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Crushing behavior of tropical and temperate crabs
J. txp. )w. Bid. Ed.. 1978. Vol. 3 I. pp. 155-I 72 Q Elsevier North-Holland Biomedical Press
CRUSHING
BEHAVIOR
OF TROPICAL
AND TEMPERATE
CRABS
Abstract: The Guamanian xanthids Ctrrpilius mrcdtr~us (L.). C. KVIWW.S I For&al). and Gipltitr .vchw~ and the parthenopid Dtr/dor/itr Irowih (L.). possess large master claws with molariform
(Shaw B; Nodder).
teeth than are used to crush the shells of hermit crabs and snails. These crabs typically
sever the spire
of their prey, or make a gash in the body whorl. They tend to employ sustained pressure on the prey shell. and. except for Eripltiu. Temperate
rarely attack
the outer lip. so that the outer lip of the shell typically
except in shells near the critical size. i.e.. the maximum
undamaged.
species of C’trnwr (C.
p~thr~rusRandall
size of vulnerability
and C. orrgoncnsi
prey in the larger of their two claws. but more commonly
Rathbun)
remums
to predation.
may also crush shelled
they use both claws together in breaking
open
their victims. Sustained pressure is applied for only short periods by these crabs. Gastropod otherwise traits
adaptations
small
lowers
equatorward
aperture,
the critical increase
conferring thickened
resistance to crushing outer
size of the prey,
in the expression
by crabs include a thick shell. narrow
lip. strong sculpture.
i.e.. permits
escape
of the characteristics
or
and a low spire. Emphasis
on these
from
size. An
cushing
at a smaller
of crushing-resistance
parallels
an in-
crease in crushing power of the crabs.
INTRODUCTION
Among the animals that have become specialized to feed on organisms encased in hard shells, crabs are some of the easiest to maintain and observe in the laboratory: nevertheless, they have been surprisingly neglected by biologists. especially in the tropics, where crabs reach their highest diversity. In this paper we describe the feeding behavior of some tropical and temperate crabs which feed on hard-shelled prey, and consider the effect of these crabs on natural selection in some gastropod species. Previous observations of the feeding behavior of shell-crushing crabs have been made largely on north-temperate species. A review of this literature may be found in Vermeij (1977).
METHODS
The xanthids Eriphksebnna(Shaw & Nodder), Cctrpilixs maculculrs (L.), C. convesus (Forskil), and the parthenopid D&for-n horridcr (L.) were collected from intertidal and subtidal areas around Guam (Mariana Islands) in 1974 and 1975. Individuals were kept outdoors at the University of Guam Marine Laboratory in separate. shaded aquaria supplied with aerated or re-circulating sea water at 25 to 29’C. I55
156
EDITH
ZIPSER
AND GEERAT
J. VERMEIJ
Observations of feeding were made during the course of experiments designed to establish the maximum (critical) size at which snail prey are vulnerable to predation by adult crabs (Vermeij, 1976). Prey animals were present at a!! times. usually in sizes large enough to be difficult for the crab to destroy. Observations of shellbreaking behavior were made during spontaneous feeding attempts by the crabs. and neither the choice of available prey nor the state of hunger of the predator was standardized or controlled. Observations were made on the crab’s behavior from the time of touching the prey to that prey’s consumption or abandonment. The duration of certain activities was timed by stopwatch. Comparable studies were done on Eriphia squamara Stimpson at the Smithsonian Tropical Research Institute, Naos Island. ‘Canal Zone and on Cancer productus Randall and C. oregonensis Rathbun at the Friday Harbor Laboratories. San Juan Island, Washington. At Friday Harbor. crabs were maintained in running water at 12-C. Our observations on the critical size of prey were also made in the laboratory. Individual crabs were offered a range of sizes of several species of prey: the critical size of a species relative to an individual predatory crab was taken as the size of the largest individual that was killed. Critical sizes of foreign species were determined after re-occupation of freshly collected empty shells with local hermit crabs (Vermeij, 1976). RESULTS FIELD
OBSERVATIONS
Eriphia sebana, Carpilius maculatus, C. convexus. and Daldorfia horrida are relatively common on reefs and reef-flats around Guam. Most or all of these crabs seem quiescent by day and active by night or at dusk and dawn. Eriphia sebana reaches furthest inshore and to higher levels than do the other species, and is commonly found in holes or under large blocks on the intertidal parts of reef-flats. During the day Daldorfia horrida is always found under very large flat stones in rubbly or even sandy areas. Direct evidence that these crabs crush shelled prey in the natural environment is still very scanty. While snorkeling with us in Pago Bay, Guam, on an August evening in 1975, W. Tobias observed a Carpih’us macuiatus on the reef-flat with a Cymatium muricinum Ridding in its master claw, but whether the shell contained a living snail or a hermit crab could not be determined. On overturning a large stone on a July afternoon in Pago Bay. a small Carpilius macularus was found and caught ; under the same stone was a freshly killed adult Mitra (.Strigatel/a) Iitterata (L.), whose spire had been neatly sliced from the body whorl. In the laboratory, the same crab and other Carpilius maculatus killed living Mitra iitterata in an identical fashion. M. Yamaguchi reports that when he found Daldorfia horrida under large
CRUSHINGBEHAVIOROFCRABS
157
slabs or rock at Cocos Island. Guam, he almost always found freshly broken shells in the immediate vicinity: these included species of Cones, Trochw. and Strombus, and all were damaged in ways identical to those inflicted by Dufdorjiu horridu in the laboratory. We have no direct evidence that Eriphiu sebunu feeds on hard-shelled prey. Such evidence is, however, available for two other species in the genus. Crane (1947) observed E. squumuta eating small gdstropods in tidepools as well as barnacles and in Panama, we have seen it scraping and crushing barnacles from intertidal rocks; the crab also readily eats barnacles in the laboratory. E. verrucosu in the Mediterranean is known to feed on gastropods and hermit crabs (Rossi & Parisi. 1973). Among species of Cuncer. C. productus is known to eat living snails and hermit crabs in the field (Vance, 1972: Spight. 1976; Bertness, 1977). There is similar direct evidence for some other large species in the genus. but not yet for the small C. oregonensis. Cuncer sp. are also known to prey on other hard-shelled animals. and it is unlikely that they or other massively-clawed crabs are speciaiized to deal with a moiluscan diet.
LABORATORY
STUDIES: TROPICAL CRABS
The tropical crabs dealt with here crush prey in their massive master (usually right) claw. Table I gives the critical sizes for various prey species for each of several individual crabs. Clearly, relatively large molluscs can be successfully crushed by adult crabs of the genera Curpifius. Eripiziu, and Dukforjiu in Guam. To emphasize this point further, we offered crabs certain large individuals of species that were generally too rare to permit accurate determinations of critical size. A 138 mm wide male Curpihs macufufus took the dorsal part of the body whorl off a 56 mm long adult Bursu bufiniu (Gmelin); the same crab split a Turbo setosus Gmelin measuring 58.6 mm in diameter and 3.3 mm in shell thickness; a 44.3 mm long, 1.8 mm thick Cyprueu urubicu (L.) was also shattered. Our 65.3 mm wide male Eriphiu sebunu easily crushed a hermit-containing 49.9 mm long and 1.2 mm thick Purpuru putdu (L.) shell from the north coast of Jamaica. A 32.6 mm long, 3.7 mm thick This melonis Duclos shell freshly collected at Panama City. Panama, and re-occupied with a hermit crab. had the venter, lip, and apex broken away by a 115.3 mm wide female Ctrrpilius mucirlutus. The critical size of a prey species is determined both by its own geometrical characteristics (shape and thickness of shell, hardness and structure of shell material) and by the behavior and morphology of the crabs. Since the Guamanian crabs studied are behaviorally and morphologically all similar to one another, it is convenient to deal with one species (Dufdor-u horridu) in detail, and to compare the other species with it. D. horridu differs from most other parthenopids in possessing a master claw with adaptations for crushing hard-shelled prey. Large, blunt molars are located
158
EDITH
ZIPSER
AND GEER;\T T\BLE
Critical
sizes (mm) for crushing of gastropod a shell is foreign. Predator
and prey
horridrr.
Crrithiwu
Lar,vest
Dtwpc~ ricimrs L. Cw~rltunrs ,/iuwvrc.s c’clslm rlrrhitrc~ll1l.s L. Troches
indicate
that
Largest offered __-
Largest knoa n
34.7 24.4 23.2 ‘1.3 24.0
34.7 24.4 26.0 21.3 83.7
27.6 30.6 30.7 30.0 31.3
3Y.O 45.2 46.0 20.5 32.7 25.4 27.6 31.9 37.0 33.8 40.7
I50 50 60 20.5 33.0 26.0 1X.0 50 s3.i J-1.0
27.6 30.6
31.3
27.6 31.3
28.0 I-1.0
26.3 23. I
26.6 24.3
26.6 21.5
33.0 26.0
31.0 28.4 24.0
2Y.5 24.6
33.0 29.5 24.6
33.0 33.0 ‘6.0
-N.-l 18.7
29.4
4s.4 29.4
50 33.0
37.8 28.9 33.5 33.1 26.0 29.6
38.2 26.6 34.0 34.6 38.1 30.0
38.’ 30.9 34.0 34.6 28.1 32.5
I50 33.0 34.0 83.7 44.0
39.0 57.9 56.1 27.6 33.0 40.6 1Y.8 29.8
40.6 85.5 54.6 _
49.0 57.9 58.5 37.6 33.0 43.8 31.0 37.2
150 100 70 28.0 33.0 83.7 44.0
x.7
23.9 Ii.2 J-1.3 1Y.2
: 4.4 lY.4
34.8 -15.2 -11.1 20.5 28.5 25.1 1’. 6 il.9 36.0 31.5 31.3
35.6
female 82.8 mm
niloricesL.
