filter feeding in the hermit crab pagurus bernhardus

7/28/2019 Filter feeding in the Hermit Crab Pagurus bernhardus

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International Association for Ecology

Filter Feeding in the Hermit Crab, Pagurus bernhardusAuthor(s): S. A. Gerlach, D. K. Ekstrm and P. B. EckardtReviewed work(s):Source: Oecologia, Vol. 24, No. 3 (1976), pp. 257-264Published by: Springer in cooperation with International Association for EcologyStable URL: http://www.jstor.org/stable/4215284 .

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Oecologia (Beri.) 24, 257-264 (1976) tJCCOlOgUl? by Springer-Verlag 1976

Filter Feeding in the Hermit Crab,Pagurus bernhardusS.A. Gerlach, D.K. Ekstrom, and P.B. EckardtMarine Biological Laboratory, Helsing0r, Denmark

Summary. The hermit crab, Pagurus bernhardus is able to remove both Arte-mia nauplii and unicellular algae from suspension. Crabs with wet weightsof 1.1-9.2 g consumed all of the 300 Artemia nauplii contained in 200 mlof sea water within 1 h. Crabs weighing 0.7-1.1 g wet weight filtered sus-pended Dunaliella algae (8 ???) from concentrations of 10-350 million cellsper liter at a rate of 26% and 47% within 2 and 5 h, respectively. A similarresult was obtained with an 11 g crab. During filter feeding activity a watercurrent is generated by the flagella of the exopods of the second and thirdmaxillipeds. Artemia nauplii are caught by grasping movements of the endo-pods of the third maxillipeds, whereas filtering of unicellular algae is probablyachieved by the two maxillae. It is assumed that filter feeding activity dependson the same structures and behavior as in deposit feeding. P. bernhardusis one more example of a benthic marine animal which may use any foodsource which becomes available in the course of the seasons.

IntroductionIt is well known that hermit crabs of the genus Pagurus are omnivorous. Evenif they are not in general particularly voracious, many species can seize smallbivalves, echinoderms, crustaceans and polychaetes, or morsels of animals orplant material, lift them with the chelipeds to the proximal part of the thirdmaxillipeds, and tear them between maxillipeds and mandibles. A second sourceof food, and probably the most important one, is the organic content of se-diments. The means of gathering the sediment varies from species to species.Most commonly this is accomplished by the minor left chela which tossesthe sediment to the endopods of the third maxillipeds. Sometimes this actionis preceded by a pushing of sand forward with the first and second pereiopods,and in other cases the endopods of the third maxillipeds directly sweep thesubstrate. The final transfer of particles to the smaller mouth parts is ac-complished by the endopods of the second maxillipeds. This pattern of behavior


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258 S.A. Gerlach et al.has been described in P. bernhardus (L.) by Jackson (1913) and by Orton (1925).Thorson (1966) reports that a 2.8 g hermit crab shoveled up 0.8 ml of sandper minute. A thorough study of this mode of feeding, and the role of thedifferent mouth parts involved in P. longicarpus and P. pollicaris was givenby Roberts (1968).There are some general remarks in the literature on filter feeding by hermitcrabs. Yonge (1949, p. 158): "in their feeding habits they show an interestingblend of the omnivorous scavenging of the true crabs and the filtering mecha-nisms of the allied porcelain crabs; they are thus capable of taking food fromthe bottom and from the surrounding waters". Brightwell (1951, p. 280), referringto the feeding of Pagurus bernhardus: feeding by "setting up a current, apparentlyby the breathing apparatus and the third maxillipeds, thus

"wafting

" fine particlesof food toward itself". G.E. and N. MacGinitie (1968, p. 297), referring generallyto hermit crabs: "some are able to feed by fanning detritus or plankton out ofthe water with their modified mouth parts". However, all detailed references tosuspension feeding by hermit crabs have been on such genera as Stratiotes andDiogenes which have long plumous setae on the second antennae, which theyuse to filter the water.

