, moving towards, and snapping at Tigriopus as soon as the latter
were introduced to the fingerbowl. One fish ate all 75 Tigriopus within 3.75
hours (Table VII). The fish fecal pellets were red and contained Tigriopus
fragments. The fish do not actively seek Tigriopus larvae, but they eat them
if they are sucked in with the respiratory current. The fecal pellets contained
Tigriopus larval fragments at the end of the experiment.
Heptacarpus paludicola
This carnivore (MacGinitie and MacGinitie, 1968) is found at the very
lower limit of Tigriopus's intertidal range. It is an active predator of
Tigriopus. The shrimp ate an average of 5.6% of the 75 Tigriopus in each
experiment (Table VIII). Heptacarpus uses its first and second chelipeds
to pick up Tigriopus. It holds the copepod with its legs and chelipeds while
it brings them to its mouth. The shrimp fecal pellets were red and contained
Tigriopus parts. The shrimp capture and eat the Tigriopus larvae using the
same method.
In early experiments it appeared that the smaller Heptacarpus ate more
Tigriopus than the larger ones. An experiment was set up to test the relation-
ship between shrimp size and its feeding rate on Tigriopus. Heptacarpus were
measured from the tip of the tail to the end of the rostrum and divided into
eight size classes over the body length range of 1.2 to 2.7 cm. One to
three predators were placed in a fingerbowl with 75 Tigriopus for 24 hours.
The smallest shrimp which had no experience catching Tigriopus ate more
copepods than the large inexperienced shrimp. However, the large shrimp which
had previously fed on Tigriopus ate more than most of the smaller inexperienced
shrimp (Figure I). The larger experienced shrimp also ate more than the
inexperienced shrimp of comparable size. It appears that the shrimp have the
ability to learn how to capture Tigriopus.
Summary
Under laboratory conditions the major predators of Tigriopus californicus,
in decreasing importance, are Clinocottus analis, Pachygrapsus crassipes,
Anthopleura elegatissima, Pagurus samuelis, Heptacarpus paludicola, and
Trichocorixia (Figure II). However, in natural situations Pachygrapsus and
Pagurus are probably the primary predators in the higher pools. Trichcorixia
is not as common and if it is a predator, it is not as effective as the two
crabs. Anthopleura is an effective predator in the lower high tide pools which
receive some fresh sea water at high tides. Even lower in the intertidal
are the cottid fish; these and wave action could efficiently keep the Tigriopus
population to a minimum down here. Tigriopus were not normally found in the
same tide pools as the shrimps. However, heavy wave action could wash
Tigriopus down to the lower pools where the shrimp are found, allowing the
shrimp to act as occassional predator of Tigriopus.
((
Acknowledgements
I would like to thank Dr. Don Abbott for his never ending patience and
guidance as well as Dr. Robin Burnett, Chuck Baxter and Lynn Hodgson for their
help and suggestions.
Literature Cited
1. Hiatt, Robert W., 1918, "The Biology of the Lined Shore Crab, Pachygrapsus
crassipes Randall", Pacific Science, 2: 13-213
MacGinitie, G. E., and Nettie MacGinitie, 1968, Natural History of Marine
2.
Animals, MCGraw-Hill Book Co., New York, pp. 273, 297, 317
Makarov, V. V., 1938, Anomura, Israel Program for Scientific Translation,
Jerusalem, translated 1962, p. 168
Meglitsch, Paul A., 1972, Invertebrate Zoology, Oxford University Press,
New York, p. 327
5. Pennak, Robert, 1953, Fresh Water Invertebrates of the United States, Ronald
Press, New York, pp. 551-559
6. Usinger, Robert, 1956, Aquatic Insects of California with Keys to North
American Genera and California Species, University of California Press,
Berkeley, pp. 188-196
Vittor, Barry A., 1971, "Effects of the Environment on Fitness-Related
Life History Characters in Tigriopus californicus", Phd. Dissertation,
University of Oregon
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21