ZOOGEOGRAPHY AND THE PREDATOR-PREY `ARMS RACE :'A COMPARISON OF ERIPHIA AND NERITA SPECIES FROM THREE FAUNAL REGIONS

William W. REYNOLDS & Linda J. REYNOLDS

Department of Biology, The Pennsylvania State University, Wilkes-Barre, Pennsylvania 18708 U .S.A .

Received March 14, 1977

Keywords : zoogeography, predation, evolution, coevolution, allometry, Eriphia, Nerita, Gulf of California, competition, ecology.

Abstract

We measured maximum shell diameters and thicknesses ofNerita funiculata Menke and N. scabricosta Lamarck (Gastropo-da: Neritidae), and claw sizes and carapace widths of the preda-tory crab Eriphia squamata Stimpson (Brachyura : Xanthidae),from the Gulf of California (Eastern Pacific) . We also tested theability of E. squamata to crush Nerita shells of various sizes . Wecompared this data on predator-prey counteradaptations withpreviously published data for congeneric species from the Wes-tern Atlantic and Indo-West Pacific regions . In relative abilitiesof the crabs to crush gastropod shells, and of the gastropod shellsto resist such crushing, the Eastern Pacific species were `stronger'than their counterparts in the Western Atlantic, but `weaker' thantheir Indo-West Pacific congeners, indicative of an intermediatelevel of 'faunal dominance' or predator-prey `arms race' escala-tion .

Introduction

A recent comparison of Guamanian and Jamaican pred-atory crabs and their shelled prey (Vermeij, 1976) indi-cated interoceanic differences in the state of escalation ofco-adaptations to the overall predator-prey relationship(i .e ., the `arms race') . Specifically, crabs from Guam inthe Indo-West Pacific (WP) region are larger, and havelarger and stronger crushing claws (in both a relative andan absolute sense) than their counterparts from Jamaicain the Western Atlantic (WA) region, while Guamaniangastropod shells are on the average larger and thicker(thus more resistant to crushing) than their Jamaicancounterparts . The implication is that in the vast and

Dr. W. Junk b .v. Publishers - The Hague, The Netherlands

Hydrobiologia vol . 56, 1, pag. 63-67, 1977

speciose Indo-West Pacific faunal region, intense bioticinteractions have produced greater selection pressures onboth predators and prey, resulting in a higher degree ofmutual counteradaptation than has occurred in thesmaller and less speciose Western Atlantic region .

The Indo-West Pacific faunal region is generally re-garded as the evolutionary and distributional center forthe tropical shore animals of the world, and continues todonate species to other regions (Briggs, 1974) . The West-ern Atlantic region is considered a secondary center ofevolutionary radiation (Briggs, 1974) . In general, thecompetitive advantage in dispersal seems to lie withspecies from the area with the richer fauna and higherlevel of competition; the richer area will donate species tothe poorer, but seldom the reverse (Briggs, 1966 ; 1974) .

The fauna of the tropical Eastern Pacific (EP) region isderived largely from the Western Atlantic, with consider-able speciation having occurred since isolation of thesefaunas by formation of the Isthmus of Panama barrierseveral million years ago (Rosenblatt, 1963 ; Brusca,1973; Briggs, 1974) . This has resulted in a large number ofamphi-American geminate or `sibling' species (Rosen-blatt, 1963) . Trans-Pacific species from the WP regionhave also invaded the EP region by crossing the EastPacific deep-water barrier, which at present is estimatedto be only about 94% effective, compared with 99% forthe New World Land Barrier (Briggs, 1974) .

Interoceanic faunal comparisons can yield valuabledata on the effect of species diversity and resultant inten-sity of biotic competition on the evolution of relativecompetitive ability. Such studies could also yield predic-tive data on the possible effects of a sea-level canal acrossCentral America (Vermeij, 1974a), which could result in

63

species from one region invading, out-competing andreplacing the fauna of the other region. Prediction on thebasis of species diversity alone is difficult because thetropical amphi-American faunas are incompletelyknown, and we `simply cannot say how many species arepresent' (Briggs, 1974, p . 117). The EP region is some-what depauperate due to lack of reef-building corals(Rosenblatt, 1963), but some general depauperization hasalso occurred in the Atlantic due to climate shifts sinceisolation of these faunas (Briggs, 1974) . For example, inthe mid-Miocene, before closure of the isthmus, the EPand WA regions had practically identical molluscanfaunas, but Pleistocene climatic shifts in the Atlanticcaused extinction of 43 genera and subgenera which stillsurvive in the Pacific, while only four genera extinct in thePacific survive in the Atlantic (Briggs, 1974) . The EPfauna as a whole has been further enriched by immigra-tion of competitively superior WP species (Brusca, 1973 ;Briggs, 1974) . These considerations would seem toindicate a possible competitive advantage to the EP overthe WA region, although some have attributed a compe-titive edge to the WA based on very rough estimates ofrelative species numbers (Briggs, 1974) .

