lSRAEt. JOURNAL OF ITCOLOGY AND EVOLUTION. Vol . 52. 2006. pp. l5 t - l -5t i

Nore'.HAVE BLACK RATS EVOLVED A CULTURALLY-TRANSMITTED

TECHNIQUE OF PINECONE OPENING INDEPENDENTLY INCYPRUS AND ISRAEL?

Evl LaNoovA, Ivan HonAiFlK, ANr) DANIET_ Fnynra*Deportment of Zoologt, Charle.s lJniversit)', Vinihti 7, CZ-129 ll pruho 2,

C:ech Republic

Kerv,ortls'. cultural transmission. tradition. feeding innovation. fbraging. R(tttu,\ ruttrts

INTRODUCTION

Cultural transmission (tradition) of various complex behaviors in animals has receivedconsiderable attention in the past 30 years (earlier revie'uvs: Cavall i-Sfbrza and Feli lman.l 98 l : M i t che l l , 1987 ;Ga le f , 1988 ;more recen t :M ik los i . 1999 ;Ga le f , 2003 ) . C lass i ca lexamples come from primates, (e.g., chimpanzees: Tomasello. 1994: whitten et al..1999) and b i rds (e.g. . t i ts : F isher and Hinde, 1949; Darwin f inches: Bowman and Bi l leb.1965: caledonian crows: Hunt,2000). Most of them have been based solely on fieldobservations of behaviors restricted to certain populations. By definit ion. the traditionmust involve social learnins of some kind (Galef. 2003). rvhich is diff icult to demon-strate solely under field conditions.

Laboratory experiments studying the rnechanisms of social transmission of diversefclod-finding techniques (rvhich may underlie these traclit ions in the wild; fbr reviervs.see Mik lc is i . 1999; Galef and Gira ldeau.200l ;Galef .2004; Galef and Laland.200-5)have been repeatedly carried out in birds (solving fbod-linding problems in pigeons: pal-ameta and Lef 'ebvre. 1985; t i ts : Sasvar i , 198-5: keas: Huberet aI . ,200 l ; in budger igars:Heyes and Sagerson,2002) and rodents (e.g.. shell-opening techniques in Norrvay rats:cagnin, l9u5; food preferences in spiny mice: McFadyen-Ketchum and porler, l9ti9:in ground squirrels: Peacock andJenkins. 1988;and in Norway rats: posadas-AndrewsandRoper , 1983 ; Ga le f c ta l . , t 9 t l 4 ;Ga le f . 1989 ;Ga le f andA l l en . 1995 : bu tseeGa le fand Whisk in, I998. 2001 ) .

The best-studied examples of traditions in rodents studied in both fiee-living animalsand their conspecifics under laboratory conditions are those of Norway rats diving fbrfbod (Gandolfi and Parisi. 1972, 1913: Galef, l9ti0) and pinecone opening in black rats(Aisner and Terkel. 1992'.Zohar and Terkel, 199-5, 1996; Terkel, 1996). The fbrmer aremore influenced by different environmental conditions (distribution of molluscs andavailabil ity of alternative prey) than by specific knor,vledge transmitted culturally. lncontrast. gaining nourishment from the seeds of pinecones seems to be a well-document-'r 'Author to *hom correspondence should be addressed. E,mail: fivnta(atcentrunt.crAccepted 5 November 2(X)6.

1 5 2 E. LANDOVA ETAI- Isr . J . Ecol . Evol .

ed example of a tradition rvhere the social lezrrning is necessary fbr efficient transition of

knor.vledge from adults to young (fbr discussion. see Galef, 2003).Althou-eh the stripping technique is casily transmitted fiom mother to otfspring

(A i sne randTerke l . 1992 ) . t hcp resenceo f t hemo the rhe rse l f i sno tessen t i a l andmay

be substituted by the presence ofgreen (i.e., fresh, not rvooded) partially-opened cones.

