Ecologists have abandoned attempts to develop asimple unifying theory to account for community

patterns (Lawton 1999) Instead to explain such patternsthey rely on local ecological processes as well as on morecontingent historical processes acting at large temporal andspatial scales (eg unique historical events controllin gspeciation and biogeographic interchanges) This mixedapproach should lead to a more realistic idea of the realworld but it deserves careful epistemological considerationAlthough historical hypotheses may account for asubstantial part of community patterns they impose limitsto theory development because they deal with contingentevents that may often be theoretically intractab le Anecological system may be unique but this does notnecessarily imply that it is lawless in the ontological senseConsequently the methodological problem remains ofdistinguishing its general properties from its idiosyncraticproperties (Mahner and Bunge 1997) Historicalexplanations also impose limits to hypothesis testingbecause they often do not make predictions and can beelucidated solely by historical reconstruction (Schluter andRicklefs 1993)

Because theory development is a prerequisite for eco-logical understanding researchers should continue todevelop general theories even as they recognize theimportance of history (Pickett et al 1994 Mahner andBunge 1997) Theory development can be fostered by test-ing the predictions of the ldquocommunity convergencerdquohypothesis through comparative studies (Schluter andRicklefs 1993) This hypothesis specifies that independent-ly assembled communities in similar but geographicallydistant habitats converge in composition and functioningif they face similar environmental pressures (ie if theyare molded by the same local ecological processes)

Ecologists have long searched for matching patterns inthe biota of arid lands because similar harsh pressures arethought to prevail in deserts (eg Orians and Solbrig1977 Mares 1993a) An example of such an analysis is theset of experimental tests for convergence in seed harvest-ing by granivorous mammals ants and birds in desertsworldwide (Mares and Rosenzweig 1978 Abramsky 1983Morton 1985 Kerley 1991 Vaacutesquez et al 1995 Lopez deCasenave et al 1998) The initial conclusions of suchexperiments indicated that seed removal by mammals was

higher in deserts of the northern continents than of thesouthern continents that ants are the main seed harvestersin southern deserts and that seed removal by birds is lowin deserts around the world (Mares and Rosenzweig 1978Abramsky 1983 Morton 1985 Kerley 1991 Kerley andWhitford 1994)

These studies seem to suggest a lack of convergence inseed harvesting However comparative studies dependstrongly on the robustness of established patterns and theabove generalization was not tested for robustness butinferred by using one research approach alone (ie baitremoval experiments) Furthermore this generalizationwas supported in some cases by only one experiment car-ried out in one location within a particular desert There-fore some of the purported patterns of granivory at thecontinental scale might be artifacts of the limited basis of

February 2000 Vol 50 No 2 BioScience 123

Articles

Luis Marone (e-mail lmaronelanetcomar) is a scientist research-

er for Consejo Nacional de Investigaciones Cientiacuteficas y Teacutecnicas

(CONICET) of Argentina Javier Lopez de Casenave is a scientist

researcher and teaching assistant in the Department of Biology

Universidad de Buenos Aires 1428 Buenos Aires Argentina Viacutector

R Cueto is a scientist researcher at the Museo Argentino de

Ciencias Naturales ldquoBernardino Rivadaviardquo 1405 Buenos Aires

Argentina Marone is a desert biologist interested in community

ecology and epistemology and Lopez de Casenave and Cueto are

biologists studying the ecology dis tribution and biogeography of

Argentine birds All three authors are members of the Desert

Community Ecology Research Team (Ecodes) Argentine Ins titute for

Arid Zones Research (IADIZA) Casilla de Correo 507 5500

Mendoza Argentina copy 2000 American Institute of Biological

Sciences

Granivory in Southern SouthAmerican Deserts ConceptualIssues and Current EvidenceLUIS MARONE JAVIER LOPEZ DE CASENAV E AND VIacuteC T OR R C UET O

GRANIVORY MAY HAVE A SIGNIFICANT

COMMUNITY ROLE IN THE MONTE AND

OTHER SOUTH AMERICAN DESERTS

DESPITE THE PROBABLE LACK OF HIGHLY

SPECIALIZED SEEDEATERS

empirical information (Mares 1993a) For example Maresand Rosenzweig (1978) Abramsky (1983) and Morton(1985) all asserted that total granivory in the extensiveMonte Desert of Argentina is depressed and granivorousassemblages depauperate in comparison with other warmtemperate deserts However this conclusion was derivedfrom a single experiment carried out near Andalgalaacute inthe far northern reaches of the Monte Desert (Figure 1Mares and Rosenzweig 1978) Despite the narrow domainof this study many scientists have tacitly extended its con-clusions to arid South America as a whole (Abramsky1983 Morton 1985 1993 Brown and Ojeda 1987 Kerley1991 Wurm 1998 but see Vaacutesquez et al 1995 Lopez deCasenave et al 1998)

In this article we summarize current evidence about theresource base of granivorous animals the pressures theseanimals impose on seed reserves and the main ecologicalfeatures of the assemblages of seed-eating ants mammalsand birds in the Monte Desert and other southern SouthAmerican deserts We examine the general validity of thecommonly accepted patterns of granivory by using multi-ple research approaches to verify pattern robustness If the

patterns are robust they should be thebasis for more reliable tests of thecommunity convergence hypothesisof granivorous assemblages in desertsfrom different continents Such testscould provide a more informedassessment of the relative roles of localecological processes and unique his-torical circumstances in organizingdesert communities

The resource baseMares and Rosenzweig (1978) ob-served that ldquototal granivory is much

depressed in the Monte Desert where granivorous mam-mals are rare and ill-adapted ants are depauperate and notusually granivorous and birds are unimportant seed con-sumersrdquo and they suggested that low granivory would bethe consequence of a seed decline in South Americandeserts caused by the relatively recent extinction of themarsupial family Argyrolagidae in South America Maresand Rosenzweig (1978) assumed that argyrolagids wereecological equivalents of the rodents of the North Ameri-can family Heteromyidae (Saacutenchez-Villagra and Kay1997) and they outlined two alternative evolutionary sce-narios whereby marsupial extinction might have led to adecline in granivorous assemblages (particularly of ants)via a decrease in their resource base (ie seeds) In the firstalternative argyrolagids were indirect evolutionary mutu-alists with ants consuming seeds not preferred by antsThus when the argyrolagids became extinct ant-preferredplants whose seeds were still consumed would have beenoutcompeted by predator-free ant-avoided plants Thedecreased availability of seeds from ant-preferred plantswould have led in turn to a decline in the granivorous antassemblages themselves In the second scenario argyro-

124 BioScience February 2000 Vol 50 No 2

Articles

Figure 1 The Monte Desert inperspective (top) The worldrsquos desertregions including some semi-aridareas that are not generallyconsidered true deserts are indicatedby shading (inset) The Monte Desertin southern South America is arelatively narrow northndashsouth beltthat is oriented along the easternslopes of the Andes Mountains Itbroadens to the south and extends tothe Atlantic coast in northernPatagonia Seed removal rates bygranivorous animals have beenassessed in three localities all inArgentina A Andalgalaacute CatamarcaProvince Ntilde Ntildeacuntildeaacuten MendozaProvince P Puerto Madryn ChubutProvince

lagids were mutualists with food plants shared with antsperhaps storing some of the seeds of these plants in sur-face caches and thereby enhancing germination as hasbeen shown among North American heteromyid rodents(Mares and Rosenzweig 1978) After the extinction ofargyrolagids those plants would have suffered a decreasein their populations and the ant assemblages would alsohave declined in abundance and richness

