PREDATORS OF PAGURUS Robert T. Cok Hopkins Marine Station Introduction The hermit crabs, Pagurus sammuelis and P, granosimanus are abudant on the rocky shore of California. To date no special studies of predation on these crabs have been carried out, although MacGinitie and MacGinitie (1949) note that Octopus apollyon often feeds on them. Mackay (1942) found that the primary food of Eancer magister to be Crustacea under which he lists small crabs as important prey. Pagurids are well protected by their hard exoskeletons and hard shell salvaged from the ocean's bottom. In addition the hermit crabs move about at a fair speed through the water and retract far into their shells when disturbed. When wedged back into their shells it is impossible to pull them out without either damaging the animals or inducing them to release their hold. Amarine animal which feeds on pagurids needs a special mechanism and behavior to extirpate these highly protected animals. The following studies were carried out in an effort to learn more about predation on hermit crabs in thearea of the Hopkins Marine Station at Mussel Point, Pacific Grove, California. Procedure The hermit crabs used in these studies were large specimens of Pagurus samuelis (Stimpson, 1859) and P, gran- osimanus (Stimpson, 1859) occupying shells of Tegula funebralis and T. brunnea larger than 1.5 cm in diameter. Animals studied as possible predators on species of Pagurus included the following: Octopus apollyon (Berry, 1912); the crabs Cancer productus (Randall, 1839), C. antennarius (Stimpson, 1856), C. gracilis (Dana, 1852), Pachygrapsus crassipes (Randall, 1839), and Hemigrapsus nudus (Lana, 1857); the starfish Pycnopodia helianthoides (Brandt, 1835), Patiria miniata (Brandt, 1835), and Pisaster ochraceous (Erandt, 1835); the sea anemone Anthopleura elegantissima (Brandt, 1835); and the hermit crab Pagurus hemphillii (Benedict, 1892). All specimens of hermit crabs and possible predators were collected in the intertidal and adjacent subtidal regions near the Hopkins Marine Station during April and May, 1965. For observations of feeding rates the animals were kept in the laboratory in 17x11x10 inch tanks provided with running sea water at 1300. Between 30 and 60 large Pagurus were placed in each of several tanks and the numbers and weights of each species were determined. Each tank was then provided with a particular species of potential predators. Periodically counts were taken of the numbers of Pagurus remaining and empty shells were removed. As controls, tanks containing comparable groups of Pagurus were set up without predators to establish the mortality rate in the absence of large predators. Details are shown in Fig. 1. During the experiments, notes and photo- graghs were made of the feeding mechanisms of the predators. After termination of the feeding rate experiments the animals were starved and used for detailed study of feeding behavior. O TANK 1.A 2. 3. 4.A 5.A 6.A 7.A 8.A PREDATOR NONE NONE NONE P. HEMPHILI ANTHOPLEURA ELEGANTISSIN HEMIGRAGSUS HUDUS PACHYGRAPSUS CRASSIPES OCTOPUS APOLLYON 2 OCTOPUS AFOLLYON PISASTER OCHRACEOUS PYCNOPODIA HELIATHOIDES CANCER PRODUCTUS 54 CANCER GRACILIS CANCER ANTENNARIUS 41 CANCER ANTENNARIUS 1 CANCER ANTENNARTUS NO. ARIMALS 11 P, sam 28 P, gran 14 P, sam 24 P. gran 42 P, sam 42 P. gran 50 P, hem 28 P. sam 22 1, gran 32 Pagurus 11 P, sam 28 P. gran 1 P, sam 28 P, gran 14 P. sam 24 P. gran 40 Pagurus 7 P. och, 50 Pagurus 2 P, hel. 60 Pagurus 80 Pagurus 25 Pagurus 10 P, hem 28 P. gran 39 Psam 14 P. sam 20 , gran 2 C, ant 27 Pagurus TOTAL WT 68em 180gm 68gm 196gm 70gm 179gm 69gm 181gm 69gm 191gm SHELL LENGTH PAGURUS DIAMETROF EXP ALIVE LEAI 1.7-3.1 days cm 1.5-2.9 cm days ca.1.5- 14 0 3.Ocm days large days days 1.6-2.8 cm days 1.6-2.8 10 cm days 14 1.5-3. 5grap om days 3sam large 12 days large daya foot 26 large days large 15 62 days large 15 days hen 14 large gre days 2 sam 8 sam .7-2.3 cm days 9 gra 24". 