energy maximization and foraging strategies in potamon

Freshwater Biology (1989) 22, 2.^3-245

Energy maximization and foraging strategies inPotamon fluviatile (Decapoda, Brachyiira)

FRANCESCA GHERARDI. FEDERICA TARDUCCI andFIORENZA MICHELI Department of Animal Biology atid Getietics.University of Florence, Italy

SUMMARY. I. Foraging of the freshwater crab Potamon fluviatile wasstudied by recording the aclivity of seventy-eight specimens in •^5^^ m-poolin a Tuscan stream during early summer. Foraging was related both to theorganic content of the substrate and to the crabs' oxygen consumption.During this period, adult females underwent "second vitellogenesis*. withabundant deposition ot yolk in oocylcs.

2. A dispotic distribution (not accompanied by agonistic interactions.,but 'peacefully' based on size) was observed within the foraging area.Larger animals (mostly males) fed on the rare patches of vegetable debris,which presented the highest organic content. Conversely, smaller speci-mens were relegated lo the poorer substrates, such as the stream banks.

3. The females extended and diversified their foraging areas by aisoventuring into terrestrial habitats, in contrast to the more sedentary andaquatic males. This behaviour (which was not accompanied by a differentenergetic output) resulted in a more proteinaceous diet (even when theN-content of vegetable debris fell drastically), and in a significant increasein fats and lhe hepatopancreas index.

4. The reserves of energetic substances are presumed to sustain thehighly expensive vitellogenesis, with the production of macrolecithal eggs.The females' behaviour as "energy maximizers' seemed to be under astrong selective pressure, since their reproductive success is directlyrelated to the efficient harvesting of food.

Introduction

Decapods dominate the macro invertebrate bio-mass of many streams. Because of their utiliza-tion of energy from diversified trophic levels,they play a primary role in the structure of aqua-tic communities and significantly contribute to

('(lrrcspondcncc: Dr FnincL'sc;i Ghcrartii, Ooparl-mont of Animal Biokigy iind (ii:ncUL-s. University (ifFlorence, V. Romana 17. 50125 Florence. Itulv.

materiiil cycling and energy flow. With theexception of crayfishes, where an extensive liter-ature exists (reviewed by Moniot, 19K4). only afew. scattered records report the feeding habitsof other freshwater decapods (in prawns,Ruello, 1973: Marte. 1980; in crabs. Williams,19f)l. i%2; Kabish. 1968; Schneider. 1971;Gherardl. Ciuidi & Vannini, 1987).

Poiunum fltiviaiik' lierbst is a commonbrachyuran living In many hill streams in south-

233

234 F. Gherardi, F. Tiirducci and F. Micheli

em and central Italy. In its feeding habits, thisspecies shows a great plasticity, extending itsforagingarea to the terrestrial habitat (Gherardi&. Vannini. 198y). It behnves like a generalist,and exploits food items most available at thetime (Gherardi, 1987). In water, the erabs for-age freely on the substratum, feeding on vege-table debris, scraping on algal-cove red surfaces.or actively preying on frogs, tadpoles and vari-ous invertebrates {Gherardi cial.. 1987). Exceptin colder months, when the animals are mostlydiurnal, foraging is concentrated during thenight (Gherardi et al.. I HSa. b).

The objective of the present study was toexamine the foraging activity of this species inthe field, and to relate it to (i) the quality of thesubstrate, (ii) the crabs' metabolism, and (iii)organic content of the hepatopanereas. gonadsand stomach. Effects of size. sex. reproductivephase, population density, and neighbours arealso investigated.