This is a report of preliminary observstions and experiments indicating thatin addition to being a carnivore and a deposit feeder, P. bernhardus can deriveconsiderable amounts of food by suspension feeding.

Methods

Hermit crabs were dredged from various parts of the Oresund and kept in a tank connectedto the laboratory sea water system. A salinity of 31%0 and a temperature of 9? C were heldconstant throughout the course of the experiments conducted in January 1976. The gastropodshells inhabited by hermit crabs were cleaned of epifauna prior to experiments. Larval stagesof the brine shrimp, Artemia salina, and cultures of the unicellular alga, Dunaliella marina, wereused as food. The algae originated from cultures in the exponential phase of growth, with concentra-tions ranging from 0.8 to 1.4 million cells per ml1. Before use the culture was centrifuged andthe cells resuspended in sea water. Cell concentrations were counted with an improved NeubauerHaemacytometer.The crabs did not get food for a period of 1-3 days prior to the experiments. During theexperiments, the animals were kept separately in 400 ml plastic bowls, containing 200 ml of seawater. A single, large animal was kept in a 1-1 glass jar filled with 500 ml sea water. A plasticnet, mounted about 10 mm above the bottom, prevented crabs from ingesting any particles whichmight have settled during the experiments. However, no such settling was observed. The waterin the experimental vessels was neither aerated nor stirred.After the experiments, the crabs were killed and their stomach and gut contents were analyzedmicroscopically. As killing in alcohol sometimes resulted in vomiting and loss of stomach contents(as well as being painful to the animals), the crabs were narcotized with solutions of MgS04or MgCl2, of which the latter proved to be the most effective.To observe the current flow, droplets of carmine suspension were placed at various positionsin the proximity of the anterior part of the animals. Great care was taken to ensure that thedroplets were stationary when released from the pipette, until caught by a current originatingfrom the crab.1 We want to thank Mrs. cand. mag. Grete Moller Christensen for cultures of Dunaliella marina


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Filter Feeding in the Hermit Crab, Pagurus bernhardus 259ResultsExperiments with Artemia nauplii (Table 1) demonstrate that Pagurus bernhardusvery effectively can filter over 300 nauplii from 200 ml sea water within 1 h,and over 400 nauplii within 2 h. Directly after feeding, the bristles of Artemiawere found in the stomach of the crabs. Fecal pellets collected 10 h after feedingalso contained such bristles.

Seventy to 100 Artemia nauplii correspond to 1 mg organic dry weight (Paf-fenh?fer, 1968); within 2 h about 5 mg food had been ingested, by animalsof about 300 mg dry weight. We conclude that P. bernhardus is capable of feedingon zooplankton. Artemia nauplii were caught by grasping movements of theendopods of the third maxillipeds which have long setae. Food particles arethen brushed off from the third maxillipeds by the endopods of the secondmaxillipeds, and are finally transported into the region of the smaller mouthappendages which move rhythmically.

Table 1. Filtering efficiency of Pagurus bernhardus when feedingon Artemia nauplii. Experiments were performed in 200 ml of seawater. Three hundred Artemia nauplii were offered at start, 150more added after 1 hWeight of crabg (wet)

Artemia leftfrom 300 after 1 h Artemia leftfrom 450 after 2 h1.151.281.469.24

2815450

Table 2. Filtering efficiency of Pagurus bernharduswhen feeding on suspensions of Dunaliella algaefor a period of 2 h (figures in brackets: 5 h). Experiments were performed with 200 ml of foodsuspension (except the last experiment: 500 ml)Weightof crabg (wet)

Concentration ofalgae suspension106cells/1

Cells filteredout106 cells

In % ofcells offered Algaefound after theend of the experiment

start 2 h (5 h) 2 h (5 h) 2 h (5 h) in stomach in midgut0.850.850.781.070.670.860.671.02

351100989838389.49.4

32160867425257.85.0

(52)6.28.02.44.92.52.60.30.9

(9.6) 39.812.224.933.334.417.046.0

(47.8) manyfewmanyfewplentymanyplentyplenty

plenty

manyplentynonenone

11.36 100 70? (54) 15.0 (23.0) 30.0 (40.0) densely packed densely packed


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260 S.A. Gerlach et al.