.Sfron~h~.s gihhrrulus
L.
nicoharinurr R6d. Colrrrr~hrllu mrrculorirr L.* Dwptr mowm Ridding D. ricimrs L. .Llorulc~ gramrltrrrr Duclos Thrtis mclotth Ducios’ I’rrsrrr~r rwhCfclhu L. Lwco:onirr Icuco:omrlis Lam.* C0rllr.s sp. D. horriclcr. male 91.5 mm Montlu grunrrlcrro Duclos Lucoxniu lcwco:oncrli.v Lam. * CupiliuT twcdr~trts. female 101 .-I mm Dwpcr morum Ridding D. ricimrs L. C. n~trcuk~~r~s,male 105.3 mm Cxpractr caprrtserprmis L. Drupcr morum Ridding D. ricimrs L. C. w~~lrrt~~s. female 105.4 mm Slromhus gihhrrrrhrs L. Drupa mown Rading C. w~culur~s. female I I I .3 mm Troches niloricus L. Drtrpu morum Rading Cunthnrus undosu.7 L. I/cl.,tu~ ~rrrbinellrrs L. Lrucozonia Irucozordi.~ Lam.* comes sp. C. n~~/rrrfr.s. female I 15.3 mm Troches niloricw L. Caiflriwn nochilos~un Sow. Bursa hu/bniu Gmelin Mow/a grantrlura Duclos Dwpa marum Ridding Iir.iwv rm+ine/hcs L. L~~~coxmiu kwco~onulis Lam. * Conur sp. Cj~tnofIwI
Smallest unritten
asterisks
female 69.6 mm
cohmw~~r Sow.
C~~prcrca it~oncfu L.
D. horritlrr.
I
prrq relative to individual crabs: x-occupied b> a hermit crab.
Ciltrn
Dalrlor~ia
J. VERMEIJ
46.0 2Y.0
_
‘8.3 43.8 29.1 30.8
CRWSHlNC
BEHAVIOR
OF CRABS
tj9
T-\BLE I ~~ootinued)
Largest
Smallest
Largest
38.2 58.6 Y-J.0 56.1
41.8 71.7 83.1 59.0
4s.’ 71.7 88.5 60.8
29.0
31.3
31.3
37.8 27.4 29.0 23.5 27.5 32.7 16.7 13.7
35.2 29.7 33.0 ‘7.4 29.3
19.7 31.7 16.7 17.0
17.0
__. ?’ 4 19.0 f-l. I 17.3 ‘5. I 26.9 lb.8 13.3
15.6 22.6 23.6 31.5 18.2 17.0 __. ” 8 16.1 24. I
‘J.8 71 3 __. is.0 17.6 I’.0 29.2 22.1 __. ‘3 6 34.0 21.0 20.2 20.5 18.0 24.4 Il.9 15.6
79.4 ‘2.6 ‘3.9 34.0 21.4 20.2 23.5 19.9 _?7 .-’ 13.3 21.4
$5.8 ‘7.9 ‘7.1 21.9 _.
25.8 _
30.3 27.9 30.0 75.5 20.0
‘7. I
28.
I
28.7
27.0
27.9
_‘7 .9
-
28.7 19.5 18.6 20.0
Largeit
160
EDITH
ZIPSER
ASD
TABLE Predator
and prey
E. sqrramura. male 38.0 mm Teguia pellisserpentis Wood Nerifafirniculara Menke Acanrhina hrevkienrara (Wood) Thrris melonis Duclos 7. rricmguluris Blainv. Cows
nu
GEERAT
I (continued)
Largest
Smallest
Largest
Largest
eaten
uneaten
offered
knoivn
1-2
18.8 II.4
18.8 22.X
44.2
11.6 19.5
32.9
25.5
19.0
25.7
35.0 50
16.4
” I _-.
25.0
25.0
15.9
15.9
25
‘4.5 30. I
26.4
26.4
30.1
30.1
30. I
17.7
18.5
22.9
25
29.0 31 1 __._
?O.I
18.9 16.4
16.4
25
AS.6
44.5
49.2
84.0
72.3
74.4
74.4
29.4
25.8
31.0
38.0
25.3
20.9
31.2
St.0
29.5
29.8
35.2
35.2
30.0 30.0
30.0
30.0
38.0
25.0
30.0
84.0
_
28.2
34.0
84.0
36.6
39.3
39.3
55
29.2
29.2
Broderip
E. squumaru. male 39.9 mm Trochus niloticus L.” Cerithium siercusmuscwum Val. Planuxis plunicoslurus Sow. E. sqrtumura. male 41 .O mm Cerifhium sfercusmuscarum Val. Acanrhina brevidentatu (Wood)
29.0
Conrrs IIKY Broderip
Cancer prochrcfus. male 122.9 mm Thuis Iamellosa Gmel.
J. VERMEIJ
24.0
I50
35.0
(smooth thick form) C. prothrcrus. male 123.7 mm
Ceratosroma foliarum Gmel.
100
C. oregorrensis. male 36.0 mm
Thais canalicrtlara Duclos T. lamcllosa Gmel. (smooth thick form)
Searlesiu tfira Reeve C. oregonensis. female 40.0 mm
Thak cunaliculura Duclos T. lamrllosa Gmelin (smooth thick form) C. oregonensis. female 49.5 mm
Thais Iumellosa Gmelin (smooth thick form) T. lamcllosa Gmelin (spiny thin form)
Amphissa cohtmbiana Dall
29.2
on the proximal apposing surfaces of both dactyl and fixed finger. i.e., where mechanical advantage of the pincer is greatest. The molar on the fixed finger extends nearly halfway to the tip of that finger. The chelipeds of D. horrida are elongated. and the four individuals observed in the laboratory tended to move them slowly. often one segment at a time. Rather then moving their chelipeds swiftly in the capture of prey, D. horrida most often made contact with snail and hermit-crab prey by lowering its body upon the prey. trapping it within a cage of abdomen and legs. A cheliped was often used to pick up a prey item from beneath the crab. Once in position, the prey is manipulated deftly by both chelae, as well as by the mouthparts and the first and/or second pairs of walking legs. Snails may be
Fig.
I
Ih?
FDI
1-H ZIPSCR
.\\D
GELRAT!
L EK1iFt.I
turned or rotated ;L few times. but \\ithin minute> the large &la ~$as IISLUIJ~ placed around part of the prey’s shell. XIost often. the master cla\\, is held in front of the crab. and the prey shell held by it is additionally supported From the opposite side by the small chela. from abo6.e by the mouthparts. ;lnd from belo\\- by the first t\\ o pairs of walking legs ( Fi g. 1). Periods of manipulation of the shell alternate R ith periods ofholding the shell in the large chela. If the prey proves difficult to break. the crab may spend more than Linhour in continuous effort, and may grip the prey in tht large claw for Ions periods of time. In order to estimate the amount of time spent in this position. a ‘hold’ \v;ts arbitrarily defined :IS ;I grip b>,the Inrpe chrla lasting longer than 5 sec. The duration of each hold in stxeral shell-breaking cpisodcs \cas dctermined (Table II). An 52.8 mm wide D. Iror~~itk~\~hile making a fatal hole in ;I ‘5 4 mm lone Dmp~/ ricimr.s (1.). used 20 holds Isstin,n L‘in average of 90 set each : 49”. -_. ofthe feeding episode of 37 10 SK was spent in holding the prey. The i.ery limited data of Table II suggest that iveakcr-shelled snails require less holding actitity, in both
340 90
0
I
0 15
28
0
3240
10
39
9
75
I
1910
I4
IO 77
56
13
;I rclati\,e and an absolute sense. Thus. the relatively weak shells of S~~onzh~s ,~~~~cIw/I~.F (L.) were broken after febver and shorter holds when compared ivith the tougher shells of Druptr ricitm. Less complete obser\xtions of the shell-breaking behavior of Duit/or/ic~ using other prey species support this conclusion. D. lwrrido gi\,es every impression of exerting considerable sustained pressure during most holding periods. Crabs quiver. rock back and forth. and occasionally lose their balance. A @rip is often accompanied by grinding or cracking noises. and is
CRUSHING
BEHAVIOR
163
OF CRABS
sometimes terminated by the prey shooting across the aquarium as if it had been released from the claw under pressure. Crabs may occasionally hold prey without discernible movenlent or apparent exertion. We have never seen D. ~r~~~~~ti{~ extract the soft parts of a prey snail without breaking the shell of the latter. Thus. even largeapertured species such as Neritl-r dbicillrr L. (whorl-expansion rate greater than 3.0) are inevitably shattered if the soft parts are to be eaten. If a prey shell. such as Mon~fa g~~m~/crtcr(Duclos) or Ceri;hitrtn cohtntrtrrSowerby, is small enou_eh to fit between the fingers of the master claw. the shell \silI be crushed through the middie rather than at one end. Small C. ~olrrn~rtr ( ~30 mm length) are typically broken in half. perpendicular to the axis of coiling. This is also the case with snails such as small T~~~*h~rs ni/otiul.y L.. Ctrnt/wu.s w~losu.s (L.). Stwtnbus mtrtctbilis Swainson. C’_rm~ti~m~t~icohrwicwn ( RGding). and Pwi.stmzirr ~z~fss~ttlfi~t Lam. whose spires are relatively tall and protruding (apical h~llf-~~n~le, ~45 ). In generai. the outer tip remains intact in such small or Lveak shells even though it could be broken easily. When large shells of these species are attacked. the shell wall is. however, too thick for the spire to be severed completely and the crab’s crushing efforts often result in lip fracture (see Table III). It is noteworthy that individ~~Is of thin or weak-lipped shells that are near the critical size for the attacking ~u~~~~~~~~~~ are never killed as :1 result of lip fracture: damage to the lip is not substantial enough to expose the soft parts. and a hole or gash must be made through the wall of the spire or body whorl if the crab is to get any nutritional benefit from its victim In unsuccessful attacks. the crab intlicts damage to the shell lip. ivhich must then be repaired.