Although these historical explanations about the role ofextinct argyrolagids cannot be tested directly they do leadto testable predictions about the status of present-day seedreserves in the Monte Desert (Mares and Rosenzweig1978 Brown and Ojeda 1987) For example the seeds con-sumed by present-day ants as well as those presumablyinvolved with marsupials in the past are predicted to beless abundant in seed banks of South American thanNorth American deserts (Marone and Horno 1997) Wetested this assertion by comparing seed reserves in wood-land and shrubland of the central Monte Desert with thosein several other South and North American deserts(Marone and Horno 1997) Densities of seeds in soil bankswere similar in arid North and South America at the habi-tat scale (Table 1) Regardless of continent most reportsfall within the range of 8000ndash30000 seedsm2 proposedby Kemp (1989) with the exception of one extraordinari-ly high value in the eastern Mojave Desert of California(Price and Joyner 1997)

Moreover with respect to production of seeds in SouthAmerica the few available data suggest seed productionrates similar to those in North America By using seedtraps to catch the seed rain during primary dispersal weestimated grass seed production in years of moderate rain-fall in the central Monte Desert to be 125 kgha (Maroneet al 1998a) Using similar methods Pulliam and Parker

(1979) and Pulliam and Dunning (1987) reported averagegrass seed production of 130ndash158 kgha in moderatelyrainy years in grasslands of the North American Chi-huahuan Desert of southeastern Arizona Finally seednumbers at the microhabitat scale as well as the propor-tion of small seeds (ie those presumably preferred byants) also appear to be similar in deserts of North andSouth America (Marone and Horno 1997) Overall thesefindings fail to support the hypothesis of a seed decline inthe South American sites Therefore differences in theresource base should not be invoked to account for differ-ences in granivorous assemblages (Mares and Rosenzweig1978) or in the foraging behavior of particular species(Medel and Vaacutesquez 1994) between South and NorthAmerican deserts Morton (1985 1993) also ruled out dif-ferences in the resource base as an explanation for differ-ences in granivorous assemblages between Australia andNorth America

Bait removal experimentsThe results of Mares and Rosenzweig (1978) on present-day consumption of seeds in the northern Monte Desertby different granivorous taxa in bait removal experimentsare still often extrapolated to the entire Monte Desert (egWurm 1998) To assess the applicability of those results tothe central Monte Desert (Figure 2) we therefore used thesame kinds of experiments in which seed consumption isestimated by comparing the amounts of seeds taken bydifferent taxa from feeding stations (dishes) placed in thedesert (Figure 3) There can be problems however incomparing results from bait removal experiments becausesuch experiments often lack standardized procedures Forinstance different authors have offered a variable assort-ment of seeds to granivores and have placed seed dishes

February 2000 Vol 50 No 2 BioScience 125

Articles

Desert General descriptionc Seed number (per m2) Seed mass (gm2) Reference

North AmericaSonora Shrubland dryndashrainy year 400ndash7700 Kemp 1989Mojave Shrubland dry year 430 05 Childs and Goodall 1973Mojave Shrubland dryndashrainy year 800ndash12100 05ndash52 Nelson and Chew 1977Mojave Shrubland 106000 380 Price and Joyner 1997Chihuahua Shrubland 13000ndash22000 Dye 1969Chihuahua Shrubland fine soils 8800ndash24500 Kemp 1989Chihuahua Shrubland coarse soils 1300ndash6000 Kemp 1989

South AmericaArid Chaco Open forest gt20000 Capurro and Bucher 1982Central Chile Thorn scrub seasonal 10700ndash23900 83ndash249 Meserve 1981bCentral Chile Matorral seasonal 13100ndash20500 Loacutepez-Calleja 1995Central Monte Open forest seasonal 14900ndash22900 36ndash60 Marone and Horno 1997Central Monte Shrubland seasonal 9300ndash15600 21ndash35 Marone and Horno 1997

aReprinted in modified form from Marone and Horno (1997) with permission of Academic PressbA single value for seed number or mass signifies an average calculated over several seasons or years Two numbers signify the extreme values of arangecThe habitat type and the contrasting conditions when the measurements were made are indicated where available These conditions account for theextreme values of each range (eg different seasons years or soil types)

Table 1a Average total seed number and seed mass in soil seed banks in different habitats from several South and NorthAmerican warm desertsb

among microhabitats in unspecified ways even thoughthe rate of seed consumption by mammals birds and antsmay differ with the type of seed (Kelrick et al 1986) or themicrohabitat (Lopez de Casenave et al 1998) Conse-quently researchers need to use caution when comparingseed removal rates quantitatively (Parmenter et al 1984Kelrick et al 1986 Vaacutesquez et al 1995)

Even when we used the most conservative measure ofseed consumption (ie the average seed removal rate inexposed microhabitats in which seed consumption bybirds and ants in the summer was significantly lower thanin microhabitats located under the canopy of shrubs andtrees) we found that the total rate of seed consumption inthe central Monte (Lopez de Casenave et al 1998) wasmore than five times greater than in the northern Monte(Mares and Rosenzweig 1978) Indeed if data from thecentral Monte Desert are incorporated into global com-parisons of the impact of desert granivores on seedresources the most logical conclusion appears to be thattotal granivory in the Monte is not abnormally depressed(Lopez de Casenave et al 1998) rather total seed removal aswell as seed removal by mammals and ants is exceptionallyhigh in North American deserts (see Morton 1985)

To avoid troublesome quantitative contrasts Vaacutesquez etal (1995) compared rankings of the relative importance ofmammals birds and ants among bait removal experi-ments worldwide We summarize their findings in Table 2adding our own results from the central Monte Desert as

well as an independent data set from the southern MonteDesert near Puerto Madryn Chubut Argentina (Figure 1Sergio L Saba Centro Nacional Patagoacutenico PuertoMadryn Chubut Argentina personal communication)Although these rankings show only the relative impacts ofevery taxa in every study site (ie they tell us nothingabout absolute granivory rates) they corroborate previousgeneralizations that the relative impact of mammals isgreater in northern continents and that the relative impactof ants is greater in southern continents The rankings alsoreveal a novel finding granivorous birds are major seedconsumers in several South American locations

The likely importance of seed-eating birds calls atten-tion to some underappreciated mechanisms of seed lossTo assess the similarities of the impact of granivores onseed resources in deserts around the world it is necessaryto simultaneou sly evaluate both seed availability and allplausible mechanisms of seed loss (which may vary amongdeserts even when total seed loss remains constant) Somemechanisms that have received far less attention thanmammal and ant consumption include avian granivoryseed germination and burial and seed mortality caused byfungi and bacteria These and other possible sources ofseed output should be carefully quantified before conjec-turing whether historical or ecological causes are morelikely to explain the organization of the seedndashgranivoresystem at regional and intercontinental scales (Kerley andWhitford 1994 Marone and Horno 1997)