Materials and Methods

The study animalAmphibious habit, burrow occupation and

high vagility are peculiar aspects of this species'behavioural ecology (Gherardi ct at., 1987,1988b). Reproductive patterns follow an annualcycle at least in the adult females (>35 mmcarapace length). Oocytes begin to grow in thegonads in November-March (first vitello-genesis' according to Adiyodi. 1985; phase 1),while the more energetically expensive "secondvitellogenesis" (characterized by the abundantdeposition uf yolk in the oocytes; phase 2) occursin April-mid July, followed by ovulation. In thepost-ovulatory phase (mid July-October: phase3). eggs (whieh are macrolecithal) are incubatedfor about 40 days inside the chamber limited bythe sternum and abdomen. Embryonic develop-ment is direct, and hatchlings remain under thefemale abdomen for at least 10 days before

kr-z-l MUDciy BANKSROCKY BANKSVEGETABLE DEBRISFINE SEDIMENTSCOARSE SEDIMENTS

FIG. 1. Map of thf pool under study (upper) and its section (lower) along the X-Y axis. Types and distribution ofsubstrates arc represented.

Foraging strategies in freshwater crabs 235

dispersing along the stream. At least in adults,ecdysis occurs only once a year in September.Copulations were observed in the field fromJune to October, when male spermatogenesiswas aiso more active (Delpino, 1934) (phase 2 ofthe males" reproductive cycle).

Methods in the field

The study area was a 50 m' pool on a hillstream near Florence. Italy (Fig. 1). Observa-tions were made in eleven sessions of 1.5 h each.beginning at 21.00 hours during the period 3June to 11 July 1986. The pool was illuminatedby a dim incandescent light, which did not alterthe crabs' behaviour. Two observers on oppositesides of the stream, at about 5 m above waterlevel (where they could not be seen by the ani-mals), recorded the positions of the crabs every2 min with respect to a grid system, theirbehaviour, and the type of substratum theyoccupied. We observed forty males, twenty-fivefemales, and thirteen others which could not besexed, Fig. 2 shows the frequency distribution ofsize. Only in a few cases was the same crabfollowed for more than one session. The number

SIZE29 33 37 41 45 49

I—I—LJ—I I I I I mm10

5-

OzUJ

OUi

0-1

5 -

= 40

99"=25

IT

FIG. 2. Size (ciirapiicc length) distribuiions of males(upper) and females (lower) which were t)hserved dur-ing their foraging aelivity in June-July.

of specimens simultaneously present in the poolranged from three to nine individuals. At theend of each session, any animals which had notpreviously been marked were caught when pos-sible, their sex and size recorded, marked with awater-proof paint, and then released.

Behaviour was classified as: immobile, walk-ing, searching for food (when the animals, eitherstill or on the move, scraped the substratum withone or both of their chelipeds), feeding (whenthey brought their chelipeds with pieces of foodto their buccal cavity) and aggression. Aggres-sive interactions were defined as avoidance,threat, strike, and fight (Bovbjerg, 1953).Avoidance occurred when one ofthe two oppo-nents simply avoided the other by changing itsdirection of movement. Threat consisted ofagonistic posturing, such as raising one or bothchelae. Strikes involved only brief encounters(<2 s). while fights involved longer interactions,with highly aggressive patterns (pushes, graspsand strikes) (Vannini &Sardini. 1971). We con-sidered the winner as the opponent which didnot flee at the end of a contest.

Methods in the laboratory

Among the various substrates, we were ableto distinguish muddy banks, rocky banks, coarsesediments (particles larger than 16 mm), finesediments (comprising silt and clay), and vege-table debris.

For the analysis of organic content of the sub-strates, surface soil 2-3 mm deep was sucked upwith a pump (three samples for each substrateevery 2 months). For the rocky banks, epilithicalgae and mosses were taken. Samples weredried at llOX'. and triturated in a mortar.Organic carbon was estimated by the Walkley &Black's (1934) method and then determinedby tri tro processor. For nitrogen content,Kjeldahl's (1883) method was used.

Oxygen consumption was evaluated with anOxygen Meter YSI mod. 57 fitted with polar-ographic electrodes mod. 5700 (for furtherdetails, see Gherardi et ai. 1988a). Animalswere collected from the stream under study inJune-July, and kept unfed for a few days in thelaboratory at room temperature (18-2(rC)before testing. Hourly consumption per animal(at 2O''C) was considered the average resultingfrom a 3-h-long experiment.