Mode of predation Predator
on snails as a function of prey size. Size and fate of prey
and prey
28.0 mm. 32.0 mm: ape.x removed 32.9 mm: base removed 33.8 mm. 34.8 mm: anterior
periphery
35.1 mm, 35.6 mm. 42.0 mm: periphery
removed and inner lip chipped
20.3 mm (juv.): crushed 23. I mm
: apex
removed
21.1 mm: split perpendicular
to outer lip
24.3 mm: siphonal area damaged 24.5 mm. 25.4 mm: spines cropped on lip 26.3 mm 26.6 mm
: dorsum removed : spines cropped on
20.7 mm: crushed 19.0 mm: left side removed,
outer lip
lip chipped
14.0 mm: apex obliquely removed 24.6 mm. 25.4 mm: spines cropped on lip
164
EDITH
ZIPSER
AND
GEERAT
J. VERMEIJ
TABLE III tcontinued) Predator
and prey
D. morw,,
C. ntutitlnr~~. 105.4 mm Strombus gihbrrulrrs
C. mriculfztw. I 1I .3 mm Trochrrs niloticu.s
Size and fate of prey 21.6 mm: apex removed 28.2 mm: punctured 29.5 mm: unmolested 39.6 mm: apex removed 45.3 mm: apex and outer lip removed 48.4 mm: peeled 36.0 36.8 37.8 38.2
mm: apex and base removed mm : part of base removed: lip damage mm: small hole in base: lip damage mm: chips on periphery and outer lip
20. I mm: left side removed 2 I .2 mm: damage to siphonal canal 25.2 mm: spines sheared from outer lip C. mucu/uttcs.1IS.3 mm Trochus niloticus
Eriphictsebuttn. 43.6 mm .Verirtr ulbicilhr
Cerithium cohunntr
E. sehunu. 56. I mm .Veritu olbicillu Cl~peomor~u maria
E. sehana, 49.3 mm Cerithiwn colicmna
E. sebanu. 65.3 mm .Verita albicill(t
.V. plicato
37.5 37.7 39.6 40.6
mm: mm: mm: mm.
apex removed small holes in base and above periphery hole in base 40.9 mm. 47.2 mm. 49.0 mm: lip damage
23.6 mm: left side and posterior removed 23.0 mm, 23.6 mm. 23.9 mm. 21.3 mm: extracted 18.2 mm: lip and apex removed 21.0 mm, 21.1 mm. 21.4 mm: lip damaged 23.0 mm. 21.1 mm. 24.9 mm. 25.0 mm. 27.6 mm. 28.3 mm. 29.3 mm: apex removed 31.5 mm: outer lip removed 34.0 mm: intact 19.2 20. I 15.2 17.0 19.0
mm: mm. mm. mm. mm:
crushed 2 I. 1 mm. 22.3 mm: extracted 15.3 mm: crushed 17.8 mm: anterior of shell removed damage to outer lip
19.5 mm, 19.6 mm. 19.9 mm. 21.6 mm. 22.9 mm. 23.9 mm, 24.5 mm. 25.4 mm, 25.4 mm. 25.7 mm, 26.2 mm: apex and outer lip removed 26.2 mm, 26.9 mm: peeled 32.3 mm: lip damaged 19.8 mm, 20.8 mm. 22.8 mm. 22.9 mm. 25.0 mm, 25.6 mm. 27. I mm : crushed 28.7 mm: extracted 30.0 mm: not eaten 19.1 mm, 19.4 mm. 19.6 mm. 19.9 mm. 10.3 mm. 22.5 mm, 24.3 mm: crushed 23.5 mm: left side and venter removed 27.9 mm: left side removed
4Y.J mm. SO.11mm
: cruhcd
53.3 mm: ventral gab
7-U mm:
crushed
li4.0 mm. 252 3.8
mm: anterior
rrmo\-ed
mm: pwlcd
21.7 mm: crushed 27.8 mm: apx.x and anterior
removed
__. .i 0 mm, 3.2
rrtno~ed
mm: anterior
Such repairs are generally unnecessary for species w-hose outer lip is thickened or dentate within. Examples of genera possessing such lips in the adult stage are C_vtttutiutu. Bwxt. Dtwpn. 2tforul~r, Mitrnr (Srrigrrtdltr). and C~~ptwtr. In adult Crrirhirm, Lmthis. and Strombus, the outer lip is thickened and flaring. but not retinforced with teeth. Drup and certain species of i~lor~t~ft are among the sturdiest shells oftheirsize, possessing not only a heavily re-inforced outer lip but also a short. thickwalled spire which cannot easily be severed. Successful attacks by Ddriortict involve partial breakage of the body tvhorl dorsally or on the left side (Fig. 1). This brr:lk is effected by 3 slanted grip around the apex and the left shoulder of the bodl \t,horl. When such attacks fail. the only indication of an encounter \\.ith ;I crab is the cropping of a fe\v knobs or spines on the outer surface of the body ivhorl or outer lip: this damage is minor. and does not need repairing. The smooth slippery shells ofcowries (C_I~XYWU) are held with one finper of the cInt{ on the base of the shell (apertural side). and the other on the dorsum. The dorsum is always the first part of the shell to fail in adult couries; the base breaks onI\ in small animals. The shells of cones (Cotm) are very short-spired and esceedingly strong. >fost commonly. the anteroventral portion of the body whorl is broken away ; rarely can the heasily thickened spire be severed. Relatively small individuals are often split parallel
to the axis of coiling. Every successful and unsuccessful attack on C’ontts is accompnnied by injury to the thin outer lip. but in no case could the lip be broken back far enough to expose the soft parts sufficiently. Cq~ifi~~~ tmtcw/m~.s and its smaller but twy similar congener. C. cotwstt.~. both hate master cla!vs uith blunt proximal molars. The molar on the fixed finger is rounded and not elon,uated as in Drtkiwfi~t (C’ermeij. 1977). Individual Cayiii~s differ in the amount of xe;tr on the mofrux and some molars are tr’orn flat with use, The shell-bre~l~~~l~behavior of a C. ~~~~~~lf~~if~~.s faced with a tough prey shell,
CRUSHING
BEHAVIOR
OF CRABS
167
such as Druptr. C~~pruw or Conus. is similar to that described for Dtrldorfia. First contact with the prey is usually made with the legs and or the small chela rather than Lvith the abdomen. The positions assumed by the chelae. legs, and mouthparts during manipulation and holding of the prey are similar to those in D. hot-r-idrr. Again. shell breakage is primarily by crushing, and in\.olves attack by way of the aperture or outer lip only when spire-breaking is impossible. Two short experiments give some impression of how important predation by Cupilius may be to the prey gastropods that co-occur \jith this crab (Table IV). On 2nd June. 1975. all the gastropods in a I rn: quadrat near the hiding place of a 105.3 mm wide female C. ~I~I~U/~UKY were collected and offered to this crab in the laboratory as prey, By the fifth day. 9 of the 12 snails (73”,,) had been consumed. and 1 had received substantial shell injuries. On 7th June. this same crab \vas given another sample of snails from a 1 rn’ quadrat near its former hiding place. By 12th June. 8 of 15 prey had been consumed. As is evident from Table 111.snails not eaten by the crab in this second trial Lvere either above the critical size or were very small ( < 10 mm long).
Effect of predation
after 5 days by a 105.4 mm uide C~rpili~~ m~~c~~l~/!~ts female on gastropods of two 1 mz quadrats
Sample II. 8 of
I5 prey
in each
ne;~r hiding place in P.!go Bay. Guam.
eaten
Prey eaten. COUUS rhraeus: 22.5 mm C. spomtrli~ : 2I .4 mm Cerirhifon colwmc:: 17.1 mm. X.9 mm I’n.r~rtrt rurbinrllu.s: 21.7 mm. 27.0 mm Crrirhim sqjw~iwr: 13.7 mm Prey not eaten.
The attack behavior of Eriphicr species is similar to that of Carpilius and except that extraction of soft parts without damage to the shell is common in Eriphin. Eriphicr sebcuw in Guam was able to extract the soft parts of Nerirrr nlbicilh if the latter were large enough (Table III); Nerircr has a large aper.ture and a correspondingly very high expansion rate (W) of the ivhorls ( 8 > 3.0). In Panama. Dnldotficr,
168
EDITH
ZIPSER AND
GEERAT
1. VERMEIJ
Eriplh sqwmrra extracts This trimguhis
Blainville ( W, 2.6) when the shell of the latter reachesa size too large to becrushed or peeled. Probably in association with this extracting behavior. Eriphicr often attacks snails at the outer lip but. with smallapertured species such as Cerithium cohnmr, this method of attack is usually unsuccessful. As with the other genera of crushing crab described earlier, successful crushing usually involves severing the spire or making a gash or hole in the body whorl of the shell away from the outer lip. LABORATORY
STUDIES:
TEMPERATE
CA.VCER
Adult Ccrncer productus have relatively more slender and more mobile chelipeds than those of Carpilius. The chelae are small and subequal, and are lined with small teeth on the apposing surfaces of the fingers. First contact with the prey. at least in the laboratory, is most often made by a sweeping motion of both chelipeds: the chelipeds are extended laterally, then quickly sweep the prey toward the mouthparts by coming together medially in front of the crab. Legs may also contact the prey. When attacking relatively small prey. such as This crrrxrficuf~~rcr Duclos. crabs most often break the shell between the fingers of the larger chela. Relatively large prey, such as Cercrtosroma .fblicrtwn (Gmelin) and Fusitriton oregonensis ( Redfield). are frequently attacked using both chelae, and the flesh is most often exposed by attacks concentrated at the aperture. The prey is held on the bottom of the aquarium in front of the crab, with the aperture upward. In the trans-apertural grip. each chela grips a structure on the opposite side of the aperture: e.g., when the apex points toward the crab, the left chela grips the outer lip, and the right chela grips the columella and body whorl. The movable fingers (dactyls) are always above or dorsal to the fixed fingers; both dactyls are inside the aperture of the prey and point toward each other. The fixed fingers extend under the prey shell. The crab, while keeping both chelae on the aperture. is able to move its chelipeds from a position in which the propus segments are nearly vertical, with carpus segments or ‘elboivs’ above the carapace, to a position in which the propus segments are nearly horizontal. with ‘elbows’ out to either side of the crab. The crab moves the propus segments vertically together, and horizontally apart, the chela meanwhile pivoting around the shell structures and presumably pushing lip and body whorl alternately toward and away from each other. In two other methods of apertural attack (cis-apertural attacks), both chelae grip a single structure, namely, either the outer lip or the columella (with body whorl). One dactyl and one fixed finger are inside the aperture. In the cis-apertural grip, the chelae may act as a pair of scissors, applying a twisting or shearing force between them as the chelae try to rotate in opposite directions (Fig. 3). Ccuzcer productus changes the position of its claws so frequently during manipulation and breakage of shells that complete records of the sequence and duration of its movements could not be obtained. Few positions were held for as long as 5 sec. Exact comparison between the behavior of Cancer and tropical crabs is thus im-
possible.