Granivorous ant assemblagesResearchers have often assumed that assemblages ofgranivorous ants are substantially less diverse in aridSouth America than in similar habitats of North America(eg Mares et al 1977 Mares and Rosenzweig 1978Brown and Ojeda 1987 Holldobler and Wilson 1990) Forexample James Hunt (in Mares et al 1977) compared antcommunities of a Sonoran Desert site near Silver Bell Ari-zona and the northern Monte Desert site near AndalgalaacuteHe recorded a higher species richness of ants in total butfewer granivorous species at Andalgalaacute The granivore sta-tus of ants however was grounded not on direct foragingobservations but on assumptions based on taxonomy

When the granivore status of ants was defined accord-ing to foraging records however the conclusions changedMedel (1995) compared seed-harvester ant assemblages ofNorth America Australia and South America by usingseed removal experiments following the methods of Mor-ton and Davidson (1988) He sampled ants in 11 locationsin the central and northern Monte Desert includingAndalgalaacute and found that these assemblages were in factmore diverse and abundant than their North Americancounterparts (Medel and Vaacutesquez 1994 Medel 1995)Using the same method we assessed the composition ofseed-harvester ant assemblages in the central MonteDesert (Javier Lopez de Casenave Silvia Claver Viacutector RCueto Luis Marone unpublished data) In December

126 BioScience February 2000 Vol 50 No 2

Articles

Figure 2 The open Prosopis flexuosa woodland in theBiosphere Reserve of Ntildeacuntildeaacuten in the central Monte DesertArgentina We carried out fieldwork in open woodlands andin Larrea cuneifolia shrublands of the reserve between 1993and 1998 Ntildeacuntildeaacutenrsquos climate is dry and temperate with coldwinters and most annual rainfall occurs in springndashsummer(OctoberndashMarch) Perennial C4 grasses mainly of the generaTrichloris Pappophorum Setaria Sporobolus Digitariaand Aristida are abundant in both open woodland andshrubland Grass seed production and dispersal are mostlyrestricted to late summer and early autumn (Marone et al1998a)

1995 we recorded 12 and 14 species removing seeds fromtwo nearby sites This species richness exceeded the meanof 98 (n = 11 sites) and 28 (n = 5 sites) reported for thenorthern Monte Desert and central Chile respectively(Medel and Vaacutesquez 1994) as well as the mean of 52 (n =10 sites) and 85 (n = 16 sites) reported for North Ameri-can and Australian deserts respectively (Morton andDavidson 1988) In summary direct foraging observationof ants is not in agreement with previous assertions thatgranivorous ants are depauperate in the Monte Desert

The bait removal method employed in all these studiesis sensitive to the definition of ldquoharvester antrdquo used If antspecies are considered to be seed harvesters simply becausethey are seen at seed stations then the number of har-vester ant species may be overestimated By contrast wecounted only ants that effectively loaded seeds from seedstations Consequently we conclude that assemblages ofpotentially seed-harvesting ants are not depauperate atleast in the central Monte Desert

The South American ant assemblages however includeseveral species with more generalist diets than those of the

obligate seed-harvester ants of the genus Pogonomyrmexwhich make up the bulk of ant assemblages in NorthAmerican deserts Although Mares and Rosenzweig(1978) Medel (1995) and Medel and Vaacutesquez (1994) allhypothesized that omnivory of the ant species in SouthAmerican deserts results from a lower seed availability inthese deserts than in North American deserts the figuresin Table 1 do not support this explanation Indeed Pogon-omyrmex species exist in South America as well The threePogonomyrmex species (P rastratus P pronotalis and Pinermis) that occur in the central Monte Desert (Claverand Fowler 1993) appear to be highly specialized grani-vores (Javier Lopez de Casenave Silvia Claver Viacutector RCueto Luis Marone unpublished data) However giventhat the South American species of this genus seem to dis-play smaller colonies and lower population densities thanthose in North America (Holldobler and Wilson 1990) thehypothesis of a lower impact of South American Pogono-myrmex species on seeds (naturally available as well asoffered in baits) is a plausible although still unexploredhypothesis

February 2000 Vol 50 No 2 BioScience 127

Articles

Figure 3 A feeding station used in bait removalexperiments (Lopez de Casenave et al 1998) A known

amount of seeds is offered in each station at the start of thetrial Every station consists of three plastic Petri dishes (9cm in diameter) a ldquomammalrdquo tray a ldquobirdrdquo tray and an

ldquoantrdquo tray Vertebrate trays are glued to the top of longplastic cylinders and set 2ndash3 cm above the ground to

prevent access by ants Seeds for birds are available onlyduring the day and seeds for mammals are available only

at night Ant trays are buried with the rim of the Petri dishlevel with the soil surface and covered with mesh hardware

cloth to prevent access by vertebrates (these trays remainactive 24 hours a day) The stations are periodically

replenished with known amounts of seeds to avoidtotaldepletion (total duration of the experiment is 48 hours)

Region Granivore ranking Reference

North America (Sonora Desert) M gt A gt B Mares and Rosenzweig 1978Israel (Negev Desert) M gt Ac Abramsky 1983South Africa (Karoo Desert) A gt M gt B Kerley 1991Australia (Simpson Desert) A gt B gt M Morton 1985Chile (dense matorral) A gt B gt M Vaacutesquez et al 1995Chile (sparse matorral) B = A gt M Vaacutesquez et al 1995Argentina (central Monte Desert)

Under-canopy sites A gt B gt M Lopez de Casenave et al 1998Open sites B = A = M Lopez de Casenave et al 1998

Argentina (Southern Monte Desert) B gt M = A Sergio L Saba personalcommunication

Argentina (Northern Monte Desert) A gt B = M Mares and Rosenzweig 1978aExpanded from Vaacutesquez et al (1995)bAccording to Vaacutesquez et al (1995) we considered two taxa to have different granivory intensities when the average seed removal rate of one was at leasttwice that of the othercThis study was carried out only during springndashsummer birds were thought to have a negligible influence and were therefore not studied

Table 2a Rankings of the relative importance of the three main granivore taxa (A ants B birds M small mammals) assuggested by bait removal experiments carried out in different arid regions of the worldb

Low population densities of Pogonomyrmex ants andgeneralized food habits among some other ant speciesmight explain why the Monte Desertrsquos granivorous antsappear to remove fewer seeds from experimental baitsthan do North American ants But it does not follow thatthe ants of the Monte Desert ldquoare depauperate and notusually granivorousrdquo (Mares and Rosenzweig 1978) Tounderstand whether differences in seed removal from arti-ficial baits reflect intercontinental differences in antgranivory it will be necessary to examine more closely theforaging behavior of the Monte Desertrsquos ants For examplepreliminary observations indicate that some Pogono-myrmex species of the Monte Desert harvest the majorityof their seeds directly from plant stalks At the same timethe frequency of individuals of these highly specializedseed-eating species was very low at experimental seed sta-tions located on the soil (Javier Lopez de Casenave SilviaClaver Viacutector R Cueto Luis Marone unpublished data)Subtle differences in ant foraging behavior among conti-nents might reduce the comparability of results from thiskind of experiment thus affecting the conclusions aboutthe importance of granivorous ants as seed harvesters