Neverthcless, in nature such pinecone opening is dclne by skil led adult individuals (strip-

pers) only and consequently the anirnals cannot find partially-opened cones outside this

specific social context (Terkcl, 1996). Rats are ablc to learn the stripping technique only

during crit ici i l periods as juveniles. Early separation of the jr-rveniles fiorn the mother

reduces the success of this transmission (Zohii l ' and Terkel. 1996). Adult black rats r'vere

unable to acquire this tcchnique even rvhen properly motivated by fbod deprivation.

exposed to pinecones fbr a long pcriod. and/or caged r'vith a skil led adult used as the

demonstrator (Aisner and Terkel, 1992). The stripping technique of pinecone opening by

black rats rvas described only from certain localit ies in Israel and it is rvidely accepted

that this behavior is highly population specil ic (Terkel, 1996).Nevertheless. the conditions necessary fbr the evttlution of rat consumption of pine

seecls arc not restricted to Israel. Pine filrcsts are lvidespread in the Mediterrancan, includ-

ing those islands r,vhere the spccies richness of the mammalian tauna has been considerably

reduced by the island efl'ect and the extinction of iiboriginal species associated rvith the

recent invasion of their commcnsal compctitors-especially black rats (Rtttttts rattus).

Squirrels, a fully arboreal species that can efficiently and easily out-compcte the rats

and are knorvn to be able to harvest pine seeds, are absent on most Mediterranean is-

lands. as they are in lsrael (Mitchell-Jones et al.. 1999: Kryituf'ek and Vohralik.200 l).

Cyprus is a typical gree n Mediterranean island. Several areas. especially the Akamaz

Peninsula and tlvct mountain areas-Troodos Mts. and the Kyrenia Range-are covered

by pine fbrests of Pirrlr.r brtrt ia (belongin-e to the hullepensis-tunariensi.t group. up to

1500 m a.s.l.) and Pinus nigru t 'uruntanita, above 800 m a.s.l.). The black rat has become',vithgut a doubt the most abundant rodent species there. cclmpeting not only rvith the

endemic specics of mousc (.Mus c'vpriuur.r) (Bonhomme et al.. 2004) and spiny-mouse(At'otrtt 's nesiotes), but also rvith its smaller commensal cousin the house mouse (Mrt.s

lttrst trltts t lornesti< Lts). The black rat. building its nests in trees. remains the clnly arboreal

rqdent species on the island (Spitzenberger, 1978; KryStuf'ek and Vohralik,200l).

We studied the occurrence of small mammals (e.g.. genera Mus. AL'otttt 's, Cntcit lura)

on Cyprus and fbund remnants of fbods consumed by black rats in pine fbrests resem-

bling those previously described from lsrael. The aim of this study is to briefly report

these findings and discuss their importance fbr the undcrstanding of the pilreetrne open-

ing tradition and the consequence of cultural evolution in animals.

LOCAI,ITIES

During tr,vo field expeditions in March and October 2005 rve visited 55 localit ies through-

out Cyprus and found indications (f 'eces. tracks. and feeding places) of black rat presence

in most of them. Pinecones opened by rats were firund in the fbllor'ving five localit ies:

Vol. 52, 2006 RAI'S TRADITION OF PINECONE OPENING ON CYPRUS 153

(1) Akamaz Peninsula, Insigies trail, NW of Neo Chorio village, 35q03'N, 32"18'8,

305 m a.s.l., 12 October 2005; Three blind galleries in chromite mine. Rats' cave

cache containing huge amounts of stripped pinecones was found.(2) Central Troodos Mts. E of Troodotissa Monastery, SW of Prodromos Village,

34o56'N, 32"50'8, 1343 m a.s.l., 3l March 2005;Atypical old mountain pine forest

with rare stripped pinecones scattered on the ground.(3) 5 km S of Dhierona, 34o49'N, 33"05'E, 613 m a.s.l., 25 March 2005; Dry secondary

pine forest with a few stripped pinecones.(4) Eastern Troodos Mts. S of Palaichori, 34o59'N, 33o03'E, 990 m a.s.l., 26 March

2005; Mountain pine forest with rare stripped pinecones scattered on the ground.

(5) North of Ardana, Kyrenia Range Mts. 3522'N, 33"54'8,285 m a.s.l., 16 October

2005. Karst cave containing rats'cache with hundreds of stripped pinecones.

Moreover, two sub-adult rats were captured using wooden live traps laid on the

ground and baited with bacon (localities No. 1 and 5). An additional rat was observed

on 16 October 2006 in the cave 34o56'N, 32"53'E in the high Troodos Mountains at an

elevation of 1605 m a.s.l), and we also found signs ofblack rat presence at another high

elevation locality, 34o57'N, 32"52'E (1300 m a.s.l). All the captured and/or observed

black rats were grey colored.