.A large ( 137.4 mm u ide) malt C. ,PIV~IU~~~~I.S \v;lj = oivcn 12 small prey. vi:.. 6
Tluris Itrtm~liosc~ (Gmelin) ranging in shell length fwm 26.5 to 31. I mm. and 6 hermit crabs inhabiting T. /mwl/~~,st~shells of the same size range (36.3 35.5 mm). The crab killed the first t\\o prey (hermits)
by crushing
\+ith the larger chcla. a third
\v:Lj damaged by crushing the hodv ~\horl of its shell. followed attack, and a fourth prey was opened by a trans-apertur;~l consumed
kvithin 2 days. and no preference
hermit
by a trans-rqxrtural attack: all 12 were
for hermit crabs over snails MS elidcnt.
long
Tiuris umrlicdr~tn. The C~ttcer- crushed
the body cvhorl of the Thcri.7Lvith its larger
claw Lvithin 5 min. The same crab MXS immediately given a second. tougher shell. (T. /cn~~cNo.~r~. 3 1.3 mm long). After two vain attempts to crush the body whorl the crab used only cis- and trans-apertural attacks for the remainder of an unsuccessful 2-Lmin feeding attempt. The same crab successfully broke back the adult lip of a 60.0 mm ~(‘I.LIr~).).tOlllC[.fi)/iC/flllll: it tried approximately 1 grip \vith the larger chela on the apex. 4 trans-apertural attacks. and 9 cis-apertural attacks. the latter all on the lip. Three of the cis-apertural attacks on the lip were effective in breaking off pieces of shell large enough to be seen. If the attacks that resulted in significant shell breakape are extracted from the general record. it may be seen that. for Cntzcrr /JrdW~ll.S. attacks on the outer lip are most often successful in breaking difficult
prey. Siint shell brcakagc by four C. pi.Llcil/i iiu during eight feedins attempt5 maq- be chaxterized as follws: twice bq crushins u ith the large chela. eight times: by trans-:~perturaI attach. and 25 timcs bq cis-apertur;ii attack (c)t‘ \ihich 5 were directed to the col~~~n~li;~ and 20 to the outcr lip). .-I similar a:ulysis !;x D~~/d,wfi~~ lwwith in ths tropical Pacific ~vould shw that IIJIJ”,,ot‘ s~~ccessful she!l-breaking in swcn feedin: episodes is by crushin s \\ith the I:trzc ~~hcln. In Cut.pi/i~c.,. too. crushing 1~1th thtr large chela is the most successful method of breaking large pre”. Ctr~lcw 0rc~~o~vz.si.s is similar to C. ~~~oc/M~~~~s in general form. but is much 5mallcr and has larger cln~.s relative to its size (Vermsij. 1977). Our only x.isibly voracious individual. ;I large (49.5 mm tvide) female lvith a larger right chela. shoived a preference for trans-apertural attacks. In \\,orkin=u unsuccessfully for 51 min on ;i C‘d/iosto/luz Iigufwn Could 13.6 mm in diameter. most (37 of 41 ) of the recorded attacks Lvere on the aperture, \
Our data on shell-breaking by crabs confirm and amplify earlier \+.ork by Vermeij (1976. 1977) and other workers. \vho sho\\,ed that temperate crabs are less specialized for crushing hard-shelled prey than are certain massively-clawed tropical xanthids and parthenopids. All crabs. including temperate species of Ctu~wr. crush small prey in the master claw and .~l~~ctvpips. Curcims, and H~v7~&~1p.s1rs. sever the spire. Larger prey are generally attacked at the aperture (except in c‘mpili~~ and Dtr/h~/~~r), and are killed by successive peelins of the body ivhorl (Eblinp CYal.. 1964; IMuntz. Eblins & Kitching. 1965: Fears. 1970: Rossi Sr Parisi, 1973: Kitchinp &I Lockbvood. 1974). Removal of the soft parts from the aperture without injury to the shell has been described for .Llrrcl-q~iprs puhn. Cmci~~m C C.. Gibson. 1970: Rossi & Parisi, ~~~wILI.~. and Eripllitr ~‘tvv~~us~~ (Muntz 6’1(II.. 1)6_ 1973). Tropical crabs can take larger prey than temperate crabs of comparable size (Vermeij. 1976) and appear to use ‘one-handed’ crushing more commonly than theq use apertural extraction or lip fracture as methods of attack. Members of the
CRUSHING BEHAVlOROFCR.-1BS
171
tropical and subtropical genus Cduppct are highly specialized to peel the outer lip of snails in the fashion of a can-opener. so that a spiral gash which may extend as much as two whorls back from the outer lip (Shoup. 1968) is made. Warner& Jones (1976), among others. have pointed out that there is an apparently irreconcilable conflict in decapod crustaceans between agility and speed on the one hand, and sustained power on the other. Decapods have a range of muscle-fiber types, including rapidly contracting fibers with short endurance times, and slow fibers capable of more sustained contraction. We suspect that the claw-closer muscle in claws adapted for prolonged application of pressure contain a high proportion of slow fibers. This prediction is consistent with the findings of Warner & Jones (1976) who showed that the proportion of slow as compared with fast fibers is greater in the claws of Cctmwprtgrtnts and ,2/la~,-opi(,tt.spt1hc~ than in claws of the much more agile M. ~~~pi~~~tt~~ (L.). In the tropics, then, crabs have achieved a far greater adaptive range than they have on temperature shores. Tropical crabs range from extremely active portunids able to catch fish or other fast-moving prey (Schafer. 1954) to crabs whose motions are slow even at high temperatures, and which are specialized to crush slow, heavily skeletonized prey. This specialization toward crushing has been carried to an extreme in certain xanthids and parthenopids. whose movements are extremely slow and clumsy. Temperate crabs. on the other hand. are generally neither as powerful nor as agile as are many of their tropical counterparts. Predation by crushing appears to be a significant source of adult mortality among tropical gastropods (Vermeij, in press}. Our laboratory observations support the view that various morphological adaptations of the gastropod shell confer resistance to crushing by crabs and other predators. These traits include thick shells, a narrow or otherwise small aperture, a thickened outer lip, strong sculpture, and a short spire. Temperate snails show a lower frequency and lesser development ofthese features, and appearto be less well adapted and more susceptible to crushing. While crushing-resistant traits would be adaptive in temperate as well as in tropical snails, their reduced significance on colder shores may reflect compromises ivith other adaptations that demand conflicting morphology. Moreover, snails and crabs alike face physiological constraints on calcification imposed by periodically or abnormally low temperatures, and the adaptive options available to them may be limited (Vermeij. in press).
ACKNOWLEDGEMENTS
Drs L. Eldredge and M. Yamaguchi kindly provided us with space in their laboratories during our stays in Guam. We are also grateful to the staff of the Friday Harbor Laboratories and the Smithsonian Tropical Research Institute for providing space and facilities. Several colleagues helped in collecting the crabs.
172
EDITH ZIPSER AND GEERAT J. VERMEIJ
This work was funded in part by grants from the National Geographic Society and the Program of Biological Oceanography, National Science Foundation. Support in the form of a John Simon Guggenheim Memorial Foundation fellowship to G. J. Vermeij permitted us to spend much time in marine laboratories, and is gratefully acknowledged.
REFERENCES BERTNESS.M.D.. 1977. Behavioral and ecological aspects of shore-level size gradients in Thais kmrellosa and Thuis enrar~imrra. 0oiog.1,. Vol. 58. pp. 86-97. CRA?IE. J.. 1947. Eastern Pacific expeditions of the New York Zoological Society. XXXVIII. Intertidal brachygnathous crabs from the west coast of tropical America with special reference to ecology. Zoologica N. Y.. Vol. 32. pp. 69-95. EBLING, F. J., J.A. KITCHING. L. MUNTZ & C. M. TAYLOR. 1964. The ecology of Lough Ine. XIII. Experimental observations of the destruction of .Ll~ri/~~edalis and lVlrce/lcrIapilluv by crabs. J. Atlim. Ecol.. Vol. 33. pp. 73-83. FEARE. C. J.. 1970. A note on the methods employed by crabs in breaking shells of dopuhelks (Nucella lapillus). Ncrrrrmlisr. HaN. No. 913. pp. 67-68. G~ssos. J. S.. 1970. The function of the operculum of Thais lapilhrs (L.) in relation to desiccation and predation. J. A&n. Ecol. Vol. 39. pp. 159-168. KITCHING,J.A. & J. LOCKWOOD.1974. Observations on shell form and its ecological significance in thaisid gastropods of the genus Lepsiella in New Zealand. Mar. Biol.. Vol. 28. pp. I3 I-144. MUNTZ. L.. F. J. EBLING& J.A. KITCHING.1965. The ecology of Lough Ine. XIV. Predatory activity of large crabs. J. Anim. Em/.. Vol. 34. pp. 31.5-329. ROSSI. A.C. & V. PARISI, 1973. Experimental studies of predation by the crab Eriphitr vermcosa on both snail and hermit crab occupants of conspecific gastropod shells. BON. Zoo/.. T. 40. pp. 117-135. SCHAFER.W., 1954. Form und Funktion der brachyuren Schere. Abh. senkenb. natrrrjorsch. Ges., No. 489. 66 S.
SHOUP. J. B.. 1968. Shell opening by crabs of the genus Calappa. Science. N. Y.. Vol. 160. pp. 887-888. SPIGHT,T. M.. 1976. Colors and patterns of an intertidal snail, Thuis lame//osa. Res. Popal. Ecol.. Vol. 17. pp. 176-190. VANCE. R.R.. 1972. The role of shell adequacy in behavioral interactions involving hermit crabs. Ecology, Vol. 53, pp. 1074-1083. VERMEII,G. J.. 1976. Interoceanic differences in vulnerability of shelled prey to crab predation. Nufure. Lond.. Vol. 260, pp. 135-136. VERMEIJ.G.J., 1977. Patterns in crab claw size: the geography of crushing. S.wf. ZOO/.. Vol. 26. pp. 138-151. VERMEIJ.G. J.. in press. Biogeo,rwp/tJ, and adapra/ioa. Harvard University Press. Cambridge. Mass. WARNER.G. F. & A. R. JONES. 1976. Leverage and muscle type in crab chelae (Crustacea: Brachyura). J. Zool. Lond., Vol. 180. pp. 57-68.