Over an annual cycle, approximately fifty

236 F. Gherardi, F. Tarducci and F. Micheli

adult animals were killed for gravimetric andchemical analyses. All specimens were frozen oncapture and brought to the laboratory on dry ice.The hepatopancreas atid female gonads wereremoved and weighed with an analytical balanceto give, respectively, the hepatopancreas (HPI).and gonadic (GI) index (i.e. the ratio betweenthe fresh weight of the organ and the freshweight of the crab per cent). Their organic con-centrations were evaluated through the methodsdescribed by Heath & Barnes (1970) for lipids.and Keppk'r & Decker (1984) forgiycogen. Thepercentage of nitrogen in the stomachs (onlyspecimens with full stomachs were used) wasdetermined by Kjetdhal's method.

Results

Substrates

Table I gives the organiccontent of the streamsubstrates over an annual cycle. These differedin their richness of both carbon (after arcsinsquare transformation, ANOVA: F=27.49,df-4 and 79. /'<O.UU1). and nitrogen(ANOVA: F= 16.26, df=4 and 79. P<U.U()l).Vegetable debris were obviously the richest sub-strate in organic carbon. Nitrogen was also moreabundant in detritus, but it changed drasticallyover the year, reaching a minimutn in June.

BehuvinwFig. 3 shows the time spent on each substrate bymales and females during their foraging activity.The two sexes differed in their choice of sub-strate, the females more often preferritig sandand stones, and spending less time on vegetable

n =40(1328)

9 9 n=25(899)

3 0 ^

0 J 1MB RB VD FS CS

FIG. 7>. Frequency distrihution of ihc time spent oneach substratum by the f'oriiging cr;ibs (in p;ironthesesthe numher of records), compared belween sexes,. Forabbreviations, see Table 1.

TABLE 1. Organic content (dry weight) of substrates (averaged from three samples). MB^muddy banks;RB = rocky banks: VD = vegetahle debris: FS-fine sediments: CS^coiirsc sediments: M = mosses.

A. Carbon {eg g ' )FebruaryAprilM^AugustOctoberDecember

Yearly average (±SE)W

B. Nitrogen (mg g"')FebruaryApriiJuneAugustOctoberDecember

Yearly average { + SE)n

MB

2.4-_---2.42

2.0-----2.O±().83

RB

4.64.02.13.32.67.1.3.9±2.3

17

3.44.82.11.82.02.32.8+1.3

IS

VD

15.412.328.329.2-

22.72l.S±13.115

5.05.92.19.55.77.05.'}±3.7

IS

FS

0.70.30.82.50.5

11.32.3+3.6

18

1.31.51.71.21.31.5L5±0.3

13

CS

s.i3.82.12.30.32.82.7+2.3

18

2.71.1l.f)0.91.41.3l.5±l.ll

17

M

13.88.1

12..';U.36.0

22.312.4±7.8la

8.85.71.35.84.38.75.4+3.2

18


debris and banks than males (;t;-=y9.771, df^4,P<O.()()I). Males especially spent relativelymore of their time on vegetable debris which,although scarce in the pool, was the richest sub-strate in organic content. In males, size waspositively correlated with the time spent onvegetable debris (after semi-logarithmic trans-formation: r=().332, df-37. P<().()25). andnegatively with that spent on the banks(r=0.439'. df^37. /»<().U()5).

The occurrence of behavioural patterns (Fig.4) differed significantly between sexes, femalessearching for food more often than males(r-15.417. df^4. P<0.01). A positive correla-tion between size and percentage of time spentin searching for food and feeding was discoveredonly in the females (r=().37, df=23. /'<0.(}5).while Immobility was negatively correlated withsize (r=-().463.'df-23. P<0.01).