24 5-1.8cm days Quantitative Results The mortality rate was zero among the control populations elegantissima, of Pagurus. Patiria miniata, Anthopleura Pachygrapsus crassipes, Hemigrapsus nudus and Pagurus hemphillii Of the other animals showed no predation over a one week span. Results are shown studied all were found devouting Pagurus. in Fig. 1. Feeding rates, calculated from the data in Fig. 1. are shown in Fig. 2. Cancer antennarius and C, productus were the major predators upon Pagurus within the confines of the lab. The feeding rate of Pycnopodia is based on the average of two one foot specimens. The feeding rate of Pisaster is based on seven specimens feeding for two weeks. Fig. 2. Rates of predation upon Pagurus. Key: Cl - controls, P.o. - Pisaster ochraceous, P.h. - Pycnopodia helianthoides, O.a. - Octopus apollyon (2'), O.a.' - Octopus apollyon (1t), C.a. - Cancer antennarius (24"424"), C.g. - Cancer gracilis, C.a. - C, antennarius (3."), C.p. - C. productus, C.a. - C. antennarius (44"). PO. Ph. O.0. O.o. C.O. C.9. C.o. C.p. C.O 15 10 2 5 20 MORTALITY (No. of Pogurus enten per week) 30 3 Qualatative Observations of Predation Pycnopodia helianthoides In the lab the only animal to which Pagurus showed a marked escape response prior to capture was Pycnopodia helian thoides. Pagurus moved quickly away from any P, helianthoides which crawled along the bottom of the tank. Inthe eighteen times I saw starfiches' arms encircle Pagurus' shells I never saw one escape. Within 15-30 seconds the shell was transported to the long tube feet near the oral opening always with the aperture of the shell toward the mouth of the starfish. It usually took between 10 minutes and 2 hours for P, helianthoides to extract the Pagurus from its shell. If at the end of two or three hours the starfish had not extracted the Pagurus it either dropped the shell containing the live Pagurus, or inverted its stomach and digested the Pagurus in the shell. Pisaster ochraceous Although capture by P, ochraceous was never observed, Pagurus after captured showed several escape responses to P, ochraceous. When Pagurus was placed under a starfish arm, Pagurus usually retracted and remained still. After a few minutes the hermit crab usually came out of its shell and struggled actively. Typically it pushed against the glass of the tank and raised the P, ochraceous' arm and then tried to struggle free. Ifthe aperture of the Pagurus' shell was not facing the glass the Pagurus came out, grasped the arm of P. ochraceous, and oscillated the shell back and forth until the tube feet released their grip and the Pagurus could climb free. (Fig. 3 ig. J. 4 Pacumnaten Sek its shell fre from the tube feet of the arm of P, ochraceous. Once a shell was placed under one of the starfish's arms it took at least two hours to transport the shell to the mouth. In the only three complete observations of moving the shells to the mouth, the shell en route to the center was always flipped over so the aperture faced the starfish before it finally reached the mouth. In all cases, P, ochraceous fed by inserting its everted stomach into the shell of the Pagurus In the intertidal region field observations of two P, ochraceous feeding on Pagurus granosimanus were made. (Figs, 4, & 5.) These findings are in contradiction to the survey of Feder (1959) who studied the feeding habits of P. ochraceous on the Monterey Peninsula and never found an hermit crabs. Tound devouitee on a rock at low tide. antennarius Approximately 45 complete feeding observations were made on three adult C. antennarius ranging from 38" to 5' across the widest part of the carcpace. Following is a detailed composite description of its behavior in feeding upon Pagurus spp. Capturing Pagurus As long as C. antennarius did not move violently Pagurus did not react to its presence. During the crabs sedentary periods Pagurus were found crawling over, under, and around its body. Depending on thelocation of the prey, C, antennarius was observed to use three different methods to capture it. If a Pagurus touched the sensitive hairs on the walking legs of C, antennarius, the legs touched were raised and extended over the hermit