CRUSHING
BEHAVIOR
OF TROPICAL
AND TEMPERATE
CRABS
Abstract: The Guamanian xanthids Ctrrpilius mrcdtr~us (L.). C. KVIWW.S I For&al). and Gipltitr .vchw~ and the parthenopid Dtr/dor/itr Irowih (L.). possess large master claws with molariform
(Shaw B; Nodder).
teeth than are used to crush the shells of hermit crabs and snails. These crabs typically
sever the spire
of their prey, or make a gash in the body whorl. They tend to employ sustained pressure on the prey shell. and. except for Eripltiu. Temperate
rarely attack
the outer lip. so that the outer lip of the shell typically
except in shells near the critical size. i.e.. the maximum
undamaged.
species of C’trnwr (C.
p~thr~rusRandall
size of vulnerability
and C. orrgoncnsi
prey in the larger of their two claws. but more commonly
Rathbun)
remums
to predation.
may also crush shelled
they use both claws together in breaking
open
their victims. Sustained pressure is applied for only short periods by these crabs. Gastropod otherwise traits
adaptations
small
lowers
equatorward
aperture,
the critical increase
conferring thickened
resistance to crushing outer
size of the prey,
in the expression
by crabs include a thick shell. narrow
lip. strong sculpture.
i.e.. permits
escape
of the characteristics
or
and a low spire. Emphasis
on these
from
size. An
cushing
at a smaller
of crushing-resistance
parallels
an in-
crease in crushing power of the crabs.
INTRODUCTION
Among the animals that have become specialized to feed on organisms encased in hard shells, crabs are some of the easiest to maintain and observe in the laboratory: nevertheless, they have been surprisingly neglected by biologists. especially in the tropics, where crabs reach their highest diversity. In this paper we describe the feeding behavior of some tropical and temperate crabs which feed on hard-shelled prey, and consider the effect of these crabs on natural selection in some gastropod species. Previous observations of the feeding behavior of shell-crushing crabs have been made largely on north-temperate species. A review of this literature may be found in Vermeij (1977).
METHODS
The xanthids Eriphksebnna(Shaw & Nodder), Cctrpilixs maculculrs (L.), C. convesus (Forskil), and the parthenopid D&for-n horridcr (L.) were collected from intertidal and subtidal areas around Guam (Mariana Islands) in 1974 and 1975. Individuals were kept outdoors at the University of Guam Marine Laboratory in separate. shaded aquaria supplied with aerated or re-circulating sea water at 25 to 29’C. I55
156
EDITH
ZIPSER
AND GEERAT
J. VERMEIJ
Observations of feeding were made during the course of experiments designed to establish the maximum (critical) size at which snail prey are vulnerable to predation by adult crabs (Vermeij, 1976). Prey animals were present at a!! times. usually in sizes large enough to be difficult for the crab to destroy. Observations of shellbreaking behavior were made during spontaneous feeding attempts by the crabs. and neither the choice of available prey nor the state of hunger of the predator was standardized or controlled. Observations were made on the crab’s behavior from the time of touching the prey to that prey’s consumption or abandonment. The duration of certain activities was timed by stopwatch. Comparable studies were done on Eriphia squamara Stimpson at the Smithsonian Tropical Research Institute, Naos Island. ‘Canal Zone and on Cancer productus Randall and C. oregonensis Rathbun at the Friday Harbor Laboratories. San Juan Island, Washington. At Friday Harbor. crabs were maintained in running water at 12-C. Our observations on the critical size of prey were also made in the laboratory. Individual crabs were offered a range of sizes of several species of prey: the critical size of a species relative to an individual predatory crab was taken as the size of the largest individual that was killed. Critical sizes of foreign species were determined after re-occupation of freshly collected empty shells with local hermit crabs (Vermeij, 1976). RESULTS FIELD
OBSERVATIONS
Eriphia sebana, Carpilius maculatus, C. convexus. and Daldorfia horrida are relatively common on reefs and reef-flats around Guam. Most or all of these crabs seem quiescent by day and active by night or at dusk and dawn. Eriphia sebana reaches furthest inshore and to higher levels than do the other species, and is commonly found in holes or under large blocks on the intertidal parts of reef-flats. During the day Daldorfia horrida is always found under very large flat stones in rubbly or even sandy areas. Direct evidence that these crabs crush shelled prey in the natural environment is still very scanty. While snorkeling with us in Pago Bay, Guam, on an August evening in 1975, W. Tobias observed a Carpih’us macuiatus on the reef-flat with a Cymatium muricinum Ridding in its master claw, but whether the shell contained a living snail or a hermit crab could not be determined. On overturning a large stone on a July afternoon in Pago Bay. a small Carpilius macularus was found and caught ; under the same stone was a freshly killed adult Mitra (.Strigatel/a) Iitterata (L.), whose spire had been neatly sliced from the body whorl. In the laboratory, the same crab and other Carpilius maculatus killed living Mitra iitterata in an identical fashion. M. Yamaguchi reports that when he found Daldorfia horrida under large
CRUSHINGBEHAVIOROFCRABS
157
slabs or rock at Cocos Island. Guam, he almost always found freshly broken shells in the immediate vicinity: these included species of Cones, Trochw. and Strombus, and all were damaged in ways identical to those inflicted by Dufdorjiu horridu in the laboratory. We have no direct evidence that Eriphiu sebunu feeds on hard-shelled prey. Such evidence is, however, available for two other species in the genus. Crane (1947) observed E. squumuta eating small gdstropods in tidepools as well as barnacles and in Panama, we have seen it scraping and crushing barnacles from intertidal rocks; the crab also readily eats barnacles in the laboratory. E. verrucosu in the Mediterranean is known to feed on gastropods and hermit crabs (Rossi & Parisi. 1973). Among species of Cuncer. C. productus is known to eat living snails and hermit crabs in the field (Vance, 1972: Spight. 1976; Bertness, 1977). There is similar direct evidence for some other large species in the genus. but not yet for the small C. oregonensis. Cuncer sp. are also known to prey on other hard-shelled animals. and it is unlikely that they or other massively-clawed crabs are speciaiized to deal with a moiluscan diet.
LABORATORY
STUDIES: TROPICAL CRABS
The tropical crabs dealt with here crush prey in their massive master (usually right) claw. Table I gives the critical sizes for various prey species for each of several individual crabs. Clearly, relatively large molluscs can be successfully crushed by adult crabs of the genera Curpifius. Eripiziu, and Dukforjiu in Guam. To emphasize this point further, we offered crabs certain large individuals of species that were generally too rare to permit accurate determinations of critical size. A 138 mm wide male Curpihs macufufus took the dorsal part of the body whorl off a 56 mm long adult Bursu bufiniu (Gmelin); the same crab split a Turbo setosus Gmelin measuring 58.6 mm in diameter and 3.3 mm in shell thickness; a 44.3 mm long, 1.8 mm thick Cyprueu urubicu (L.) was also shattered. Our 65.3 mm wide male Eriphiu sebunu easily crushed a hermit-containing 49.9 mm long and 1.2 mm thick Purpuru putdu (L.) shell from the north coast of Jamaica. A 32.6 mm long, 3.7 mm thick This melonis Duclos shell freshly collected at Panama City. Panama, and re-occupied with a hermit crab. had the venter, lip, and apex broken away by a 115.3 mm wide female Ctrrpilius mucirlutus. The critical size of a prey species is determined both by its own geometrical characteristics (shape and thickness of shell, hardness and structure of shell material) and by the behavior and morphology of the crabs. Since the Guamanian crabs studied are behaviorally and morphologically all similar to one another, it is convenient to deal with one species (Dufdor-u horridu) in detail, and to compare the other species with it. D. horridu differs from most other parthenopids in possessing a master claw with adaptations for crushing hard-shelled prey. Large, blunt molars are located
158
EDITH
ZIPSER
AND GEER;\T T\BLE
Critical
sizes (mm) for crushing of gastropod a shell is foreign. Predator
and prey
horridrr.
Crrithiwu
Lar,vest
Dtwpc~ ricimrs L. Cw~rltunrs ,/iuwvrc.s c’clslm rlrrhitrc~ll1l.s L. Troches
indicate
that
Largest offered __-
Largest knoa n
34.7 24.4 23.2 ‘1.3 24.0
34.7 24.4 26.0 21.3 83.7
27.6 30.6 30.7 30.0 31.3
3Y.O 45.2 46.0 20.5 32.7 25.4 27.6 31.9 37.0 33.8 40.7
I50 50 60 20.5 33.0 26.0 1X.0 50 s3.i J-1.0
27.6 30.6
31.3
27.6 31.3
28.0 I-1.0
26.3 23. I
26.6 24.3
26.6 21.5
33.0 26.0
31.0 28.4 24.0
2Y.5 24.6
33.0 29.5 24.6
33.0 33.0 ‘6.0
-N.-l 18.7
29.4
4s.4 29.4
50 33.0
37.8 28.9 33.5 33.1 26.0 29.6
38.2 26.6 34.0 34.6 38.1 30.0
38.’ 30.9 34.0 34.6 28.1 32.5
I50 33.0 34.0 83.7 44.0
39.0 57.9 56.1 27.6 33.0 40.6 1Y.8 29.8
40.6 85.5 54.6 _
49.0 57.9 58.5 37.6 33.0 43.8 31.0 37.2
150 100 70 28.0 33.0 83.7 44.0
x.7
23.9 Ii.2 J-1.3 1Y.2
: 4.4 lY.4
34.8 -15.2 -11.1 20.5 28.5 25.1 1’. 6 il.9 36.0 31.5 31.3
35.6
female 82.8 mm
niloricesL.