Aggression was a rare behaviour, in spite ofthe fact that the density of the crabs could often

%

0-1

n = 40(i328)

D 9 9 n = 25(900l

wFIG, 4, Frequency distrilmtion ol Iht behaviour p;ii-terns pcrl'urmcd hy ihe foraging crabs (in parenthesesthe numher of records), compared hetween sexes. Forabhreviaiions. see Tahle 2.

be high, and the areas inspected by differentanimals were often superimposed. Only eigh-teen interactions were observed, and they weremostly of low aggressive value (56% of threatand 28'/f of avoidance v. 16% of sttikes andfights). Males and females won equally, while in67% of the interactions the winner was the largercrab. Animals reacted aggressively when the twoopponents were at an average distance of28.7 cm (SE^4.1 em; minimum 5 cm. maxi-mum 70 cm).

Table 2 shows the frequency of behaviour pat-terns on the different substrates. Consideringthe overall time an animal spent on eaeh sub-stratum, aggression occurred more often whenat least one animal was grazing on vegetabledebris {comparing the frequency distribution ofaggression on two categories of substrates, veg-etable debris and others, with the same distribu-tioti of non-agressive patterns: /^=4.266. df= 1,/*<().05). The occurrence of searching for foodand feeding in animals moving on detritus alsodiffered significantly from its frequency on othersubstrates ('/:=312.\1?>. df-1 . /'<U.aOl).

Locomotory speed und size of the foraging areaThe frequency distribution of locomotory

speed every 2 min is shown in Fig. 5. Femaleswere significantly faster than males while forag-ing in the pool (r=27.4. df=8. /'<0.00]). Itifemales, the distance covered after 1 h waspositively correlated with size (r=0.575, df= 15,P<0.01). Movement was randomly oriented,being the directions followed uniformly dis-tributed in the plane (Rayleigh test. Batschelet,1981: males: 2=1.099, «=377. ns: females:2—2.064, /i=224, ns), with no difference

TABLE 2. Time budget (in %) on each substrate while foraging. In parentheses the percentage of one behaviourpattern wiih respect to ils frequency on the olher substrates. The total hchavioural patterns and occupiedsubstrates arc indicated, respectively, at the final column and row. I = immolr'ile; M=^moving; A = aggrcssion:S = scarchmg for food: F=fceding. For the other abbreviations, sec Table 1-

1MASFOccupiedsubstrates

MB88.610.20.00.8(1.4

236

(lfi.2)(10.5)(0,0)(0.7)(0.1)

RB47,011.53.n6.5

32.0200

(7.3)(10.0)(i3.y)(4.8)(y.i)

VD20,6.2.

13.57.

f.32

407

1

(10.0)(16.6)(39.5)(31,9)(51.3)

FS67Ul

17

13H85

.72

.4

.6

.2

(46.(39.(27.(24.(16.

3)3)9)5)6)

CS44.49.21.4

17.727.4

588

(2(1.2)(23.A)(18.6)(.38.1)(22,9)

Behaviourpatterns

129222943

273704


%30

0

=401377)

=25(2441

5 15 25 35 45 55 65 75 >B0cm / m i n

FIG, 5. Frequency distribution of locomotory speed recorded every 2 min (in parentheses the number of records),compared between sexes.

between sexes (;f=13.467. df=17. ns). Con-sidering the mean vector length r' as a straight-tiess index (Batschelet. 1981), both sexesfollowed a path with pronounced detours and

m1.2

deviations (in males. average=n.26. n=18; infemales. average=0.22, «= 10; males v. females;Mann-Whitney t/test: t/=81. ns).

The area occupied by crabs while foraging

0.8

0.4

30 60 90 minFIG. 6. Incrt-asc of the foraging area with time (mean values ±SE). For the method of computation of the area, seethe text.