crab then lowered and flexed to draw the hermit crab below the crab's body. (Fig. 6.) In capturing prey behind its body, C. antennarius extended its last pair of walking legs, encircled the hermit crab posterierly, and swept it forward under its body. C, antennarius was seen to gather as many as eight hermit crabs under its body at one time in; walking legs in Fig. A second means by which C. antennarius captures Pagurus is by reaching out with a cheliped and clamping its pincers around a Pagurus' shell. I have observed t is procedure only about six times, mainly when a Pagurus was located in a corner or was olimbi ig. 7.) t chela Fi aroune and ina oe o The third common method of capture was observed over thirty times. It occurred when a Pagurus moved rapidly in front of C, antennarius. After sighting the moving animal some distance away the crab raised itself on its walking legs so its body cleared the floor by about two inches. The chelae were raised high and the pincers were opened. The crab next tiptoed to the prey by walking on the distal part of the dactyls of the walking legs. (Figs. 8. & 9.) Once the prey was beneath its abdomen the crab lowered its body quickly to the floor while sliding all the walking legs in under the abdomen. At the same time the chelipeds were moved down to 2 Fig. 8. Crab tiptoing over a pagurid in a light colored shel Fig. C. antennarius tiptoing directly over a Pagurus. In the next few seconds the body was lowered and the Pagurus caged. Fig. 10. 4 capture. a under the abdomen of C, antennarius Rackay (1943 described a claw raising behavior in a tank-adapted Cancer magister at the approach of food. He, however, attributed this behavior possibly to a conditioned response resulting from feeding a crab eliciting a defensive behavior. My observations support this hypothesis as I never witnessed any such behavior in any of the Cancer spp. when feeding undisturbed on hermit crabs. Positioning the Shell When shells containig pagurids were located beneath its body, C. antennarius scrapæd a shell forward with either of its two front pairs of walking legs and raised it upward. The chelipeds, first walking legs, and third maxillapeds were used to rotate and position the shell. (Fig. 11.) Usually Fig. 11. This coab gathered six Pagurus under his body and then proceeded to examine one. the aperture of the shell was then examined thoroughly by all three pairs of maxillapeds. Next, the shell was manuevered around while the pincers closed and opened on the shell at various angles. The crab occassionly attempted to crack a shell during this period as shown by the scratches and nicks in the shell. About three out of four times the drab discarded the shell it Whad been examining and brought another shell forward from the storehouse of leleneath its abdomen. (Fig. 12.) Fig. 12. Discarding a shell after examining it. When beginning to feed for the day, C, antennarius examined and tested the first captured shells for five to thirty minutes before it actually applied enough leverage to chip off a portion of a shell. If the crab had already been cracking shells and feeding on Pagurus immediately before he began on another shell, the examination period was very short and never lasted over ten minutes. Cracking the Shell With small or partially broken shells, C. antennarius usually held the Pagurus' shell with one cheliped and crushed it by using the other chela much like a nutcracker. The shell was placed at the extreme proximal end between the pincers, where the greatest leverage exists, and broken. (Fig. 13.) Fig. 13. C. antenarius syrrting off the upper part of a Thais shell with its left pincer. With larger shells, especially Tegula shells 2 cm. or more in diameter, the crab commonly began by inserting the dactyls of the two chelipeds into the aperture of the shell. While one pincer held the shell the other crimped the outer lip until a piece broke off from the whorl. (Fig. 14.) If the pincer did not break off part of the whorl the walking legs many times /02 Fig. . ra loken from a shell. raised