.Sfron~h~.s gihhrrulus
L.
nicoharinurr R6d. Colrrrr~hrllu mrrculorirr L.* Dwptr mowm Ridding D. ricimrs L. .Llorulc~ gramrltrrrr Duclos Thrtis mclotth Ducios’ I’rrsrrr~r rwhCfclhu L. Lwco:onirr Icuco:omrlis Lam.* C0rllr.s sp. D. horriclcr. male 91.5 mm Montlu grunrrlcrro Duclos Lucoxniu lcwco:oncrli.v Lam. * CupiliuT twcdr~trts. female 101 .-I mm Dwpcr morum Ridding D. ricimrs L. C. n~trcuk~~r~s,male 105.3 mm Cxpractr caprrtserprmis L. Drupcr morum Ridding D. ricimrs L. C. w~~lrrt~~s. female 105.4 mm Slromhus gihhrrrrhrs L. Drupa mown Rading C. w~culur~s. female I I I .3 mm Troches niloricus L. Drtrpu morum Rading Cunthnrus undosu.7 L. I/cl.,tu~ ~rrrbinellrrs L. Lrucozonia Irucozordi.~ Lam.* comes sp. C. n~~/rrrfr.s. female I 15.3 mm Troches niloricw L. Caiflriwn nochilos~un Sow. Bursa hu/bniu Gmelin Mow/a grantrlura Duclos Dwpa marum Ridding Iir.iwv rm+ine/hcs L. L~~~coxmiu kwco~onulis Lam. * Conur sp. Cj~tnofIwI
Smallest unritten
asterisks
female 69.6 mm
cohmw~~r Sow.
C~~prcrca it~oncfu L.
D. horritlrr.
I
prrq relative to individual crabs: x-occupied b> a hermit crab.
Ciltrn
Dalrlor~ia
J. VERMEIJ
46.0 2Y.0
_
‘8.3 43.8 29.1 30.8
CRWSHlNC
BEHAVIOR
OF CRABS
tj9
T-\BLE I ~~ootinued)
Largest
Smallest
Largest
38.2 58.6 Y-J.0 56.1
41.8 71.7 83.1 59.0
4s.’ 71.7 88.5 60.8
29.0
31.3
31.3
37.8 27.4 29.0 23.5 27.5 32.7 16.7 13.7
35.2 29.7 33.0 ‘7.4 29.3
19.7 31.7 16.7 17.0
17.0
__. ?’ 4 19.0 f-l. I 17.3 ‘5. I 26.9 lb.8 13.3
15.6 22.6 23.6 31.5 18.2 17.0 __. ” 8 16.1 24. I
‘J.8 71 3 __. is.0 17.6 I’.0 29.2 22.1 __. ‘3 6 34.0 21.0 20.2 20.5 18.0 24.4 Il.9 15.6
79.4 ‘2.6 ‘3.9 34.0 21.4 20.2 23.5 19.9 _?7 .-’ 13.3 21.4
$5.8 ‘7.9 ‘7.1 21.9 _.
25.8 _
30.3 27.9 30.0 75.5 20.0
‘7. I
28.
I
28.7
27.0
27.9
_‘7 .9
-
28.7 19.5 18.6 20.0
Largeit
160
EDITH
ZIPSER
ASD
TABLE Predator
and prey
E. sqrramura. male 38.0 mm Teguia pellisserpentis Wood Nerifafirniculara Menke Acanrhina hrevkienrara (Wood) Thrris melonis Duclos 7. rricmguluris Blainv. Cows
nu
GEERAT
I (continued)
Largest
Smallest
Largest
Largest
eaten
uneaten
offered
knoivn
1-2
18.8 II.4
18.8 22.X
44.2
11.6 19.5
32.9
25.5
19.0
25.7
35.0 50
16.4
” I _-.
25.0
25.0
15.9
15.9
25
‘4.5 30. I
26.4
26.4
30.1
30.1
30. I
17.7
18.5
22.9
25
29.0 31 1 __._
?O.I
18.9 16.4
16.4
25
AS.6
44.5
49.2
84.0
72.3
74.4
74.4
29.4
25.8
31.0
38.0
25.3
20.9
31.2
St.0
29.5
29.8
35.2
35.2
30.0 30.0
30.0
30.0
38.0
25.0
30.0
84.0
_
28.2
34.0
84.0
36.6
39.3
39.3
55
29.2
29.2
Broderip
E. squumaru. male 39.9 mm Trochus niloticus L.” Cerithium siercusmuscwum Val. Planuxis plunicoslurus Sow. E. sqrtumura. male 41 .O mm Cerifhium sfercusmuscarum Val. Acanrhina brevidentatu (Wood)
29.0
Conrrs IIKY Broderip
Cancer prochrcfus. male 122.9 mm Thuis Iamellosa Gmel.
J. VERMEIJ
24.0
I50
35.0
(smooth thick form) C. prothrcrus. male 123.7 mm
Ceratosroma foliarum Gmel.
100
C. oregorrensis. male 36.0 mm
Thais canalicrtlara Duclos T. lamcllosa Gmel. (smooth thick form)
Searlesiu tfira Reeve C. oregonensis. female 40.0 mm
Thak cunaliculura Duclos T. lamrllosa Gmelin (smooth thick form) C. oregonensis. female 49.5 mm
Thais Iumellosa Gmelin (smooth thick form) T. lamcllosa Gmelin (spiny thin form)
Amphissa cohtmbiana Dall
29.2
on the proximal apposing surfaces of both dactyl and fixed finger. i.e., where mechanical advantage of the pincer is greatest. The molar on the fixed finger extends nearly halfway to the tip of that finger. The chelipeds of D. horrida are elongated. and the four individuals observed in the laboratory tended to move them slowly. often one segment at a time. Rather then moving their chelipeds swiftly in the capture of prey, D. horrida most often made contact with snail and hermit-crab prey by lowering its body upon the prey. trapping it within a cage of abdomen and legs. A cheliped was often used to pick up a prey item from beneath the crab. Once in position, the prey is manipulated deftly by both chelae, as well as by the mouthparts and the first and/or second pairs of walking legs. Snails may be
Fig.
I
Ih?
FDI
1-H ZIPSCR
.\\D
GELRAT!
L EK1iFt.I
turned or rotated ;L few times. but \\ithin minute> the large &la ~$as IISLUIJ~ placed around part of the prey’s shell. XIost often. the master cla\\, is held in front of the crab. and the prey shell held by it is additionally supported From the opposite side by the small chela. from abo6.e by the mouthparts. ;lnd from belo\\- by the first t\\ o pairs of walking legs ( Fi g. 1). Periods of manipulation of the shell alternate R ith periods ofholding the shell in the large chela. If the prey proves difficult to break. the crab may spend more than Linhour in continuous effort, and may grip the prey in tht large claw for Ions periods of time. In order to estimate the amount of time spent in this position. a ‘hold’ \v;ts arbitrarily defined :IS ;I grip b>,the Inrpe chrla lasting longer than 5 sec. The duration of each hold in stxeral shell-breaking cpisodcs \cas dctermined (Table II). An 52.8 mm wide D. Iror~~itk~\~hile making a fatal hole in ;I ‘5 4 mm lone Dmp~/ ricimr.s (1.). used 20 holds Isstin,n L‘in average of 90 set each : 49”. -_. ofthe feeding episode of 37 10 SK was spent in holding the prey. The i.ery limited data of Table II suggest that iveakcr-shelled snails require less holding actitity, in both
340 90
0
I
0 15
28
0
3240
10
39
9
75
I
1910
I4
IO 77
56
13
;I rclati\,e and an absolute sense. Thus. the relatively weak shells of S~~onzh~s ,~~~~cIw/I~.F (L.) were broken after febver and shorter holds when compared ivith the tougher shells of Druptr ricitm. Less complete obser\xtions of the shell-breaking behavior of Duit/or/ic~ using other prey species support this conclusion. D. lwrrido gi\,es every impression of exerting considerable sustained pressure during most holding periods. Crabs quiver. rock back and forth. and occasionally lose their balance. A @rip is often accompanied by grinding or cracking noises. and is
CRUSHING
BEHAVIOR
163
OF CRABS
sometimes terminated by the prey shooting across the aquarium as if it had been released from the claw under pressure. Crabs may occasionally hold prey without discernible movenlent or apparent exertion. We have never seen D. ~r~~~~~ti{~ extract the soft parts of a prey snail without breaking the shell of the latter. Thus. even largeapertured species such as Neritl-r dbicillrr L. (whorl-expansion rate greater than 3.0) are inevitably shattered if the soft parts are to be eaten. If a prey shell. such as Mon~fa g~~m~/crtcr(Duclos) or Ceri;hitrtn cohtntrtrrSowerby, is small enou_eh to fit between the fingers of the master claw. the shell \silI be crushed through the middie rather than at one end. Small C. ~olrrn~rtr ( ~30 mm length) are typically broken in half. perpendicular to the axis of coiling. This is also the case with snails such as small T~~~*h~rs ni/otiul.y L.. Ctrnt/wu.s w~losu.s (L.). Stwtnbus mtrtctbilis Swainson. C’_rm~ti~m~t~icohrwicwn ( RGding). and Pwi.stmzirr ~z~fss~ttlfi~t Lam. whose spires are relatively tall and protruding (apical h~llf-~~n~le, ~45 ). In generai. the outer tip remains intact in such small or Lveak shells even though it could be broken easily. When large shells of these species are attacked. the shell wall is. however, too thick for the spire to be severed completely and the crab’s crushing efforts often result in lip fracture (see Table III). It is noteworthy that individ~~Is of thin or weak-lipped shells that are near the critical size for the attacking ~u~~~~~~~~~~ are never killed as :1 result of lip fracture: damage to the lip is not substantial enough to expose the soft parts. and a hole or gash must be made through the wall of the spire or body whorl if the crab is to get any nutritional benefit from its victim In unsuccessful attacks. the crab intlicts damage to the shell lip. ivhich must then be repaired.