Studies of seed removal from bait stations and of foodhabits of putative granivorous animals are necessary butnot sufficient to make inferences about the communityrole of granivores One straightforward approach to deter-mine the community role of those animals is to directlyassess the extent to which the dynamics of the resource(ie seeds) is affected by the activity of the consumer (iebirds ants or mammals) That is the importance ofgranivory can be better addressed through mechanismicstudies of the effects of seed consumption on the fate ofnaturally dispersed seeds (Price and Joyner 1997 Maroneet al 1998b)

Granivorous mammal assemblagesThe absence of functional analogues of North Americarsquosheteromyid rodents and the low diversity and abundanceof other mammalian granivores in South Americandeserts have been blamed for the ldquoinsignificantrdquo mam-malian seed consumption recorded in the northern MonteDesert (Mares et al 1977 Mares and Rosenzweig 1978Brown and Ojeda 1987) Recent studies however suggestthat this rate of seed consumption does not apply to theentire Monte Desert rodents remove almost an order ofmagnitude more seeds in the central Monte Desert than inthe northern Monte Desert (Lopez de Casenave et al1998) Mammalian seed removal is also markedly higherin the southern Monte than in Andalgalaacute (Sergio L Sabapersonal communication) Thus even if South Americatruly lacks analogues of heteromyids the premise thatrodent granivory is insignificant in the Monte Desert over-all deserves scrutiny for at least two reasons

First the spacious cheek pouches of heteromyidsenhance their fabled proficiency at gathering and hoard-ing seeds In a study of several heteromyid species indi-

viduals on average filled their cheek pouches to more than90 of pouch capacity during a single feeding bout in thefield (Vander Wall et al 1997) On a daily basis thereforethese rodents may harvest far more seeds than they needto fulfill their immediate energy requirements Althoughsome South American rodents have been shown to hoardsome seeds at least under laborator y conditions (Vaacutesquez1996) these species lack cheek pouches (Nowak and Par-adiso 1983) It follows that on average South Americanrodents would be expected to harvest fewer seeds frombaits than do heteromyids Some indirect evidence seemsto corroborate this assertion Predavecrsquos (1997) estimatesof seed consumption by Australian desert rodents (whichlike South American rodents lack cheek pouches) weredramatically higher when based on calculations of ener-getics than when based on bait removal experiments

Another reason for caution with previous generaliza-tions about mammal granivory in South America is thatbasic dietary information is still lacking for South Ameri-can desert rodents and desert ecologists often disagreeabout their food habits Although this discrepancy some-times simply reflects the fact that the proportion of seedsin animalsrsquo diets varies widely in time and space disagree-ment is also fostered by the lack of dietary informationThis lack of information is a major problem because somecalculatio ns of seed consumption (eg those based onenergetics) are sensitive to subtle variations in dietary val-ues (Kerley 1992) Hence terms such as ldquogranivorerdquo arenot always used in a consistent way Strictly speaking aselective consumer (eg a granivorous mammal) is ananimal that takes some or all food items in different pro-portions than the proportions at which they are present inthe patches where the animal feeds within the size limitsimposed by the perceptive handling and swallowingcapabilities of the consumer (Jaksic 1989)

Because this definition is difficult to apply in natureother more rudimentary ones could be used providedthat they are used only as a basis of comparative assess-ments For example Kerley and Whitford (1994) suggest-ed that mammals can be designated as granivores folivoresor insectivores when their diets are dominated by therespective dietary category (ie more than 50 of the dietconsists of the category) whereas those of more mixed dietscan be termed omnivores Using this criterion Meserve(1981a) showed that two rodent species in the southernfringe of the Atacama Desert of Chile Oligoryzomys longi-caudatus and Phyllotis darwini were granivorous especiallyin the dry season when 73 and 59 respectively of theiridentified diets consisted of seeds Abrothrix (Akodon) oli-vaceus almost achieved granivore status with 45 of itsdiet consisting of seeds Similarly Pizzimenti and De Salle(1980) found that in several localities of the Andes ofsouthern Peruacute more than 50 of the diet of some rodentspecies consisted of seeds (eg Phyllotis darwini 53 Ppictus 60) Given that some heteromyid rodents that areusually considered specialized seedeaters also consume sig-

128 BioScience February 2000 Vol 50 No 2

Articles

nificant amounts of insects and green vegetation duringsome seasons (Mares 1993a) it appears that some of theabove-mentioned Atacama and Altiplano rodent speciesshould also be considered granivores

In the Monte Desert Mares et al (1977) and Mares(1993b) reported finding no granivorous small mammalsIn some localities of the central Monte Desert howeverCalomys musculinus may be the most abundant rodentspecies (Ojeda 1989) and data from other semi-arid habi-tats of Argentina show that the dry-season diet of C mus-culinus consists of approximately 90 seeds (Dellafioreand Polop 1994) In a recent study in the central MonteDesert Campos (1997) found that during the dry seasonC musculinus appeared to consume a relatively high pro-portion of seeds (50) and that the diets of other smallmammals included few seeds (less than 5 in the diets ofGraomys griseoflavus Eligmodontia typus Thylamys pusil-lus and Akodon molinae) However these low values mayseverely underestimate the proportion of seeds in the dietof C musculinus and the other small mammals FirstCampos (1997) indicated that the microhistological tech-nique that she had employed underestimates food itemsother than leavesmdashin particular seeds Second Campos(1997) tallied seeds in stomach contents by counting onlythe glume remains of grass diaspores however rodentsoften dehusk grass diaspores and discard the glume beforeconsumption (Martha J Piantanida Divisioacuten Mastozo-ologiacutea Museo Argentino de Ciencias Naturales BuenosAires Argentina personal communication) Finallyrodents consume forb seeds as well as grass seeds Forinstance 43 of the diet of C musculinus in west-centralArgentina consists of Chenopodium seeds and 22 of itconsists of Amaranthus seeds (Dellafiore and Polop 1994)

North American species of the heteromyid generaMicrodipodops and Dipodomys are usually labeled as spe-cialized granivores (eg Kelt et al 1996) Neverthelessthey also consume insects and green vegetation (Mares1993a Kerley and Whitford 1994) Moreover Kerley et al(1997) have proposed that the keystone status of kangaroorats in the Chihuahuan Desert might be due tograminivory (ie herbivory) rather than to granivory Bycontrast those South American rodents (eg several Olig-oryzomys Calomys and Phyllotis species) that appear todisplay similar seasonal changes in diet (granivorous atsome times herbivorousinsectivorous at others) arealmost never labeled ldquogranivoresrdquo in the literature