To shed further light on this question of faunaldominance, we gathered data on representative EP (Gulfof California) predator and prey species for comparisonwith previously published data on WP and WA species .To facilitate interoceanic comparisons, we chose forstudy genera with representatives in all three zoogeo-graphic regions, so that comparisons would be intrage-neric . For purposes of this study, these selected genera areregarded as representatives of each region, but not neces-sarily as specific predator-prey pairs .

The prey genus we chose for study was Nerita (Gastro-poda: Neritidae), represented by N. funiculata Menke(EP), N. scabricosta Lamarck (EP), N. tessellata Gmelin(WA), N. versicolor Gmelin (WA), N. peloronta L . (WA),N. albicilla L . (WP), and N. plicata L . (WP) . These neritesare generally small, globular, low-spired, ribbed herbi-vorous intertidal gastropods (Morris, 1966, 1973 ; Hughes,1971 ; Brusca, 1973), whose antipredatory adaptations in-clude thickened shell lips, narrow, toothed apertures, andcalcareous, inflexible opercula, as well as shell sculpture(ribbing) and low spires (Hughes, 1971 ; Vermeij, 1974a,1974b). The predatory crab genus studied was Eriphia(Brachyura: Xanthidae), represented by E. squamataStimpson (EP), E. gonagra Fabricius (WA), E. scabriculaDana (WP), E. smithii McLeay (WP), and E. sebanaShaw & Nodder (WP) .

64

Methods

We gathered the data on EP species during July 1976 atPuerto Penasco, Sonora, Mexico (northern Gulf of Cali-fornia), where E. squamata is the dominant large inter-tidal crab (ranging to Ecuador and the Galapagos) oc-curring in association with N. scabricosta (largest of theNeritidae ; ranges south to Ecuador) and N. funiculata(ranges south to Peru; Brusca, 1973). The WP and WAdata for congeneric species are from a previous study(Vermeij, 1976) .

We measured maximum shell thicknesses and maxi-mum shell diameters of Nerita funiculata and N. scabri-costa, and added similar data reported by Vermeij (1976)for WA and WP Nerita species (Table I) . We calculated a`prey index' by dividing the maximum shell thickness(mm) by maximum(tested) shell diameter, which wasoften smaller than maximum reported size of the species(Table I) .

We measured the manus height and thickness (width)of the large crushing claw, and the width of the carapace,of 5o Eriphia squamata (Table II) . Manus height andmanus thickness (mm) were each divided by carapacewidth to yield a size-specific measure of relative claw size,and tabulated along with similar data for WP and WAEriphia species reported by Vermeij (1976) . We thencalculated a `predator index' (Table II) by multiplying themeans of the above values to give a measure of claw cross-sectional area for each species, as an indicator of clawstrength (which depends on the cross-sectional area of themuscle-cf. Vermeij, 1976) . We calculated both arith-metic and logarithmic least-squares regressions fromthe claw-size carapace width data to determine whetherallometry exists in the relation of claw size to body size(cf. Gould, 1971 ; Reynolds & Karlotski, 1977) .

In addition to these morphological criteria of respec-tive predator and prey `strength', we conducted behavioraltests to determine the actual ability of E. squamata tocrush shells of N. funiculata and N. scabricosta. Sevencrabs ranging from 21-35 mm in carapace width wereoffered a range of shell sizes in closed containers . Most ofthese were N. funiculata shells inhabited by hermit crabs.

Table 1. Pre, data N, Nerita 'PP.

Region SpaiesMaximum aft, reported

(mm)Maximum she tested

(mm)Maximum shell thickness

(mm)Prey index

EP N. funiev/am 25 18.0 1 0 0.056EP N acabrtromu 45 17.0 1 0 0.059WAWA

N .-lb.N.,meirob,

2128

20.927 .2

1510

0.0720.037

WA 1.pe 1omnm 38 34 .5 0.029WP N albieilb 30 30.0 0.083WP N. 'Banta 28 27 .9 0.088

Table 11 . Predator data for Eefphle Wp.