Mode of predation Predator
on snails as a function of prey size. Size and fate of prey
and prey
28.0 mm. 32.0 mm: ape.x removed 32.9 mm: base removed 33.8 mm. 34.8 mm: anterior
periphery
35.1 mm, 35.6 mm. 42.0 mm: periphery
removed and inner lip chipped
20.3 mm (juv.): crushed 23. I mm
: apex
removed
21.1 mm: split perpendicular
to outer lip
24.3 mm: siphonal area damaged 24.5 mm. 25.4 mm: spines cropped on lip 26.3 mm 26.6 mm
: dorsum removed : spines cropped on
20.7 mm: crushed 19.0 mm: left side removed,
outer lip
lip chipped
14.0 mm: apex obliquely removed 24.6 mm. 25.4 mm: spines cropped on lip
164
EDITH
ZIPSER
AND
GEERAT
J. VERMEIJ
TABLE III tcontinued) Predator
and prey
D. morw,,
C. ntutitlnr~~. 105.4 mm Strombus gihbrrulrrs
C. mriculfztw. I 1I .3 mm Trochrrs niloticu.s
Size and fate of prey 21.6 mm: apex removed 28.2 mm: punctured 29.5 mm: unmolested 39.6 mm: apex removed 45.3 mm: apex and outer lip removed 48.4 mm: peeled 36.0 36.8 37.8 38.2
mm: apex and base removed mm : part of base removed: lip damage mm: small hole in base: lip damage mm: chips on periphery and outer lip
20. I mm: left side removed 2 I .2 mm: damage to siphonal canal 25.2 mm: spines sheared from outer lip C. mucu/uttcs.1IS.3 mm Trochus niloticus
Eriphictsebuttn. 43.6 mm .Verirtr ulbicilhr
Cerithium cohunntr
E. sehunu. 56. I mm .Veritu olbicillu Cl~peomor~u maria
E. sehana, 49.3 mm Cerithiwn colicmna
E. sebanu. 65.3 mm .Verita albicill(t
.V. plicato
37.5 37.7 39.6 40.6
mm: mm: mm: mm.
apex removed small holes in base and above periphery hole in base 40.9 mm. 47.2 mm. 49.0 mm: lip damage
23.6 mm: left side and posterior removed 23.0 mm, 23.6 mm. 23.9 mm. 21.3 mm: extracted 18.2 mm: lip and apex removed 21.0 mm, 21.1 mm. 21.4 mm: lip damaged 23.0 mm. 21.1 mm. 24.9 mm. 25.0 mm. 27.6 mm. 28.3 mm. 29.3 mm: apex removed 31.5 mm: outer lip removed 34.0 mm: intact 19.2 20. I 15.2 17.0 19.0
mm: mm. mm. mm. mm:
crushed 2 I. 1 mm. 22.3 mm: extracted 15.3 mm: crushed 17.8 mm: anterior of shell removed damage to outer lip
19.5 mm, 19.6 mm. 19.9 mm. 21.6 mm. 22.9 mm. 23.9 mm, 24.5 mm. 25.4 mm, 25.4 mm. 25.7 mm, 26.2 mm: apex and outer lip removed 26.2 mm, 26.9 mm: peeled 32.3 mm: lip damaged 19.8 mm, 20.8 mm. 22.8 mm. 22.9 mm. 25.0 mm, 25.6 mm. 27. I mm : crushed 28.7 mm: extracted 30.0 mm: not eaten 19.1 mm, 19.4 mm. 19.6 mm. 19.9 mm. 10.3 mm. 22.5 mm, 24.3 mm: crushed 23.5 mm: left side and venter removed 27.9 mm: left side removed
4Y.J mm. SO.11mm
: cruhcd
53.3 mm: ventral gab
7-U mm:
crushed
li4.0 mm. 252 3.8
mm: anterior
rrmo\-ed
mm: pwlcd
21.7 mm: crushed 27.8 mm: apx.x and anterior
removed
__. .i 0 mm, 3.2
rrtno~ed
mm: anterior
Such repairs are generally unnecessary for species w-hose outer lip is thickened or dentate within. Examples of genera possessing such lips in the adult stage are C_vtttutiutu. Bwxt. Dtwpn. 2tforul~r, Mitrnr (Srrigrrtdltr). and C~~ptwtr. In adult Crrirhirm, Lmthis. and Strombus, the outer lip is thickened and flaring. but not retinforced with teeth. Drup and certain species of i~lor~t~ft are among the sturdiest shells oftheirsize, possessing not only a heavily re-inforced outer lip but also a short. thickwalled spire which cannot easily be severed. Successful attacks by Ddriortict involve partial breakage of the body tvhorl dorsally or on the left side (Fig. 1). This brr:lk is effected by 3 slanted grip around the apex and the left shoulder of the bodl \t,horl. When such attacks fail. the only indication of an encounter \\.ith ;I crab is the cropping of a fe\v knobs or spines on the outer surface of the body ivhorl or outer lip: this damage is minor. and does not need repairing. The smooth slippery shells ofcowries (C_I~XYWU) are held with one finper of the cInt{ on the base of the shell (apertural side). and the other on the dorsum. The dorsum is always the first part of the shell to fail in adult couries; the base breaks onI\ in small animals. The shells of cones (Cotm) are very short-spired and esceedingly strong. >fost commonly. the anteroventral portion of the body whorl is broken away ; rarely can the heasily thickened spire be severed. Relatively small individuals are often split parallel
to the axis of coiling. Every successful and unsuccessful attack on C’ontts is accompnnied by injury to the thin outer lip. but in no case could the lip be broken back far enough to expose the soft parts sufficiently. Cq~ifi~~~ tmtcw/m~.s and its smaller but twy similar congener. C. cotwstt.~. both hate master cla!vs uith blunt proximal molars. The molar on the fixed finger is rounded and not elon,uated as in Drtkiwfi~t (C’ermeij. 1977). Individual Cayiii~s differ in the amount of xe;tr on the mofrux and some molars are tr’orn flat with use, The shell-bre~l~~~l~behavior of a C. ~~~~~~lf~~if~~.s faced with a tough prey shell,
CRUSHING
BEHAVIOR
OF CRABS
167
such as Druptr. C~~pruw or Conus. is similar to that described for Dtrldorfia. First contact with the prey is usually made with the legs and or the small chela rather than Lvith the abdomen. The positions assumed by the chelae. legs, and mouthparts during manipulation and holding of the prey are similar to those in D. hot-r-idrr. Again. shell breakage is primarily by crushing, and in\.olves attack by way of the aperture or outer lip only when spire-breaking is impossible. Two short experiments give some impression of how important predation by Cupilius may be to the prey gastropods that co-occur \jith this crab (Table IV). On 2nd June. 1975. all the gastropods in a I rn: quadrat near the hiding place of a 105.3 mm wide female C. ~I~I~U/~UKY were collected and offered to this crab in the laboratory as prey, By the fifth day. 9 of the 12 snails (73”,,) had been consumed. and 1 had received substantial shell injuries. On 7th June. this same crab \vas given another sample of snails from a 1 rn’ quadrat near its former hiding place. By 12th June. 8 of 15 prey had been consumed. As is evident from Table 111.snails not eaten by the crab in this second trial Lvere either above the critical size or were very small ( < 10 mm long).
Effect of predation
after 5 days by a 105.4 mm uide C~rpili~~ m~~c~~l~/!~ts female on gastropods of two 1 mz quadrats
Sample II. 8 of
I5 prey
in each
ne;~r hiding place in P.!go Bay. Guam.
eaten
Prey eaten. COUUS rhraeus: 22.5 mm C. spomtrli~ : 2I .4 mm Cerirhifon colwmc:: 17.1 mm. X.9 mm I’n.r~rtrt rurbinrllu.s: 21.7 mm. 27.0 mm Crrirhim sqjw~iwr: 13.7 mm Prey not eaten.
The attack behavior of Eriphicr species is similar to that of Carpilius and except that extraction of soft parts without damage to the shell is common in Eriphin. Eriphicr sebcuw in Guam was able to extract the soft parts of Nerirrr nlbicilh if the latter were large enough (Table III); Nerircr has a large aper.ture and a correspondingly very high expansion rate (W) of the ivhorls ( 8 > 3.0). In Panama. Dnldotficr,
168
EDITH
ZIPSER AND
GEERAT
1. VERMEIJ
Eriplh sqwmrra extracts This trimguhis
Blainville ( W, 2.6) when the shell of the latter reachesa size too large to becrushed or peeled. Probably in association with this extracting behavior. Eriphicr often attacks snails at the outer lip but. with smallapertured species such as Cerithium cohnmr, this method of attack is usually unsuccessful. As with the other genera of crushing crab described earlier, successful crushing usually involves severing the spire or making a gash or hole in the body whorl of the shell away from the outer lip. LABORATORY
STUDIES:
TEMPERATE
CA.VCER
Adult Ccrncer productus have relatively more slender and more mobile chelipeds than those of Carpilius. The chelae are small and subequal, and are lined with small teeth on the apposing surfaces of the fingers. First contact with the prey. at least in the laboratory, is most often made by a sweeping motion of both chelipeds: the chelipeds are extended laterally, then quickly sweep the prey toward the mouthparts by coming together medially in front of the crab. Legs may also contact the prey. When attacking relatively small prey. such as This crrrxrficuf~~rcr Duclos. crabs most often break the shell between the fingers of the larger chela. Relatively large prey, such as Cercrtosroma .fblicrtwn (Gmelin) and Fusitriton oregonensis ( Redfield). are frequently attacked using both chelae, and the flesh is most often exposed by attacks concentrated at the aperture. The prey is held on the bottom of the aquarium in front of the crab, with the aperture upward. In the trans-apertural grip. each chela grips a structure on the opposite side of the aperture: e.g., when the apex points toward the crab, the left chela grips the outer lip, and the right chela grips the columella and body whorl. The movable fingers (dactyls) are always above or dorsal to the fixed fingers; both dactyls are inside the aperture of the prey and point toward each other. The fixed fingers extend under the prey shell. The crab, while keeping both chelae on the aperture. is able to move its chelipeds from a position in which the propus segments are nearly vertical, with carpus segments or ‘elboivs’ above the carapace, to a position in which the propus segments are nearly horizontal. with ‘elbows’ out to either side of the crab. The crab moves the propus segments vertically together, and horizontally apart, the chela meanwhile pivoting around the shell structures and presumably pushing lip and body whorl alternately toward and away from each other. In two other methods of apertural attack (cis-apertural attacks), both chelae grip a single structure, namely, either the outer lip or the columella (with body whorl). One dactyl and one fixed finger are inside the aperture. In the cis-apertural grip, the chelae may act as a pair of scissors, applying a twisting or shearing force between them as the chelae try to rotate in opposite directions (Fig. 3). Ccuzcer productus changes the position of its claws so frequently during manipulation and breakage of shells that complete records of the sequence and duration of its movements could not be obtained. Few positions were held for as long as 5 sec. Exact comparison between the behavior of Cancer and tropical crabs is thus im-
possible.