This semantic inconsistency which has implications forthe conclusions of comparative studies may reflect anunfortunate attribute of research practice that deserves thescrutiny of the sociologists of science when basic empiri-cal information on a particular subject is lacking or frag-mentary unproven assertions may gain credence as factseven though such assertions are only at best plausibleassumptions This problem however should fade awaywhen these basic assumptions (eg that the ability ofrodents to harvest clumped seeds is similar in North andSouth America or that the incidence of seeds in the diet ofSouth American rodents is negligible) are carefully testedbefore deciding about the suitability of the specifichypothesis under scrutiny (eg that seed-eating mammalsin the Monte Desert and other South American desertshave a significant impact on seed reserves) This researchstrategy is essential to preventing ldquonaive refutationismrdquo(Lakatos 1978) in which a specific hypothesis is consid-ered false simply by the refutation of just one of its pre-dictions (eg that South American small mammalsremove similar amounts of seeds offered in bait experi-ments as their North American counterparts)

Granivorous bird assemblagesThe low rates of seed removal by birds observed in baitremoval experiments seemed to suggest that birds areeither unimportant seedeaters in deserts or that they fail todetect the experimentally proffered trays For examplebirds ate few of the test seeds in the South African Karoo(Kerley 1991) the Chihuahuan Desert (Parmenter et al1984) and the Australian Desert (Morton 1985) Giventhe diverse and abundant avian granivores of Australiandeserts Morton (1985 1993) conjectured that these birdsshould have a major community role in Australian desertseven though they did not visit any of his seed stations Sev-eral authors have suggested that the short time span of baitremoval experiments (2ndash3 days) may be inadequate for

February 2000 Vol 50 No 2 BioScience 129

Articles

Figure 4 Seasonal rates of seed removal by granivores inthe central Monte Desert Birds open circles ants solid

circles mammals open triangles Mean rates of removalfor the 23ndash25 trays available only to the respective taxonare shown Within a season means with the same letter

are not significantly different according to Tukeyrsquos test ( Plt 005) Figure redrawn from Lopez de Casenave et al

(1998) and used with permission from Blackwell Science

measuring seed consumption by desert birds (Mares andRosenzweig 1978 Morton 1985)

In most bait experiments carried out in South Americandeserts however avian granivores quickly discovered baitsand consumed seeds Indeed birds often consumed moreseeds than did the other granivore taxa (Table 2) We knowof no idiosyncratic characteristic of South American birdsthat may explain this pattern Thus to control for anypropensity of the Monte avifauna to detect seed trays withunusual skills we used an approach that did not rely on arti-ficial baits to assess whether birds are important seedeatersin the central Monte Desert (Marone et al 1998b)

Bait experiments have shown that bird granivores arethe main autumnndashwinter seed consumers in the centralMonte Desert (Figure 4 see Lopez de Casenave et al1998) To assess the impact of seed-eating birds on theautumnndashwinter soil seed reserves we compared the soilseed bank in the late summer of 1995 (12 February) withthat present the following early spring (25 October) alsotaking into account the total number of seeds that enteredthe soil from late summer to early spring (ie we mea-sured seed rain Marone et al 1998b) In late summerbefore consumption by birds the mean seed density ofgrass seed banks was 2400 seedsm2 or 036 gm2 The nextspringmdashfollowing the input of approximately 3000 grassseedsm2 or 071 gm2 as well as the period of bird con-sumption in autumn and wintermdashthe density of grassseeds was 2700 seedsm2 or 039 gm2 Medium and largegrass seeds suffered higher postdispersal losses than didsmall seeds Likewise densities of forb seeds in the seedbank were statistically indistinguishable between late sum-mer (5500 seedsm2 or 134 gm2) and spring (6500seedsm2 or 153 gm2) although forb seed productionduring the study period had been relatively low (400seedsm2 or 012 gm 2) These results suggest thatautumnndashwinter seed predators in the central MonteDesert favor grass seeds over forb seeds

Several lines of evidence confirm that postdispersalgrass seed loss during autumnndashwinter in the centralMonte Desert is due mainly to vertebrate consumptionFirst granivorous ants are active almost exclusively during

the spring and summer (Figure 4 Lopez de Casenave et al1998) Furthermore C4 grasses germinate mostly in latespring and summer and total grass seed germinationwhich usually does not surpass 05 of previous soil seedreserves (Marone et al 1998b) reached only 5 of previ-ous reserves during the exceptionally wet summer of 1998which was associated with a strong El NintildeoSouthernOscillation event (Luis Marone Manuel E Horno RafaelGonzaacutelez del Solar unpublished data) Finally given thecomposition of the seed bank at different depths (0ndash2 cm2ndash4 cm and 4ndash6 cm) Marone et al (1998a) concludedthat grass seeds especially the medium and large seedswould suffer negligible loss by deep burial

Therefore it was not surprising that the pattern of seedlosses coincided with the pattern of seed consumption bygranivorous birds in the autumns and winters of 1993through 1995 Nearly 93 of the seed mass in bird stom-achs came from grass seeds and only 7 came from forbseeds Furthermore medium and large grass seeds sufferedthe highest losses from the soil seed bank and were also themain target of foraging by granivores Moreover a signifi-cant positive correlation existed across grass speciesbetween the mass decrease of seed species from the soiltoward spring and the mass of those seed species in birddiets in autumnndashwinter (Figure 5 Marone et al 1998b)This positive correlation suggests that bird consumptioncould explain a great deal of the autumnndashwinter grass seedloss observed in soils of the central Monte Desert

These lines of evidence indicate that vertebrate grani-vores (particularly birds) have a major impact on theabundance floristic composition and size distribution ofseed reserves in the Monte Desert where vertebrategranivory in general and avian granivory in particularhad previously been considered unimportant Moreovernewly produced seeds from perennial grasses constitute amajor fraction of autumnndashwinter bird diet This findingsupports the proposal (Marone 1992) that the timing andamount of rainfall in the central Monte Desert may great-ly influence the abundance and migrations of granivorousbirds via the opportunistic response of seed production bygrasses to variations in rainfall Population interactions

130 BioScience February 2000 Vol 50 No 2

Articles

Figure 5 Relationship between the mass of seeds fromperennial grasses in the autumn and winter diets (in1993ndash1995) of four granivorous bird species in the centralMonte Desert and the loss of seeds of each species during theautumn and winter of 1995 The bird species are Zonotrichiacapensis Phrygilus carbonarius Diuca diuca andSaltatricula multicolor The overall correlation wassignificant (r = 087 n = 11 P lt 0001) Grass species are asfollows Pap Pappophorum spp Set Setaria leucopila DigDigitaria californica Tri Trichloris crinita Dip Diplachnedubia Spo Sporobolus cryptandrus Ari Aristida spp NeoNeobouteloua lophostachya Chl Chloris castilloniana BouBouteloua spp The point for Stipa spp is not shown on thefigure but overlaps with that for Bouteloua spp

between seeds and avian granivores in this South Ameri-can desert may therefore be more important than hithertoappreciated

Concluding remarksThe relative importance of seed consumption or granivo-rous assemblages in deserts around the world cannot beassessed through one research approach alone (eg baitremoval experiments energetics approaches descriptionsof the species composition of granivorous assemblages orquantification of individualsrsquo diets) Instead research pro-grams that include multiple approaches involving redun-dancy and cross-checks of hypotheses and methods maylead to the most robust conclusions and therefore to syn-thesis and integration (Pickett et al 1994) Furthermoreany such program should involve long-term studies thattake into account the spatial and temporal variability ofnatural communities