A few hermited N. scabricosta shells (less common atPuerto Penasco) were also offered . Live Nerita snailswere able to crawl up the sides of the containers andescape, and so were less satisfactory for the experimentsthan 'hermited' shells . The hermit crabs served as `bait' toinduce the crabs to crush the shells (cf. Vermeij, 1976) .These shells possess mechanical properties indistinguish-able from those of living snails (Curry, 1975) . The meanshell diameter of the largest shell crushed and the nextlargest shell not crushed (where possible, these werein i mm increments) was termed 'prey critical size' forthat crab (Vermeij, 1976) . Where the largest shell offeredwas crushed, its size was tabulated as the prey critical size,and so indicated by a '+' (Table I11) . Similar data onability of E. sebana to crush various WA and WP Neritaspecies, as reported by Vermeij (1976), were added forcomparison (Table III) . Finally, we calculated a 'preda-tion index' by dividing prey critical size (mm) by crabcarapace width, denoting with a '+' indeterminate criticalprey sizes (largest available shell crushed) . We plottedprey critical size (Fig . IC) against crab carapace width forour seven E. squamata (preying on N. funiculata, preyindex 0.056), and also used Vermeij's (1976) values fortwo large E. sebana preying on N. albicilla (prey index0.063) ; we used prey with similar prey indices to ensurethat differences in prey critical size would be due primar-ily to crab strength and not shell strength . We calculateda leastsquares regression line based on this data (Fig . I C),and indicated the range of critical prey size values inrelation to varying prey index (0 .029-0 .072) for the twolarge E. sebana (56.1 and 65 .3 mm carapace width) .

Table 111. Calculation of peedation loden from Prey mite me (largest shell crashed) and predator nine .

'Clot to maximlnd eon .

Results

The EP and WP Nerita species (Table i) showed a closelinear relationship between shell thickness and maxi-mum shell size (Fig . IA), with a correlation coefficient (r)of 0.997 . The three WA species were more variable, andtheir inclusion in the regression lowered r to 0 .281 . Theprey indices (Table I) of the EP species (0 .056 and 0 .059)were smaller than those of the WP species (0 .063 and0.068), but larger than the average for the three WAspecies (0 .029, 0 .037, 0 .072 ; z = 0 .046) .

There is some degree of allometry (cf. Reynolds & Kar-lotski, 1977) in the claw size/carapace width relationship,both interspecifically (Fig . i B) and intraspecifically . For5o E. squamata ranging from 14.5-40 mm in carapacewidth, the .regression of manus area (as manus height x

_ B

EE

20-6

1k1to-,sCARAPACE WIDTH mm

Fig . i . A, relationship of shell thickness to shell size of Nerita spp .from the Eastern Pacific (o), Western Pacific (9), and WesternAtlantic (A) ; x = mean value for WA spp . ; regression line cal-culated for EP and WP species . B, relationship of manus area(upper curve) and of manus height (lower curve) to carapacewidth for Eriphia spp . ; curves fitted by eye ; dotted rectangle in-cludes data range for 50 E. squamata . C, relationship of preycritical size to crab carapace width ; x = mean for seven E. squa-mata ; calculated regression line based on prey index of 0.056 forE. squamata (o), 0 .063 for E. sebana (e) ; vertical bars indicaterange of data for E, sebana preying on Nerita with prey indicesfrom 0 .029 to 0.072 . D, mean predator and prey indices for theWestern Atlantic (A), Eastern Pacific (o), and Western Pacific (.) .

6 5

Region Specie nCarapace 910th Mamas heightrange (mm)

Canpaee 5110thMe. a thl kflsseCanpace width

PredatorW..

mean range mean range

EP E. 4- 50 14.5-40,0 0 .420 0.300-0 .470 0290 0 .210-0.330 0.122WA E. V- I7 18.8-43 .7 0.416 0.373-0 .485 0.288 0 .254-0.344 0.120WP E -bd.b 4 21.0-24 .4 0.440 0.414 - 0 .463 0,308 0 .299 - 0.314 0.136WPWP

E .emfth0E nbona

823

34.9-65 .136.7 -65 .3

0.4730,503

0.416-0 .5040.411 - 0 .603

0 .3150.314

0,269-0.3710 .262 - 0.366

0.1500.158

Predator Carapace51NN (mm)

Prey Critical aloe(mm)

Leegestoffered(mm)