Experiments with Dunaliella algae (Table 2) give evidence that a reasonablylarge percentage of the suspended algae can be filtered out of the water within2 h. Filtering efficiency ranges from 9 to 46%, with a mean of 26%. Sincethe methods applied for counting algae were rather crude (single samples, nostirring prior to sampling), too much emphasis cannot be laid on these figures,which only serve to indicate that a significant decrease in the number of cellsin suspension did occur. This general tendency is clearly shown in Table 2,both in low concentrations of 10 million cells per liter, and in very high concentra-tions of 350 million cells per liter.Filter feeding is not restricted to small crabs : a specimen weighing 11 gcaused a 30% reduction of algae in 2 h. Measurements taken in 5-h experimentsshowed a continuous uptake of algae.

Large quantities of Dunaliella cells were found in the stomachs of all exper-imental crabs, except for some which vomited prior to dying. We have noproof that algae were digested in the diverticula of the gut. After 2 h of feedingonly one animal had large quantities of algae in the midgut ; however the midgutof crabs allowed to feed for 5 h was filled with both whole algae and fragmentsof algae. We do not know, again, to what extent food is utilized in the midgutof P. bernhardus; in this species the non-cuticularized midgut is rather longcompared with other Paguridae (Jackson, 1913). Roughly 18 million cells of

exopods of second and third maxillipeds

first antenna

respiratory currents

endopod of third maxilliped endopod of second maxillipedFig. 1. Schema of antennae and mouth parts in Pagurus [modified from Roberts (1968), Fig. 4:Pagurus longicarpus],and water currents observed during filter feeding activity


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Filter Feeding in the Hermit Crab, Pagurus bernhardus 261Dunaliella (diameter 8 ?p?) have a dry weight of 1 mg (Winter, 1969); onehermit crab of about 200 mg dry weight could take 0.14 mg food dry weightfrom a concentration of about 40 million cells per liter, and 0.02-0.05 mg foodfrom a concentration of about 10 million cells per liter, within 2 h. From thiscalculation it seems evident that filter feeding on phytoplankton does not providea large quantity of food per unit of time, but that algae might be consideredas an additional source of food.

During filter feeding activity, a nearly constant water current is providedby the flagella of the exopods of the second and third maxillipeds which normallybeat in unison. The flagella of the right and left side occasionally work togetherin short bursts of activity, but mostly those of one side are working. Thecurrent thus created comes directly from in front of the animal when flagella ofboth sides work together, and from the opposite laterofrontal area, when onlythose of the one side are working. In all cases a current of 1-2 cm/s flowsupward and slightly frontally away from the animal (Fig. 1).

Tests with carmine revealed that the incoming current apparently is composedof two layers. The upper layer curves upward in front of the animal and itseems that its main purpose is to bring chemical information to the first antennae ;they repeatedly dip into the current and then are brushed off by the endopodsof the third maxillipeds. The lower layer of the current curves upward directlybeneath the mouth area and passes across the setae of the third and secondmaxillipeds, thus reaching the direct proximity of the smaller mouth appendages.Large quantities of carmine particles, which have a size range similar to Dun-aliella algae, were found in both the stomach and gut of the crabs after theexperiments. It seems that P. bernhardus is not particularly selective while filterfeeding on smaller particles.

Normally the respiratory current enters between shell and crab on the leftside of the animal. The water is expelled from the gill chambers by the paddlelikemotion of the scaphognathites. The exhalant currents join the outward waterflow created by the action of the macilliped flagella.

DiscussionThe normal respiratory current of Pagurus is created by paddlelike movementsof the scaphognathites, appendages of the second maxillae. But there are atleast five more ways for a hermit crab to create water currents: 1) graspingmovements of the endopods of the third maxillipeds, 2) the beating of theflagella of the exopods of the second and third maxillipeds, 3) the beatingof the flagella of the first maxillipeds, 4) the beating of the left pleopods, and5) movements of the abdomen in the shell. Brock (1926) described the currentsmade by the flagella of the second and third maxillipeds as orientational, sincethey provide chemical stimuli for the first antennae.