Partly as a consequence of such a lack of integrationnatural rates of seed consumption and the abundance anddiversity of granivorous assemblages in some South Amer-ican deserts may have been underestimated in the pastThe evidence we have discussed in this article comes fromvarious desert locations of southern South America andwas obtained by using different research approaches Thisevidence suggests that birds and ants are importantseedeaters during the colder and warmer months respec-tively and that the role of small mammals as granivores inthe central Monte Desert of Argentina deserves moredetailed assessment These results should be readily incor-porated into comparative studies to distinguish betweenidiosyncratic and general processes molding desert com-munities worldwide Although ecological ldquolawsrdquo are by nomeans universal ecological understanding will continueto depend on theory development (Pickett et al 1994Mahner and Bunge 1997) To develop ecological theoryresearchers need good observations combined with rigor-ous and realistic experiments carried out in the context ofresearch programs that are focused whenever possible ontesting mechanisms to account for ecological phenomena(Werner 1998)

AcknowledgmentsWe acknowledge Sergio Camiacuten Silvia Claver RafaelGonzaacutelez del Solar Fernando Milesi Martha J PiantanidaBertilde Rossi Eduardo Tomaacutes-Mezquida and GualbertoZalazar for their constructive and pleasant cooperationduring field and laborator y work Manuel E Horno andIris Peralta contributed partnership and stimulating dis-cussion at the initial (and more chaotic) stages of ourstudies we are especially indebted to both of them SergioL Saba was kind enough to let us use his unpublisheddata First drafts of the manuscript were greatly improvedthrough critical review from Rebecca Chasan Chris Dick-man Pete Feinsinger Lali Guichoacuten Rafael Gonzaacutelez delSolar Fabiaacuten Jaksic Graham Kerley Fernando Milesi

Stephen Morton Mary V Price Julian Reid AlejandraRibichich Rodrigo Vaacutesquez and four anonymous review-ers At different stages field and laboratory work werefinanced by the Man and the Biosphere Programme Unit-ed Nations Educational Scientific and Cultural Organiza-tion the Association of Field Ornithologists Programa deCiencias Naturales Museo Argentino de Ciencias Natu-rales ldquoBernardino Rivadaviardquo IADIZA-Provincia de Men-doza and the Argentine funding agencies CONICET (PEI032797) and Agencia Nacional de Promocioacuten Cientiacutefica yTecnoloacutegica (PICT 01-03187) L M acknowledges CON-ICET and the Canadian Government for financial sup-port and Mario Bunge for the stimulating environment atMcGill University where the final version of this paperwas written This article is Contribution No 8 of theDesert Community Ecology Research Team Plant Eco-physiology Department IADIZA Institute

References citedAbramsky Z 1983 Experiments on seed predation by rodents and ants in

the Israeli desert Oecologia 57 328ndash332

Brown JH Ojeda RA 1987 Granivory Patterns processes and conse-

quences of seed consumption on two continents Revista Chilena de

Historia Natural 60 337ndash349

Campos CM 1997 Utilizacioacuten de recursos alimentarios por mamiacuteferos

medianos y pequentildeos del desierto del Monte PhD dissertation Uni-

versidad Nacional de Coacuterdoba Coacuterdoba Argentina

Capurro HA Bucher EH 1982 Poblaciones de aves graniacutevoras y disponi-

bilidad de semillas en el bosque chaquentildeo de Chamical Ecosur 9

117ndash131

Childs S Goodall DW 1973 Seed reserves of desert soils Logan (UT)

Utah State University USIBP Desert Biome Research Memorandum

73-5

Claver S Fowler HG 1993 The ant fauna (Hymenoptera Formicidae) of

the Ntildeacuntildeaacuten Biosphere Reserve Naturalia 18 189ndash193

Dellafiore CM Polop JJ 1994 Feeding habits of Calomys musculinus in the

crop fields and its borders Mastozoolog iacutea Neotropical (Argentina) 1

45ndash50

Dye AJ 1969 Germination potentials and accumulation of native plant

seeds from southern New Mexico Masterrsquos thesis New Mexico State

University Las Cruces NM

Holldobler B Wilson EO 1990 The Ants Cambridge (MA) Harvard Uni-

versity Press

Jaksic FM 1989 Opportunist selective and other often-confused terms in

the predation literature Revista Chilena de Historia Natural 62 7ndash8

Kelrick MI MacMahon JA Parmenter RR Sisson DV 1986 Native seed

preferences of shrubndashsteppe rodents birds and ants The relationships

of seed attributes and seed use Oecologia 68 327ndash337

Kelt DA Brown JH Heske EJ Marquet PA Morton SR Reid JRW Rogovin

KA Shenbrot G 1996 Community structure of desert small mam-

mals Comparisons across four continents Ecology 77 746ndash761

Kemp PR 1989 Seed bank and vegetation processes in deserts Pages

257ndash281 in Allessio-Leck M Parker VT Simpson RL eds Ecology of

Soil Seed Banks San Diego (CA) Academic Press

Kerley GIH 1991 Seed removal by rodents birds and ants in the semi-arid

Karoo South Africa Journal of Arid Environments 20 63ndash69

______ 1992 Small mammal seed consumption in the Karoo South

Africa Further evidence for divergence in desert biotic processes

Oecologia 89 471ndash475

Kerley GIH Whitford WG 1994 Desert-dwelling small mammals as grani-

vores Intercontinental variations Australian Journal of Zoology 42

543ndash555

Kerley GIH Whitford WG Kay FR 1997 Mechanisms for the keystone sta-

February 2000 Vol 50 No 2 BioScience 131

Articles

empirical information (Mares 1993a) For example Maresand Rosenzweig (1978) Abramsky (1983) and Morton(1985) all asserted that total granivory in the extensiveMonte Desert of Argentina is depressed and granivorousassemblages depauperate in comparison with other warmtemperate deserts However this conclusion was derivedfrom a single experiment carried out near Andalgalaacute inthe far northern reaches of the Monte Desert (Figure 1Mares and Rosenzweig 1978) Despite the narrow domainof this study many scientists have tacitly extended its con-clusions to arid South America as a whole (Abramsky1983 Morton 1985 1993 Brown and Ojeda 1987 Kerley1991 Wurm 1998 but see Vaacutesquez et al 1995 Lopez deCasenave et al 1998)

In this article we summarize current evidence about theresource base of granivorous animals the pressures theseanimals impose on seed reserves and the main ecologicalfeatures of the assemblages of seed-eating ants mammalsand birds in the Monte Desert and other southern SouthAmerican deserts We examine the general validity of thecommonly accepted patterns of granivory by using multi-ple research approaches to verify pattern robustness If the

patterns are robust they should be thebasis for more reliable tests of thecommunity convergence hypothesisof granivorous assemblages in desertsfrom different continents Such testscould provide a more informedassessment of the relative roles of localecological processes and unique his-torical circumstances in organizingdesert communities