Predationindet

E. aquamam (EP) 21.0 N. f.Wmkn (EP) 9 .0 10 .0 0.4329.0 N. funfaabm (EP) 14.5 15.0 0.50E. eq=ta (EP)

E. agmmate (EP) 29.5 N junkvbta (EP) 17 .0+ 17 .0 0.59+E. equaman (EP) 29.5 N. ambrlrona (EP) I7 0+ 17 .0 0.59+E. squaman (EP) 32.5 N. Juedrvbta (EP) 17 .5 18 .0 0.54E. nquaman (EP) 33.5 N. funlcubn (EP) 14 .5 15 .0 0.43E. aquamam (EP) 34.0 N. ft nim4m (EP) 16 .5+ 16 .5 0.49+E. aquamata (EP) 35 .0 N . Junlmlam (EP) 15 .0 15 .5 0.43E. aebam (WP) 36 .1 N. aIUMI k (WP) 23 .6 24,3 0,42E& sebarea (WP) 56 .1 N. pllmta (107) 21 .0 22.6 0.37E. aebana (WP) 56 .1 N. teeeham (WA) 20 .9+ 20.9' 0.37+E web-(IVP) 56 .1 N. verwoolor(WA) 21 .7+ 21 .7 0.39+E, ft.(W% 56.1 N. PNOronta (WA) 30 .0+ 30.0 0,53+E.sebaru(WP) 65 .3 N.a16Mlla(WP) 27 .1 30.0' 042E. aebaw (WP)E.eehane(WP(

65 .365 .3

N. pfimm 1187)Nrcaulks.(WA)

27 .9+20 .7+

27 .9'20.7

0,43+0,32+

E U- (WP) 65,3 N. rerafmbr (WA) 27 .2+ 27,2' 0,42+E aebnm (WP) 65 .3 N pebmnta (WA) 34 .5+ 34.5 033+

manus thickness) on carapace width yielded a logarith-mic regression (r = 0.944) equation :

109 M = -1 .3276 + 2 .2834 log C, orM = 0.047 C 2 28

where M = manus area (mm 2) and C = carapace width(mm) . This indicates some allometry, since the ex-ponent 2 .28 exceeds the expected power of 2 which shouldrelate an area (L 2) to a linear dimension (L) .

In the interspecific comparison (Fig. IB), manus areais proportional to the 2 .26 power of carapace width (r =

0.995); and the linear dimension of manus height is pro-portional to the 1 .18 power of carapace width (r = 0 .994),versus an expected value of 1 .o in the absence of allo-metry. This means that larger crabs have larger claws,relatively as well as absolutely .

The predator indices of EP E. squamata (o,122) and ofWA E. gonagra (0.120) were very similar (Table II), whilevalues for the three WP species were considerably greater(0.136, 0 .150, 0 .158 ; X = 0 .148). At least two of the WPEriphia species (Vermeij's data for E. scabricula are in-complete) apparently reach a larger size (65 mm carapacewidth) than either WA E. gonagra (44 mm) or EP E.

squamata (55 mm; Brusca, 1973) .In the behavioral tests, prey critical size (Table III) was

related to crab carapace width (Fig . I C) by the equation

P = 3 .75 + 0.36 C

(r = 0 .954)where P = prey critical size (mm) and C = crab carapacewidth, (mm) .

The effect of varying prey index (from 0 .029 to 0 .072)on prey critical size for a given predator (E. sebana) is evi-

dent from the vertical (range) lines in Fig . i C .

Predation index (Table III) was correlated with bothprey index (Table I) and with predator index (Table II) .

With a constant predator index (E. sebana, 0.158), preda-tion index was negatively correlated with the prey indicesof five Nerita species (56.1 mm E. sebana, r =-0.792 ; 65 .3mm E. sebana, r = -0 .761). Conversely, with the preyindex held constant (N.funiculata, 0.056), the predationindex was even more strongly correlated (r = 0.886) withthe predator indices of seven individual E. squamata(21-35 mm carapace width) . The mean predator andprey indices of the EP species were intermediate to thoseof the WA and WP species (Fig . iD), the latter being the`strongest' in both indices .