one side of thecrab's body into a tilted position while its chelipeds were extended forward, while squeezing the shell harder and harder. In this tilted position the C. antennarius appeared able to apply a greater force with its pincers. By tilting its body and extending its chelipeds the crab usually formed a 90 degree angle or less between its two chelipeds clamped to the shell. Normally the crab's chelipeds function at very obtuse angles to each e chelipeds in Fig. other. (Contrast the 13. & 14, with Fig. 15.) The chela holding the shell always remained in a low position during tilting while the crimping chela moved into a near verticle position. The tougher the shell the more the C. antennarius tilted its body and extended its chelipeds. A tilt of 45 degrees was observed once inan unsuccessful attempt at cracking a very hard shell containing a Pagurus. The average time it took the 44" C. antennarius to extract a Pagurus from a Tegula shell from the time the first chip was made was fifteen minutes (based on 12 timings). The times ranged from 3 minutes to thirty minutes depending pf the shell. (Fig. 16.) mainly on size, ty broken by C. antennarius Fig. 16. A Te graghed innediately which was retrievede after the Pagurus was extracted. If such pieces are left in the tank, the C, antennarius crushes all the large sections to fragments. Note how the crab ehipped away at the body whorls leaving the columella still intact. This shell was examined by the 44" C, antennarius for six minutes and broken down in eleven minutes. Devouring the Pagurus When a shell was broken down so that the Pagurus was exposed, the chelipeds thrust the remaining section of the shell up to the mouth region. With the chelipeds and sometimes the first pair of walking legs the shell was held firmly while the maxillapeds pulled, turned, and pushed the struggling Pagurus. The prey usually disappeared into ompletely exposed. the mouth 1-3 minute the maxillapeds Fig. 17. A sh for extract fon of tne erposed Pagurus. Other Predators Due to its secretive habits Octopus apollyon was only observed feeding seven times in the lab. The octopus grabbed a shell, examined the inside of the shell with the distal portion of an arm, enclosed the shell completlely with its body and arms, and extracted the Pagurus by some unobserved means. Evasterias troschelii was found feeding on a Pagurus hemphillii in the subtidal region in about 20 feet of water. No detailed study was made of the predatory behavior of Cancer productus and C, gracilis. Through casual observation, however, their behavior seemed to resemble that of C. antennarius. Summary 1. Under lab conditions hermit crabs were preyed upon by Cancer antennarius, C, productus, C, gracilis, Pycnopodia helianthoides, Pisaster orchraceous, and Octopus apollyon. In the field fisaster orchraceous and Evasterias trochelii were found preying on Pagurus. 2. Cancer antennarius in the lab was observed to have a specific behavior for capturing and retaining Pagurus. After which the shell was examined and later cracked by varied techniques using both of the crab's pincers. Once the fagurus was exposed from the cracked shell the maxillapeds helped extract the hermit crab and push it toward the mouth. 3. Pisaster orchraceous and oftentimes Pycnopodia helianthoides when unable to extract the Pagurus whole will insert their stomach into the shell and digest the Pagurus. 4. Pagurus in lab tanks reacted to the mere presence of a moving fycnopodia helianthoides and showed an escape response to Pisaster ochraceous after capture. References Feder, Howard M. 1959 The food of the starfish, Pisaster ochraceous, along the California Coast. Ecology 40. No. 4, Oct. 1959. MacGinitie, George E. and Nettie MacGinitie 1949 Natural History of Marine Animals. MoGraw-Hill Book Co., New York, 1949. Mackay, Donald C. G. 1942 The Pacific Edible Crab, Cancer magister. Bull. LXII, Fish. Res. Brd. Can. Ottawa, Mackay, Donald C. G. 1943 The behavior of the Pacific Edible Crab, Cancer magister Dana. J. of Comparative Psych. 36, No. 3, Aug. 1943.