.A large ( 137.4 mm u ide) malt C. ,PIV~IU~~~~I.S \v;lj = oivcn 12 small prey. vi:.. 6
Tluris Itrtm~liosc~ (Gmelin) ranging in shell length fwm 26.5 to 31. I mm. and 6 hermit crabs inhabiting T. /mwl/~~,st~shells of the same size range (36.3 35.5 mm). The crab killed the first t\\o prey (hermits)
by crushing
\+ith the larger chcla. a third
\v:Lj damaged by crushing the hodv ~\horl of its shell. followed attack, and a fourth prey was opened by a trans-apertur;~l consumed
kvithin 2 days. and no preference
hermit
by a trans-rqxrtural attack: all 12 were
for hermit crabs over snails MS elidcnt.
long
Tiuris umrlicdr~tn. The C~ttcer- crushed
the body cvhorl of the Thcri.7Lvith its larger
claw Lvithin 5 min. The same crab MXS immediately given a second. tougher shell. (T. /cn~~cNo.~r~. 3 1.3 mm long). After two vain attempts to crush the body whorl the crab used only cis- and trans-apertural attacks for the remainder of an unsuccessful 2-Lmin feeding attempt. The same crab successfully broke back the adult lip of a 60.0 mm ~(‘I.LIr~).).tOlllC[.fi)/iC/flllll: it tried approximately 1 grip \vith the larger chela on the apex. 4 trans-apertural attacks. and 9 cis-apertural attacks. the latter all on the lip. Three of the cis-apertural attacks on the lip were effective in breaking off pieces of shell large enough to be seen. If the attacks that resulted in significant shell breakape are extracted from the general record. it may be seen that. for Cntzcrr /JrdW~ll.S. attacks on the outer lip are most often successful in breaking difficult
prey. Siint shell brcakagc by four C. pi.Llcil/i iiu during eight feedins attempt5 maq- be chaxterized as follws: twice bq crushins u ith the large chela. eight times: by trans-:~perturaI attach. and 25 timcs bq cis-apertur;ii attack (c)t‘ \ihich 5 were directed to the col~~~n~li;~ and 20 to the outcr lip). .-I similar a:ulysis !;x D~~/d,wfi~~ lwwith in ths tropical Pacific ~vould shw that IIJIJ”,,ot‘ s~~ccessful she!l-breaking in swcn feedin: episodes is by crushin s \\ith the I:trzc ~~hcln. In Cut.pi/i~c.,. too. crushing 1~1th thtr large chela is the most successful method of breaking large pre”. Ctr~lcw 0rc~~o~vz.si.s is similar to C. ~~~oc/M~~~~s in general form. but is much 5mallcr and has larger cln~.s relative to its size (Vermsij. 1977). Our only x.isibly voracious individual. ;I large (49.5 mm tvide) female lvith a larger right chela. shoived a preference for trans-apertural attacks. In \\,orkin=u unsuccessfully for 51 min on ;i C‘d/iosto/luz Iigufwn Could 13.6 mm in diameter. most (37 of 41 ) of the recorded attacks Lvere on the aperture, \
Our data on shell-breaking by crabs confirm and amplify earlier \+.ork by Vermeij (1976. 1977) and other workers. \vho sho\\,ed that temperate crabs are less specialized for crushing hard-shelled prey than are certain massively-clawed tropical xanthids and parthenopids. All crabs. including temperate species of Ctu~wr. crush small prey in the master claw and .~l~~ctvpips. Curcims, and H~v7~&~1p.s1rs. sever the spire. Larger prey are generally attacked at the aperture (except in c‘mpili~~ and Dtr/h~/~~r), and are killed by successive peelins of the body ivhorl (Eblinp CYal.. 1964; IMuntz. Eblins & Kitching. 1965: Fears. 1970: Rossi Sr Parisi, 1973: Kitchinp &I Lockbvood. 1974). Removal of the soft parts from the aperture without injury to the shell has been described for .Llrrcl-q~iprs puhn. Cmci~~m C C.. Gibson. 1970: Rossi & Parisi, ~~~wILI.~. and Eripllitr ~‘tvv~~us~~ (Muntz 6’1(II.. 1)6_ 1973). Tropical crabs can take larger prey than temperate crabs of comparable size (Vermeij. 1976) and appear to use ‘one-handed’ crushing more commonly than theq use apertural extraction or lip fracture as methods of attack. Members of the
CRUSHING BEHAVlOROFCR.-1BS
171
tropical and subtropical genus Cduppct are highly specialized to peel the outer lip of snails in the fashion of a can-opener. so that a spiral gash which may extend as much as two whorls back from the outer lip (Shoup. 1968) is made. Warner& Jones (1976), among others. have pointed out that there is an apparently irreconcilable conflict in decapod crustaceans between agility and speed on the one hand, and sustained power on the other. Decapods have a range of muscle-fiber types, including rapidly contracting fibers with short endurance times, and slow fibers capable of more sustained contraction. We suspect that the claw-closer muscle in claws adapted for prolonged application of pressure contain a high proportion of slow fibers. This prediction is consistent with the findings of Warner & Jones (1976) who showed that the proportion of slow as compared with fast fibers is greater in the claws of Cctmwprtgrtnts and ,2/la~,-opi(,tt.spt1hc~ than in claws of the much more agile M. ~~~pi~~~tt~~ (L.). In the tropics, then, crabs have achieved a far greater adaptive range than they have on temperature shores. Tropical crabs range from extremely active portunids able to catch fish or other fast-moving prey (Schafer. 1954) to crabs whose motions are slow even at high temperatures, and which are specialized to crush slow, heavily skeletonized prey. This specialization toward crushing has been carried to an extreme in certain xanthids and parthenopids. whose movements are extremely slow and clumsy. Temperate crabs. on the other hand. are generally neither as powerful nor as agile as are many of their tropical counterparts. Predation by crushing appears to be a significant source of adult mortality among tropical gastropods (Vermeij, in press}. Our laboratory observations support the view that various morphological adaptations of the gastropod shell confer resistance to crushing by crabs and other predators. These traits include thick shells, a narrow or otherwise small aperture, a thickened outer lip, strong sculpture, and a short spire. Temperate snails show a lower frequency and lesser development ofthese features, and appearto be less well adapted and more susceptible to crushing. While crushing-resistant traits would be adaptive in temperate as well as in tropical snails, their reduced significance on colder shores may reflect compromises ivith other adaptations that demand conflicting morphology. Moreover, snails and crabs alike face physiological constraints on calcification imposed by periodically or abnormally low temperatures, and the adaptive options available to them may be limited (Vermeij. in press).
ACKNOWLEDGEMENTS
Drs L. Eldredge and M. Yamaguchi kindly provided us with space in their laboratories during our stays in Guam. We are also grateful to the staff of the Friday Harbor Laboratories and the Smithsonian Tropical Research Institute for providing space and facilities. Several colleagues helped in collecting the crabs.
172
EDITH ZIPSER AND GEERAT J. VERMEIJ
This work was funded in part by grants from the National Geographic Society and the Program of Biological Oceanography, National Science Foundation. Support in the form of a John Simon Guggenheim Memorial Foundation fellowship to G. J. Vermeij permitted us to spend much time in marine laboratories, and is gratefully acknowledged.
REFERENCES BERTNESS.M.D.. 1977. Behavioral and ecological aspects of shore-level size gradients in Thais kmrellosa and Thuis enrar~imrra. 0oiog.1,. Vol. 58. pp. 86-97. CRA?IE. J.. 1947. Eastern Pacific expeditions of the New York Zoological Society. XXXVIII. Intertidal brachygnathous crabs from the west coast of tropical America with special reference to ecology. Zoologica N. Y.. Vol. 32. pp. 69-95. EBLING, F. J., J.A. KITCHING. L. MUNTZ & C. M. TAYLOR. 1964. The ecology of Lough Ine. XIII. Experimental observations of the destruction of .Ll~ri/~~edalis and lVlrce/lcrIapilluv by crabs. J. Atlim. Ecol.. Vol. 33. pp. 73-83. FEARE. C. J.. 1970. A note on the methods employed by crabs in breaking shells of dopuhelks (Nucella lapillus). Ncrrrrmlisr. HaN. No. 913. pp. 67-68. G~ssos. J. S.. 1970. The function of the operculum of Thais lapilhrs (L.) in relation to desiccation and predation. J. A&n. Ecol. Vol. 39. pp. 159-168. KITCHING,J.A. & J. LOCKWOOD.1974. Observations on shell form and its ecological significance in thaisid gastropods of the genus Lepsiella in New Zealand. Mar. Biol.. Vol. 28. pp. I3 I-144. MUNTZ. L.. F. J. EBLING& J.A. KITCHING.1965. The ecology of Lough Ine. XIV. Predatory activity of large crabs. J. Anim. Em/.. Vol. 34. pp. 31.5-329. ROSSI. A.C. & V. PARISI, 1973. Experimental studies of predation by the crab Eriphitr vermcosa on both snail and hermit crab occupants of conspecific gastropod shells. BON. Zoo/.. T. 40. pp. 117-135. SCHAFER.W., 1954. Form und Funktion der brachyuren Schere. Abh. senkenb. natrrrjorsch. Ges., No. 489. 66 S.
SHOUP. J. B.. 1968. Shell opening by crabs of the genus Calappa. Science. N. Y.. Vol. 160. pp. 887-888. SPIGHT,T. M.. 1976. Colors and patterns of an intertidal snail, Thuis lame//osa. Res. Popal. Ecol.. Vol. 17. pp. 176-190. VANCE. R.R.. 1972. The role of shell adequacy in behavioral interactions involving hermit crabs. Ecology, Vol. 53, pp. 1074-1083. VERMEII,G. J.. 1976. Interoceanic differences in vulnerability of shelled prey to crab predation. Nufure. Lond.. Vol. 260, pp. 135-136. VERMEIJ.G.J., 1977. Patterns in crab claw size: the geography of crushing. S.wf. ZOO/.. Vol. 26. pp. 138-151. VERMEIJ.G. J.. in press. Biogeo,rwp/tJ, and adapra/ioa. Harvard University Press. Cambridge. Mass. WARNER.G. F. & A. R. JONES. 1976. Leverage and muscle type in crab chelae (Crustacea: Brachyura). J. Zool. Lond., Vol. 180. pp. 57-68.