Foraging strategies in freshwater crubs 239

increased with time (Fig. 6). This is calculatedhere as the sum of the 1 dm' quadrats in whichthe animal was seen every 2 min. plus the sum ofminimum number of quadrats the animal wouldhave had to traverse in order to reach disjunctquadrats (grid cell methods: Siniff & Tester.1965). Area grew faster In females (in males:/)=n.766: in females: /?= 1.209; males r. females:t=b.695. df-2197. P<U.()()1). In addition, thesize of the area traversed in 1 h was positivelycorrelated with size only in the females(r=0.494.df=18. P<0.025).

FIG, 7. Areas occupied during one hour by nine speci-mens which were foraging in the pool during one ses-sion of observation. Letters indicate locations of stopsfor feeding. For each iinimii!. sex and size (carapacelength in mm. in parentheses) arc also shown.

No correlation was discovered between areaand density of foragers (r=0.122, df—47, ns),while the extent of superimposition of the areaoccupied by the crabs simultaneously present inthe pool increased as the number of crabsincreased (/•=0.259. df=166. P<0.005).

Relationships between contiguous animals(Fig, 7) were studied in terms of the extent ofsuperimposed areas, comparing the couples ofthe same or of different sexes with respect toincreasing densities: no difference was foundbetween these two categories (ANOVA:F=-3.7. df= 152 and I. ns), while a significantdifference in the degree of superimpositionresulted from different densities (F=5.19, df=4and 152, /*<().01), and replications (F=3.17,df=9and 152, P<0.01).

The same aspect was analysed in couples ofequal and different size, discriminating 'small'(<42 mm carapace length), and 'large'{^42 mm carapace length), and thus con-sidering the three possible combinations (small-small, large-large and small-large). No dif-ference was found among size classes (ANOVA:F--0.37. df-153 and 2. ns). while the densityof foragers did influence the extent of superim-position (F-3.76, df-4 and 153, F<0.01).

Oxygen consumptionA positive correlation between size and

hourly oxygen consumption existed for both

m g

Zgt -Q.

COzoo

^-\

15-

10-

-

5 -

20 30 40SIZE

50 mm

FIG. H. Oxygen consumption plotted against size(carapace length) for male and female crabs tested inJune-July. All measurements were made at lO'C.

24(1 F. Gherardi, F. Tarducci and F. Micheli

TABLE 3, Relative size and organic content (dr>' weight) o( gonads (G). hepatopancreas (HP), and stomachs(average ±SE). compared (by /-test, after arcsin square transformation) among reproductive phases (see thetext) (•P<(l.()5, "P<0.01).

A. Females

GKgg-'xIO^)nG lipids (g a ')M

MPKgg 1x10=)/I

HL lipids (g g •)n

H P glycogen ( m g g i )n

Stomach nitrogen (egg ')n

B. Males

GKgg-'xlOi)nlIPKsg 'xUP)nHP lipids (gg-')nHPgtyeogen(mgg-')nStomaeh nitrogen (eg g ')n

Phase 10.82+0.15

11O.I2±O.OI83.56±0.34

10O.()6±().ni

10I.I7±1UI78.72+0.96

15

Phase 12.yi±O.31

16.v?n±{)..i2

120,1010.01

120.K9±()..14

in!().7O±l.fi58

Phase 21.05 ±0.18

140.18+0.0185.5O±O.5O

11().13±(l.().'

141.38+0.449

12.12+1.19S

Phase 23.13±0.19

183.(>8±0.22

19O.L1±0.03

120.7810.2788.431(1.t«)

11

Phase 30.43±0.06

120.0710.0153.42+0.27

13n.O.SlO.D!(1

0.4610.17

10.6513.125

1 V.2

0.83

0.70

0.34

O.((9

(1.72

1 r. :

0.43

1.86

3.36"

6,((4**

0.2i

2.19*

1 V. 3

1.36'*

1.59

0.25

0.47

1.43

0.47

2 I'. 32.59"

4.59**

3,11* •

2.64*

1.26

0.88

sexes (males: y=03Xx-4.99, /•=0.546. df=14,P<0.025: females: y=0.43.t-7.95. r=0.795,df= 14. P<(1.0()5) (Fig. 8). The regression coeffi-cietit does not differ sigtiificanlly betweeti sexes(/=(). 145, df=3n. ns). i.e. a male and female ofthe same size consumed oxygen to the sameextent, thus having the satiie aerobic energydemands.