The resource baseMares and Rosenzweig (1978) ob-served that ldquototal granivory is much

depressed in the Monte Desert where granivorous mam-mals are rare and ill-adapted ants are depauperate and notusually granivorous and birds are unimportant seed con-sumersrdquo and they suggested that low granivory would bethe consequence of a seed decline in South Americandeserts caused by the relatively recent extinction of themarsupial family Argyrolagidae in South America Maresand Rosenzweig (1978) assumed that argyrolagids wereecological equivalents of the rodents of the North Ameri-can family Heteromyidae (Saacutenchez-Villagra and Kay1997) and they outlined two alternative evolutionary sce-narios whereby marsupial extinction might have led to adecline in granivorous assemblages (particularly of ants)via a decrease in their resource base (ie seeds) In the firstalternative argyrolagids were indirect evolutionary mutu-alists with ants consuming seeds not preferred by antsThus when the argyrolagids became extinct ant-preferredplants whose seeds were still consumed would have beenoutcompeted by predator-free ant-avoided plants Thedecreased availability of seeds from ant-preferred plantswould have led in turn to a decline in the granivorous antassemblages themselves In the second scenario argyro-

124 BioScience February 2000 Vol 50 No 2

Articles

Figure 1 The Monte Desert inperspective (top) The worldrsquos desertregions including some semi-aridareas that are not generallyconsidered true deserts are indicatedby shading (inset) The Monte Desertin southern South America is arelatively narrow northndashsouth beltthat is oriented along the easternslopes of the Andes Mountains Itbroadens to the south and extends tothe Atlantic coast in northernPatagonia Seed removal rates bygranivorous animals have beenassessed in three localities all inArgentina A Andalgalaacute CatamarcaProvince Ntilde Ntildeacuntildeaacuten MendozaProvince P Puerto Madryn ChubutProvince

lagids were mutualists with food plants shared with antsperhaps storing some of the seeds of these plants in sur-face caches and thereby enhancing germination as hasbeen shown among North American heteromyid rodents(Mares and Rosenzweig 1978) After the extinction ofargyrolagids those plants would have suffered a decreasein their populations and the ant assemblages would alsohave declined in abundance and richness

Although these historical explanations about the role ofextinct argyrolagids cannot be tested directly they do leadto testable predictions about the status of present-day seedreserves in the Monte Desert (Mares and Rosenzweig1978 Brown and Ojeda 1987) For example the seeds con-sumed by present-day ants as well as those presumablyinvolved with marsupials in the past are predicted to beless abundant in seed banks of South American thanNorth American deserts (Marone and Horno 1997) Wetested this assertion by comparing seed reserves in wood-land and shrubland of the central Monte Desert with thosein several other South and North American deserts(Marone and Horno 1997) Densities of seeds in soil bankswere similar in arid North and South America at the habi-tat scale (Table 1) Regardless of continent most reportsfall within the range of 8000ndash30000 seedsm2 proposedby Kemp (1989) with the exception of one extraordinari-ly high value in the eastern Mojave Desert of California(Price and Joyner 1997)

Moreover with respect to production of seeds in SouthAmerica the few available data suggest seed productionrates similar to those in North America By using seedtraps to catch the seed rain during primary dispersal weestimated grass seed production in years of moderate rain-fall in the central Monte Desert to be 125 kgha (Maroneet al 1998a) Using similar methods Pulliam and Parker

(1979) and Pulliam and Dunning (1987) reported averagegrass seed production of 130ndash158 kgha in moderatelyrainy years in grasslands of the North American Chi-huahuan Desert of southeastern Arizona Finally seednumbers at the microhabitat scale as well as the propor-tion of small seeds (ie those presumably preferred byants) also appear to be similar in deserts of North andSouth America (Marone and Horno 1997) Overall thesefindings fail to support the hypothesis of a seed decline inthe South American sites Therefore differences in theresource base should not be invoked to account for differ-ences in granivorous assemblages (Mares and Rosenzweig1978) or in the foraging behavior of particular species(Medel and Vaacutesquez 1994) between South and NorthAmerican deserts Morton (1985 1993) also ruled out dif-ferences in the resource base as an explanation for differ-ences in granivorous assemblages between Australia andNorth America

Bait removal experimentsThe results of Mares and Rosenzweig (1978) on present-day consumption of seeds in the northern Monte Desertby different granivorous taxa in bait removal experimentsare still often extrapolated to the entire Monte Desert (egWurm 1998) To assess the applicability of those results tothe central Monte Desert (Figure 2) we therefore used thesame kinds of experiments in which seed consumption isestimated by comparing the amounts of seeds taken bydifferent taxa from feeding stations (dishes) placed in thedesert (Figure 3) There can be problems however incomparing results from bait removal experiments becausesuch experiments often lack standardized procedures Forinstance different authors have offered a variable assort-ment of seeds to granivores and have placed seed dishes

February 2000 Vol 50 No 2 BioScience 125

Articles

Desert General descriptionc Seed number (per m2) Seed mass (gm2) Reference

North AmericaSonora Shrubland dryndashrainy year 400ndash7700 Kemp 1989Mojave Shrubland dry year 430 05 Childs and Goodall 1973Mojave Shrubland dryndashrainy year 800ndash12100 05ndash52 Nelson and Chew 1977Mojave Shrubland 106000 380 Price and Joyner 1997Chihuahua Shrubland 13000ndash22000 Dye 1969Chihuahua Shrubland fine soils 8800ndash24500 Kemp 1989Chihuahua Shrubland coarse soils 1300ndash6000 Kemp 1989

South AmericaArid Chaco Open forest gt20000 Capurro and Bucher 1982Central Chile Thorn scrub seasonal 10700ndash23900 83ndash249 Meserve 1981bCentral Chile Matorral seasonal 13100ndash20500 Loacutepez-Calleja 1995Central Monte Open forest seasonal 14900ndash22900 36ndash60 Marone and Horno 1997Central Monte Shrubland seasonal 9300ndash15600 21ndash35 Marone and Horno 1997

aReprinted in modified form from Marone and Horno (1997) with permission of Academic PressbA single value for seed number or mass signifies an average calculated over several seasons or years Two numbers signify the extreme values of arangecThe habitat type and the contrasting conditions when the measurements were made are indicated where available These conditions account for theextreme values of each range (eg different seasons years or soil types)

Table 1a Average total seed number and seed mass in soil seed banks in different habitats from several South and NorthAmerican warm desertsb

among microhabitats in unspecified ways even thoughthe rate of seed consumption by mammals birds and antsmay differ with the type of seed (Kelrick et al 1986) or themicrohabitat (Lopez de Casenave et al 1998) Conse-quently researchers need to use caution when comparingseed removal rates quantitatively (Parmenter et al 1984Kelrick et al 1986 Vaacutesquez et al 1995)

Even when we used the most conservative measure ofseed consumption (ie the average seed removal rate inexposed microhabitats in which seed consumption bybirds and ants in the summer was significantly lower thanin microhabitats located under the canopy of shrubs andtrees) we found that the total rate of seed consumption inthe central Monte (Lopez de Casenave et al 1998) wasmore than five times greater than in the northern Monte(Mares and Rosenzweig 1978) Indeed if data from thecentral Monte Desert are incorporated into global com-parisons of the impact of desert granivores on seedresources the most logical conclusion appears to be thattotal granivory in the Monte is not abnormally depressed(Lopez de Casenave et al 1998) rather total seed removal aswell as seed removal by mammals and ants is exceptionallyhigh in North American deserts (see Morton 1985)