However, the function of these water currents may be many-sided. Accordingto Roberts (1968) they expel indigestible material and fecal pellets out of rangeof the mouth parts, and from our experiments one might conclude that watercurrents generated by the flagella of the maxillipeds play a significant role


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262 S.A. Ger ach et al.

in filter feeding. However, we cannot exclude the possibility that P. bernhardusis capable of filter feeding by using more than one type of current. Possiblyeven the normal respiratory current may be filtered through the smaller mouthparts.Artemia nauplii are caught by grasping movements of the endopods of thethird maxillipeds ; it seems that this is the same kind of movement as that displayedwhen hermit crabs and other Anomura (Galathea, Lopholithodes) sort lightorganic particles out of suspended sediment.In Porcellana grasping, horizontal movements have been described as filterfeeding activity. In Pagurus the activity of the third maxillipeds cannot, however,explain the filtering efficiency with minute particles like Dunaliella algae, becausethe denticulate setae on the endopods of the third maxillipeds are rather coarse.

Like Eremita some hermit crabs {Diogenes brevirostris, Stratiotes setosus)have long plumous setae in two rows on the long second antennae. Usuallythese species feed from the sediment like other hermit crabs, but if food particlesare in suspension, the second antennae begin rapid to and fro movementsinterspersed with cleaning movements (cast-net feeding, Boltt, 1961 ; Greenwood,1972). However, the antennal filter mechanism is rather coarse, in Diogenesbrevirostris the plumous setae are 3 mm long and set 0.2 mm apart. Pagurushas only simple setae on the second antennae, and they are shorter than thewidth of the segments. Roberts (1968) therefore concludes that an auxiliarymode of feeding with the antennae is not possible in Pagurus.Zoea larvae ?? Pagurus longicarpus, reared in the laboratory, capture naupliiof Artemia as well as post-trochophores of Arenicola, using the maxillipedswhen encounters happen during normal swimming behavior. Plankton algaehave been found in the gut of these zoea larvae too, but details of ingestioncould not be observed (Roberts, 1974).

It is difficult to see what the smaller mouth parts really do during feedingactivity. Apparently the endites of the appendages make backward and forwardmovements in such a way that, as the second maxillae move forward, thefirst maxillipeds and the first maxillae move backward (Roberts, 1974). Coarsesand grains are brushed free from epigrowth with spines and setae on thecoxal and basal endites. Material to be discarded is moved forward until itis cast away by the flagella. In P. pollicaris long plumous setae form a bandon the coxal endites of the second maxillae, and in Pagurus longicarpus suchsetae are found on the first maxillae, too. These setae may serve to preventmaterial loosened from sand grains from escaping the buccal area (Roberts,1968). We think that suspension feeding on small particles like Dunaliella algaeis effected by a water current passing between first and second maxillae. Thiswould mean that one filtering mechanism is used 1) for sorting food particlesfrom sand grains, 2) for sorting food particles from suspended sediment, and3) for sorting food particles from suspension. However, further observationsare necessary to obtain a real understanding of the filter feeding apparatusof Pagurus bernhardus.From our experiments it is evident that a hermit crab in a few hours cancollect enough zooplankton to fill stomach and gut, provided the zooplankton


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Filter Feeding in the Hermit Crab, Pagurus bernhardus 263

concentration is high enough. The efficiency in retaining phytoplankton ispoorer, and from suspensions of algae which correspond to naturally occurringphytoplankton concentrations (9 and 38 million cells per liter) less than 0.15 mgfood (dry weight) was gained by crabs of 0.7-1 g wet weight, within 2 h. Organ-isms which exclusively depend on phytoplankton, like bivalves, have much higherefficiencies under similar laboratory conditions. A 1.5 g (wet weight) mussel,Modiolus modiolus, at 12? C and with a food concentration of 20 million Chlamy-domonas cells per liter, filters out nearly 10 million cells per hour, correspondingto about 0.8 mg dry weight. The large 11 g hermit crab of our experimentwhich, in 5 h, filtered algae of 1.2 mg dry weight out of the water (containing100 million cells per liter) might be compared with an 11 g Modiolus modioluswhich filtered about 3.5 mg algae in 1 h (Winter, 1969). Feeding on planktonalgae seems to be only of minor importance for P. bernhardus, but it mightbe important when other food is scarce, or when phytoplankton is very dense.