Analyses of gonads, hepatopancreas, andstomach content

Table 3 summatizes the results obtained fromthe analysis of gonad. hepatopanereas and stom-ach content in ihe different reproductive phases.In the females. GI is significantly hipher duringApril-mid .luly when histulogical analysis alsorevealed the occurrence of the secondvitellogenesis. which is accompanied by a con-

sistent deposition of fats in the gonads. Duringthis phase. HPI (Fig. 9) and the lipid content ofhepatopancreas (Fig. 10) were also higher, whileglycogen (Fig. 11) did not change significantly.Conversely, in males all these measurementswere constant throughout the year. Fat concen-tration is significantly correlated with HPI inboth males (r=().434. /)=().0(15. df=20,P<{i.ii5). and females (r=O.47y. / J=0 . ( )08 .df=24. P<().()2), suggesting that the incrementin the relative size of this organ depends largelyon the deptisititm of fats.

ANOVA test (after arcsin <;quare transforma-tion) was used to compare HPI. and hepato-pancreas content of fats and glycogen betweensexes and at different periods. Although being inoverall equal in both scxcMHPI: 1=2.43. df=]and 59. ns; fats: F=0.12, df=i and 4S. ns). atleast fats were not constant throughout the year


7.5

5.5-

3.5-

1.5-"

SECONDVITELLOGENESIS

BEGINSOVULATION

BEGINS

• \ 99

I . IN ' D ' J ' F ' M ' A ' M ' J ' J ' A ' S ' 0I c I

PHASE1

PHASE2

1 PHASE3

INTENSESPERMATOGENESIS

7.5n

5.5-

3.5

1.5-1! •

I Z, 1 i^ TN ' 0^ PHASE

1

A ' S ' OPHASE2

FKl.'). I k'p:iiopancreas index during a yearly cycle in thiny-fnut females (upper) and ihirty-onc males (lower).

(F=4.66. df=2 and48. /'<().1)5; on Ihc amtrary:HPI: F=2.(i7. df=2 and 54. ns). hul it was sig-nificantly hiyhcr in the phase 2 in females(F=(i.l)7.df=2and48. P<O.U1). The interaciionbetween sexes and periods was also significantfornPi(F=S.24.df=2and5y. /*<0. l l l ) .OnihcLontrary. no significant diffcicEice wns reveitk'dfor giycogen content between sexes (F=ll,62.df=I and 33. ns). in reproductive phases(F=0.22. df=2 and 33. ns). and in the interac-tion between these latter two factors (F=l . I6 .df=2and 33. ns).

During the second vitellogenesis. females alsohad a more protein-rich diet than males duringthe same period (after arcsin square transforma-tion: /=2.3, /'<().05). aithouph ihe N-ointent ufthe stomachs did not difter over the whole

annual cycle between sexes (ANOVA afterarcsin square transformation: F=(I,1S. df=41and 1. ns), neither did it change in the wholept)pulation throughout the year (F=0.53, df=41and 2. ns).

Discussion

Plant debris, broken down into more or lessamorphous detritus, mixed witb small mineralparticles and diatom frustules. is one of the mainsourees of energy for many members of thestream community. It constitutes the principalfoodstuff of a wide range of invertebrates,includini; most orders of insects, most nf thesmaller Mulatostrata, most oligochaetes, and


0.3-

~ 0.2H

- 0.1 iinqa.