RESULTS

In five localities distributed throughout Cyprus, we found pinecones stripped by rats

that could be easily distinguished from those fed upon by other animals such as, e.g., the

crossbill (I-oxia cumirostra) (see Fig. 1). The black rats can open the pinecones either by

an efficient stripping technique, which is transmitted socially, or by a shaving technique,

HilsHA

Fig. 1. Pinecones of different age opened by stripping method

Peninsula (A, B, C) and (5) North of Ardana, Kyrenia Range

by the crossbill (F).

of rats from localities (1) AkamazMts. (D, E). Pinecones consumed

r54 E. LANDOVA ET AL. Isr. J. Ecol. Evol.

an inefficient way that requires a greater energy expenditure during pinecone opening(Yanai et al., 1989; Aisner et a]., l99I:' Zohar and Terkel, 1996). The scales of the coneshad been removed exclusively using the spiral stripping technique. No example of theinefficient shaving technique was recorded. In two cases (localities 1 and 5) the strippedcones were found in caves, where the rats had cached them in huge numbers. In the lo-cality onAkamaz Peninsula (1), the stored closed pinecones, as well as the opened, usedones, covered almost the entire surface of the cave and their volume was roughly esti-mated as one cubic meter. The rats had clearly used the cache for a long period (years?);the cones in the lower strata showed signs of decomposition, whereas the others werefreshly stripped (Fig. 2).In the remaining three localities (localities 14) we found thecones in small, visibly artificial aggregations under the pine trees; however, no cave wasavailable in close proximity to these findings.

DISCUSSION

Our findings suggest that the black rats on Cyprus use the same technique to harvest pineseeds as those in Israel. The stripped pinecones found in Cyprus are indistinguishablefrom those reported in Israel by Terkel (Aisner and Terkel, 1992;Terkel,1996;Zoharand Terkel, 1996). This evidence is unequivocal; nevertheless, we did not observe strip-

Fig. 2. Bottom of the cave covered by pinecones - detail.

Vrl . 52. 2006 RAT'S I 'RADITION OF PINECONE OPENINC] ON CYPRUS 155

ping behavior directly as clnly young. apparently incxperienced black rats entered ourr.vooden live traps designed fbr mice.

As cln most other Mediterrancan islands. black rats constitute an important com-ponent of the rodent population in Cyprus. They are distributed throughout the island(Spitzenbcrger. l97U) in nearly evcry type of habitat f iom coastal clif l .s and agriculturallandscapcs up to the highest elevations of the Troodos Mountains (our observations).

Black rats are relatively nerv imrnigrants to the Meditcrranean islands. evcn rvhencompared to another commensal murid species-the house mousc (Cucchi et al., 2005).The archaeo-zoological records of the black rat suppr)rt its appearanec' on Mediterraneanis lands dur ing the Roman per iod. i .e . . the l i rs t centur ies 1 ' .p . . (e.g. ,McCormick,2003:Corsica and Sardinia: Vigne. 1992). This coincides approximately with the first out-breaks of pla-eue in thc late Roman period (Audoin-Rcluzeau. 1999). We can, therefbrc.reasonably expect that the Cyprus population of black rats is about 2,(X)0 years old.rvhich provides a timc frarne fbr the pineconc opening tradition therc.

Although Cyprus was most probably colonizcd by rats frorn the Turkish. Syrian.Lebanese. or lsraeli coasls. it is unlikely that the original f i lunders of thc current Cy-prus population of the black rat transf'crred their pineconc strippin-u behavior f iont theirhomelands. Thc island at'eii is separatcd fl 'om the nearest Turkish mainland by 70 kmof Mediterrancan Sea. complicating the exchanse of knorvlcdge by rats (althou-sh tradeconnections across the Mediterrancan have existed frorn antiquity). Moreovcr', the ar-eas of Cyprus and the ad.jacent mainland have been dcnscly pclpulated by hurnans andlargely defitrcstcd since the Ronran pcriod. preventin.l earlicr populations of rats fiorlthe possib i l i ty of t ransrn i t t ing p ineconc opcning.