However, it is still an open question how valuable the contribution is thatmight come from phytoplankton. Zoea larvae of P. longicarpus could be rearedon a diet of Artemia or zooplankton, but a diet of algae w^s not sufficientfor complete development, although there was evidence of longer survival com-pared with starved animals (Roberts, 1974). There are more decapod crustaceanswith filter feeding capacities. Jatzke (1970) reports on a 6-month-old lobster(Homarus gammarus) which lived under in situ conditions, but without accessto larger food items. During 17 months it grew like other lobsters which werefed in the laboratory.The hermit crab, P. bernhardus, provides one more example of a benthicanimal's ability to rely on more than one feeding type, so that it may useoptimally any food source becoming available to it in the course of the seasons.

References

Boltt, R.E. : Antennary feeding of the hermit crab Diogenes brevirostris Stimpson. Nature (Lond.)192, 1099-1100(1961)Brightwell, L.R.: Some experiments with the common hermit crab (Eupagurus bernhardusLinn.),and transparent univalve shells. Proc. zool. Soc. Lond. 121, 279-283 (1951)Brock, F.: Das Verhalten des Einsiedlerkrebses Pagurus arrosor Herbst w?hrend der Suche undAufnahme der Nahrung. Z. Morph. ?kol. Tiere 6, 415-552 (1926)Greenwood, J.G. : The mouth parts and feeding behaviour of two species of hermit crabs. J.nat. Hist. 6, 325-337 (1972)Jackson, H.G.: Eupagurus. Proc. Trans. Lpool biol. Soc. 27, 495-573 (1913); and in: L.M.B.C.Memoirs on British Marine Plants and Animals (W.A. Herdman, ed.), Vol. 21, pp. 1-79. Lon-don: Liverpool Marine Biological Committee 1913Jatzke, P. : The Trichterkreisel, an in situ device for cultivating marine animals in tidal currents.Helgol?nder wiss. Meeresunters. 20, 685-690 (1970)

MacGinitie, G.E.: Natural history of marine animals, 2nd ed., pp. 1-523. New York: McGraw Hill1968Orton, J.H. : On the mode of feeding of the hermit crab, Eupagurus bernhardus,and some otherDecapoda. J. mar. biol. Ass. UK 14, 909-921 (1927)Paffenh?fer, G.-A. : Nahrungsaufnahme, Stoffumsatz und Energiehaushalt des marinen Hydroidpo-lypen Clava multicornis.Helgol?nder wiss. Meeresunters. 18, 1-44 (1968)


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Roberts, M.H. : Functional morphology of mouth parts of the hermit crabs, Pagurus longicarpusand Pagurus pollicaris. Chesapeake Sc. 9, 9-20 (1968)Roberts, M.H. : Larval development of Pagurus longicarpus Say reared in the laboratory V. Effectof diet on survival and molting. Biol. Bull. mar. biol. Lab., Woods Hole 146, 67-77 (1974)Thorson, G. : Some factors influencing the recruitment and establishment of marine benthic com-munities. Neth. J. Sea Res. 3, 267-293 (1966)Winter, J.E. : ?ber den Einflu? der Nahrungskonzentration und anderer Faktoren auf Filtrierleistungund Nahrungsausnutzung der Muscheln ?rctica isl?ndica and Modiolus modiolus. Mar. Biol.4, 87-135 (1969)Yonge, CM.: The sea shore, pp. 1-311. London: Collins 1949

Received March 7, 1976

filter feeding in the hermit crab pagurus bernhardus

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