—r

SECONDVITELLOGENESIS

BEGINS

tOVULATION

BEGINS

. 1 99

—I 1 1D J F M

PHASE1

1 1A M J

PHASE2

1 1 - T 1A S OPHASE

3INTENSE

SPERMATOGENESIS0.3-1

.'H 0.2 ^

cfcf

I 1 ' [ I 1 I I I ' IN D G F M A M J J A S O

P H A S E1

PHASE2

FIG. 10. Lipid content of hepatopancreas during a yearly cycle in thirty females (upper) and twenty-four males(lower).

some molluscs (see, e.g.. Chapman & Demory,1963; Hynes. 1963; Jones. 1950). For a foodgeneralist iike P. fluviatile. heaps of vegetabledebris patchily distributed along the stream are arich deposit of organic substances, which aremore frequL-ntly explored than other substratesduring its aquatic foraging, and where the ani-mal spends most time feeding.

In addition to the spatial instability of thesepatches (depending on current intensity), theirquality also drastically changes over the year.due to a seasonal pattern in the abundance of themicro-fauna occurring in them: in early summer,most insects, the aquatic larvae of which forageand refuge within debris, emerge from thestream, causing a drastic reduction in the protein

content of these substrates (Gherardi. un-published). This decrease was reflected in thediet of the sedentary and aquatic males, whilethe females maintained a relatively high proteincontent in their stomachs, probably because oftheir trcqucnt and long-lasting excursions ontoland (Gherardi & Vannini. 1989). where there isabundant prey (Gherardi. I9S7).

Aggression occurred more often on vegetabledebris than on other substrates, as has beenobserved in the crayfish Orconectes ru.sticusGirard, whose aggressive activity in the labora-tory was affected by the quality of food (Capelli& Hamilton. 1984). However, at least in thefield, aggression seldom occurred in this species,notwithstanding the sometimes high iinimal den-


SECONDVITELLOGENESIS OVULATION

BEGINS • BEGINS

2 -

99

' N ' D ' J ' F ' M A ' M ' JPHASE

1PHASE

2

' A ' S ' 0 'PHASE

3

- 3 -o

2-

1 -

0-1

INTENSESPERMATOGENESIS

cfcf

r"Zr"r-;r"i , I r 1 . . I . rM ' A ' M ' JPHASE

1

J ' A ' S OPHASE

2FIG. II. Glycogen contcnl of hepatopancreas during a yearly cycle in twenty-one females (upper) and eighteenmales (lower).

sity in the pool and the paucity of patches ofdebris. The area inspected by the animals whileforaging was not actively defended by them, norwas its size related to animal density, contrary towhat is observed in territorial animals (Grant,I96H; Barlow, 1974). Conversely, there was alarge extent of superimposition of contiguousforagers (independent of sex and size), whichincreased with the crabs' density.

Moreover, the few agonistic interactions sel-dom escalated, and were limited to low aggres-sive patterns, such as avoidance and threats.Because of the low fidelity of crabs to any par-ticular area, and their dispersal along the stream(Gherardi & Vannini, 1989), this weak and rareaggression can only in part be due to a pre-

existing hierarchy maintained in time on thebasis of individual recognition (even if in thelaboratory /'. fluviatile proved capable of learn-ing some physical characteristics of a conspecificin a hierarchy; Vannini & Gherardi, 1981). Thewinner, either a male or female, was more oftenthe larger individual, in accordance with obser-vations in many other decapods, where sizeappears to be the most important factor in deter-mining a hierarchy (see, e.g.. Lowe. 195ft; Bovb-Jerg, 1956). In P. fluviatile, cheliped length,which shows a positive allometry (more markedin the males) with respect to carapace length(Ghcrdardi et ai, 1987). has a strong aggressivevalue (Vannini. Gherardi & Pirillo. 1983). Thefunction of chelipeds as "resource holding poten-