While lve can only speculate about thc probabil ity of exchange beti.veen ntainlandand Cyprus rats durinc thc last centuries, thcrc is another argument in fhvor of the indc-pcndent development o l ' th is t radi t ion i r r Cyprus and in Israel . Thcrc is ind i rect ev idcncethat the tradition of pincconc openin-u in Isracl arose only reccntly. tvith the present dis-tributictn of pine firrcsts bcing the result ol 'cun'cnt reti)restation cfhrts (Terkel. 1996). Itmay also be signiticant that pinecone opcning behavior in lsracl was not reportccl prior'to thc car ly l9 t l0s (Aisncr . l9 lJ l ex Terkel , 199(r ; .

It is notable that the localitics rvhere rve fbund strippcd pinecones arc also separated byagricultural landscapes r.vithout pinc fil-cst. representint a nertural barrier and preventing theeasv migriition clf knorvled.eeablc rats fl'clm one population to another across Cyprus (Fig. I ).

The possibil i ty that the tradition of pineconc opcnin-s evolved indcpendently at dif-f 'erent t imcs and places looks rnore l ikely rvhcn firod habits and thc seneral ecologicalstrate.cy of black ri its are consiclcrcd. In the Meditcl 'rancan (e.g.. in Clorsica and Turkcy)they re-srularly ncst in trees. use arborcal highivays. and consume seeds, f iuits (includin-uponlegranate Ptrtt itu gr(ttuttun and thc citrus C'i lr 'rr.r ' ourdttt iu). and. somctirtrcs. bark(Kahrnann and Qaglar . 1970).

On thc other hancl. laboratory studies carricd out in lsracl shrtlved unequivocall l ' thatadult rats can barely i icquirc the strippin-u tcchnique even aficr long-term exposure toplncconcs and proper mot ivut ion (Aisncr and Terkel . 1992). In enr iched envi ronmentsrescmbling the natural situitt ion. not onc of one hundred cxpcrirnental black rats rvas

1 5 6 E. LANDOVA ETAL. Isr. J. Ecol. Evol

able to acquire the strippin-q technique, and even when faced with serious starvationthey used inefficient methods to open the cones (Terkel, 1996). In a simplified laboratoryenvironment, however, spontaneous asocial pinecone opening and the efficient strippingmethod "vere detected, although its incidence rvas lolv (six of 172 experimental blackrats). Tcl apply these laboratory results to our natural example on Cyprus. it is necessaryto multiply the incidence of spontaneous learning by the number of rat generations overthe centuries and the estimated size of the black rat population in the 9250 km2 area ofCyprus. The resulting statistical probabil ity of the spontaneous development of the in-novation is almost certain across a populaticln scale. This conclusion is also consistentr.vith the opinion of Galef (2(X)3), that the independent tradition of pinecone openingcould arise in suitable conditions, e.g.. restriction clf tbod resources to pinecones and theabsence of squirrels. Hor.vever. it has not yet been reported fiom another locality.

The efhcient strippin-e method of pinecone opening has further ecological consequenc-es. We rvere surprised by the presence of black rats even in the high elevations of the Troo-dos Mountains. rvhere rve had originally expected small mammal assemblages nclt aff'ectedby black rat presence and consequcnt predation. Pine seeds seem to be the only availablesource clf food in these areas. Food storage in caves and the efficient extraction of seeds bymeans of the stripping technique may provide the key factor to black rat survival in theserelatively cold and snowy areas. Ctxsequently. just as the black rat presence represents animporlant cause of extinction of thc insular endemic species of small rodents. the strippingtechnique rnay be also vierved as an important factor in conservation biology.

Thc story of pinecone opening in black rats reinforces the knorvledge that culturaltransmission may contribute considerably to the evolution and distribution of suchadaptive behavioral characteristics. rvhich may be inventcd rvith diff iculty. but repeat-edly. and therefbre their distribution does not appear to be confined solely to a ceftainpopulation consisting of animals sharing a tradition transmitted fiom a single in-eeniouslnventor.

ACKNOWLEDGMENTS

We thank Radek Lridan, Pavel Hulva, Miloi Macholdn. Alena Pazderovii. and PetrKlvaia fbr thcir kind help in thc fleld. We are indebted to Vladirnir Vohralfk, specialistin the mamrnzrlian f 'auna of Turkey and Cyprus, fbr his valuable comments on earlier ver-sions of this manuscript. This research was supported by the Czech Science Foundationpro1ect no.206105123321 given to LH. Participation of E.L. was supported by institutionalgrant no. 002 1620828. provided by the Ministry of Education, Youth and Sport of theCzech Reoubl ic .

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