66

Discussion and conclusions

Among the three WA Nerita species, there is a negative

relationship between prey index and the elevation in-habited within the intertidal zone . N. peloronta, the

largest species with the lowest prey index (0 .029), occurshighest in the intertidal, while the small, thick (preyindex = 0.072) N. tessellata lives under stones in the lowintertidal. N. versicolor is intermediate in all these re-spects (Abbott, 1968, 1970 ; Hughes, 1971) . There may bea trade-off between size and shell thickness ; and intertidalzonation and microhabitat probably influence vulner-ability to predation to some extent (Vermeij, 1974b) .However, this clear relationship among the WA speciesis not apparent among the Pacific species . N. plicata (WP)occurs higher in the intertidal zone than WP N. albicilla(Hughes, 1971), but is slightly smaller, with a slightlygreater prey index (Table I) . The EP species, N. scabricos-ta and N. funiculata, do not differ greatly in prey index ;nor did we observe any obvious difference in intertidalzonation between them, although N. funiculata wasmuch more abundant at Puerto Penasco (we saw morelarge N. scabricosta further south in the Gulf, and fewerE. squamata and N. funiculata) . N. scabricosta is thelargest high intertidal neritid, reaching 50 mm in shell

diameter (Vermeij, 1974b) . While the large N. scabricos-

ta possesses a spire, the smallerNafuniculata has no spireat all, lack of a spire being an effective anti-predatoradaptation (Vermeij, 1974b). This is another possibleindication of a trade-off between size and morphologicalanti-predator adaptations (Vermeij, 1974a) . Nerites in

general are well adapted morphologically to resist preda-tion (Vermeij, 1974b). Further data are necessary toclarify whether there is any shell size allometry amongthese gastropods .

The claw size allometry among Eriphia species (Fig .i B) indicates that the WP species have larger claws in botha relative and an absolute sense, since they reach a largercarapace width (Table II). However, even small speci-mens of E. scabricula have a greater predator index thanthe EP and WA species, so the difference is not duesolely to a difference in overall size . The intraspecific (on-togenetic) claw size allometry in E. squamata parallelsthe ontogenetic allometry of claw length in relation tobody length in the lobster Homarus americanus (Gould,1971) . Lack of allometry in the critical prey size/crabcarapace width relationship (Fig . i C) could be taken toindicate that the claw size allometry does not indicate areal allometric increase in claw strength with size, since

`preservation of shape is not the anticipated result of achange in size,' because larger animals `must changetheir shape in order to function as well as smaller animalsbuilt on the same plan (a consequence, for the most part,of declining surface/volume ratios at increased sizes)'(Gould, 1971, p . 129) . However, it appears that in this casethe allometry is obscured by the use of prey critical sizesfor prey with a prey index of 0 .063 for the larger E. sebana,

while the prey index for the smaller E. squamata was only0.056 (Fig . IC) ; for E. squamata preying onN,funiculata,there is in fact an allometric relationship between preycritical size and crab carapace width, indicating that theallometric increase in claw size may imply greater relativeclaw strength in larger crabs .

In the behavioral tests, we observed that the size of thefirst shell selected and crushed by E. squamata tended tobe about 0.42 times the carapace width of the crab, beforeeither larger or smaller shells were crushed . This mayindicate an optimum prey size preference on the part ofthe crabs, which is probably related to claw size andstrength and the required energy expenditure per unitreturn . With increased motivation (hunger coupled withunavailability of optimum prey size), larger shells couldbe crushed with presumably greater effort, sometimesresulting in indeterminate upper critical prey sizes andpredation indices (Table III) due to unavailability of largerprey. Behavioral preference and motivation are likely asimportant ecologically as maximum ability, since theyreflect what will be done rather than what can be done .

The EP species had mean predator and prey indices(Fig. ID) greater than those of WA species, althoughsmaller than those of WP species . (The nearly identicalpredator indices of the EP and WA crabs may indicatethat these are sibling species [Rosenblatt, 1963] whichhave speciated since formation of the Isthmus of Pana-ma). Therefore, insofar as species of Eriphia and Nerita

can be regarded as representatives of their respectivezoogeographic regions, it would appear that the level ofpredator-prey `arms race' escalation in the Eastern Pacificregion is slightly greater than that in the Western Atlantic(although less than in the Indo-West Pacific), perhapsdue in part to the influence of trans-Pacific WP immi-grants in the EP . On the basis of the data presented here,we would predict that EP species should have a slightcompetitive advantage over WA species should contactoccur through a sealevel canal . This is in agreement withthe conclusions of Vermeij (1974a) based solely onfeatures of gastropod shell morphology, but contrastswith Briggs' (1974) conclusions based on rough estimates

of relative species numbers . It is particularly likely thatthose EP species derived from the WP region by trans-Pacific migration would invade and dominate the WAregion should they gain access through a sea-level canal .

Acknowledgement

We thank Dr Donald A . Thomson and the students of hisMarine Ecology summer field course from the Universityof Arizona who helped us to collect the crabs and gastro-pods for this study. We are also grateful for laboratoryand living accommodations provided us at the Universityof Arizona-Universidad de Sonora Marine Station atPuerto Peiiasco .

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