244 F. Gherardi. F. Tardticci and F. Micheli

tial' (sensu Maynard Smith & Parker. 1976)could explain the 'peaceful* behaviour of thecrabs observed here: on the basis of this non-ambiguous asymmetry, with no expenditure ofsurplus energy in fighting, larger animals haveeasy access to the patches of vegetable debris.while smaller specimens are relegated to thepoorer substrates such as the stream banks. Forthese latter animals, feeding on debris does notpay for the risks of dangerous injuries inflicted inescalated contests where the opponent is betterarmed, i.e. for small size classes these patchesdo not represent economically defcndableresources. However, this dispotic distributionover the foraging area matches the difference inenergetic requirements revealed in the popula-tion, smaller specimens significantly consumingiess oxygen than bigger ones (however, theyhave a higher weight-relative oxygen consump-tion than adults; Gherardi c/«/., 198Ha).

A different feeding strategy between sexesseemed to occur: males moved more slowly thanthe females, and occupied a smaller area, mini-mizing the time required to search for food, butmaximizing the rate of energy intake while feed-ing, as they prevalently grazed oti vegetabledebris ("time minimizers". Schoener, 1971). Onthe contrary, females were frequently excludedfrom the richer sources of energy because theywere normally smaller than males and had rela-tively shorter ehelipeds. were faster in theirmovements, inspected a wider foraging area,and searched for food mostly on sand andstones. The size of the inspected areas waspositively correlated with carapace length infemales, probably because larger crabs havehigher energy requirements. As shown by radio-telemetry (Gberardi et ai, 19R8b), in this sexthese short movements over an area whereorganic matter accumulates are intercalated, atleast in early summer, with long displacementsalong the stream or into the surrounding ter-restrial habitat ("nomadie" movements), in con-trast to the sedentary behaviour of the males.Much evidence, such as the consistent increaseof both gonad index and its fat content, as well ashistoiogieal analysis, suggest that in early sum-mer second viteliogenesis (Adiyodi. 1985)occurs. In other phases of the reproductivecycle, radio-tracked females appeared less vag-ile and more aquatic in their habits (Gherardi &Vannini, 1989).

This sexual diversity in spatial strategy associ-

ated with the reproductive phases was notrelated to differences in energy expenditure inthe sexes (oxygen consumption was the same formales and females of equal size), but was accom-panied by a consistent increase in the femalehepatopancreas index. The hepatopancreas,wbich in Crustacea functions as an indicatororgan of the general energy flow affecting anindividual (Aldricb. 1975). mainly accumulateslipids (glycogen on the contrary is scanty andalmost constant over the yearly cycle), whichcould measure the actual energetic input.

The rationale here is that increased locomo-tion, in spite of its costs in terms of risks ofpredation. furnishes an energetic reward tofemales, allowing them to extend and diversifytheir foraging area and thus to maximize foodintake in terms of quantity and/or quality. Thealimentary input wbich exceeds metabolicrequirements is stored in the hepatopancreas aslong-term lipid reserves to sustain the highlyexpensive viteliogenesis. resulting in the produc-tion of macrolecithal eggs. In this speeies, wherefemale parental investment is high, thebehaviour of "energy maximizers' (Schoener.1971) seems to be subjeet to a strong selectivepressure in females, whose reproductive successis directly related to the efficiency of harvestingfood.

Acknowledgments

We are indebted to Professor Marco Vannini(Dipartimento di Biologia Animate e Genetica.University of Florence) for the enthusiasm heshowed in supporting and encouraging thisresearch. Thanks are also due to Dr Fabio Mon-aci (Centro per lo Studio della Genesi e dellaClassificazioneeCartografiadelSuolo,C.N.R.)and Dr Pedro Castro (University of California)for their individual help in tbe laboratory ana-lysis, and to Dr Giuseppe Messana (Centro diStudio per la Faunistica ed Eculogia tropicali.C.N.R.) for his valuable and constant advice.The study was supported by a M.P.I, grant(•(•.()%•).

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(Manuscript accepted 1.^ February 19H9)

energy maximization and foraging strategies in potamon

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