To avoid troublesome quantitative contrasts Vaacutesquez etal (1995) compared rankings of the relative importance ofmammals birds and ants among bait removal experi-ments worldwide We summarize their findings in Table 2adding our own results from the central Monte Desert as

well as an independent data set from the southern MonteDesert near Puerto Madryn Chubut Argentina (Figure 1Sergio L Saba Centro Nacional Patagoacutenico PuertoMadryn Chubut Argentina personal communication)Although these rankings show only the relative impacts ofevery taxa in every study site (ie they tell us nothingabout absolute granivory rates) they corroborate previousgeneralizations that the relative impact of mammals isgreater in northern continents and that the relative impactof ants is greater in southern continents The rankings alsoreveal a novel finding granivorous birds are major seedconsumers in several South American locations

The likely importance of seed-eating birds calls atten-tion to some underappreciated mechanisms of seed lossTo assess the similarities of the impact of granivores onseed resources in deserts around the world it is necessaryto simultaneou sly evaluate both seed availability and allplausible mechanisms of seed loss (which may vary amongdeserts even when total seed loss remains constant) Somemechanisms that have received far less attention thanmammal and ant consumption include avian granivoryseed germination and burial and seed mortality caused byfungi and bacteria These and other possible sources ofseed output should be carefully quantified before conjec-turing whether historical or ecological causes are morelikely to explain the organization of the seedndashgranivoresystem at regional and intercontinental scales (Kerley andWhitford 1994 Marone and Horno 1997)

Granivorous ant assemblagesResearchers have often assumed that assemblages ofgranivorous ants are substantially less diverse in aridSouth America than in similar habitats of North America(eg Mares et al 1977 Mares and Rosenzweig 1978Brown and Ojeda 1987 Holldobler and Wilson 1990) Forexample James Hunt (in Mares et al 1977) compared antcommunities of a Sonoran Desert site near Silver Bell Ari-zona and the northern Monte Desert site near AndalgalaacuteHe recorded a higher species richness of ants in total butfewer granivorous species at Andalgalaacute The granivore sta-tus of ants however was grounded not on direct foragingobservations but on assumptions based on taxonomy

When the granivore status of ants was defined accord-ing to foraging records however the conclusions changedMedel (1995) compared seed-harvester ant assemblages ofNorth America Australia and South America by usingseed removal experiments following the methods of Mor-ton and Davidson (1988) He sampled ants in 11 locationsin the central and northern Monte Desert includingAndalgalaacute and found that these assemblages were in factmore diverse and abundant than their North Americancounterparts (Medel and Vaacutesquez 1994 Medel 1995)Using the same method we assessed the composition ofseed-harvester ant assemblages in the central MonteDesert (Javier Lopez de Casenave Silvia Claver Viacutector RCueto Luis Marone unpublished data) In December

126 BioScience February 2000 Vol 50 No 2

Articles

Figure 2 The open Prosopis flexuosa woodland in theBiosphere Reserve of Ntildeacuntildeaacuten in the central Monte DesertArgentina We carried out fieldwork in open woodlands andin Larrea cuneifolia shrublands of the reserve between 1993and 1998 Ntildeacuntildeaacutenrsquos climate is dry and temperate with coldwinters and most annual rainfall occurs in springndashsummer(OctoberndashMarch) Perennial C4 grasses mainly of the generaTrichloris Pappophorum Setaria Sporobolus Digitariaand Aristida are abundant in both open woodland andshrubland Grass seed production and dispersal are mostlyrestricted to late summer and early autumn (Marone et al1998a)

1995 we recorded 12 and 14 species removing seeds fromtwo nearby sites This species richness exceeded the meanof 98 (n = 11 sites) and 28 (n = 5 sites) reported for thenorthern Monte Desert and central Chile respectively(Medel and Vaacutesquez 1994) as well as the mean of 52 (n =10 sites) and 85 (n = 16 sites) reported for North Ameri-can and Australian deserts respectively (Morton andDavidson 1988) In summary direct foraging observationof ants is not in agreement with previous assertions thatgranivorous ants are depauperate in the Monte Desert

The bait removal method employed in all these studiesis sensitive to the definition of ldquoharvester antrdquo used If antspecies are considered to be seed harvesters simply becausethey are seen at seed stations then the number of har-vester ant species may be overestimated By contrast wecounted only ants that effectively loaded seeds from seedstations Consequently we conclude that assemblages ofpotentially seed-harvesting ants are not depauperate atleast in the central Monte Desert

The South American ant assemblages however includeseveral species with more generalist diets than those of the

obligate seed-harvester ants of the genus Pogonomyrmexwhich make up the bulk of ant assemblages in NorthAmerican deserts Although Mares and Rosenzweig(1978) Medel (1995) and Medel and Vaacutesquez (1994) allhypothesized that omnivory of the ant species in SouthAmerican deserts results from a lower seed availability inthese deserts than in North American deserts the figuresin Table 1 do not support this explanation Indeed Pogon-omyrmex species exist in South America as well The threePogonomyrmex species (P rastratus P pronotalis and Pinermis) that occur in the central Monte Desert (Claverand Fowler 1993) appear to be highly specialized grani-vores (Javier Lopez de Casenave Silvia Claver Viacutector RCueto Luis Marone unpublished data) However giventhat the South American species of this genus seem to dis-play smaller colonies and lower population densities thanthose in North America (Holldobler and Wilson 1990) thehypothesis of a lower impact of South American Pogono-myrmex species on seeds (naturally available as well asoffered in baits) is a plausible although still unexploredhypothesis

February 2000 Vol 50 No 2 BioScience 127

Articles

Figure 3 A feeding station used in bait removalexperiments (Lopez de Casenave et al 1998) A known

amount of seeds is offered in each station at the start of thetrial Every station consists of three plastic Petri dishes (9cm in diameter) a ldquomammalrdquo tray a ldquobirdrdquo tray and an

ldquoantrdquo tray Vertebrate trays are glued to the top of longplastic cylinders and set 2ndash3 cm above the ground to

prevent access by ants Seeds for birds are available onlyduring the day and seeds for mammals are available only

at night Ant trays are buried with the rim of the Petri dishlevel with the soil surface and covered with mesh hardware

cloth to prevent access by vertebrates (these trays remainactive 24 hours a day) The stations are periodically

replenished with known amounts of seeds to avoidtotaldepletion (total duration of the experiment is 48 hours)

Region Granivore ranking Reference

North America (Sonora Desert) M gt A gt B Mares and Rosenzweig 1978Israel (Negev Desert) M gt Ac Abramsky 1983South Africa (Karoo Desert) A gt M gt B Kerley 1991Australia (Simpson Desert) A gt B gt M Morton 1985Chile (dense matorral) A gt B gt M Vaacutesquez et al 1995Chile (sparse matorral) B = A gt M Vaacutesquez et al 1995Argentina (central Monte Desert)

Under-canopy sites A gt B gt M Lopez de Casenave et al 1998Open sites B = A = M Lopez de Casenave et al 1998

Argentina (Southern Monte Desert) B gt M = A Sergio L Saba personalcommunication

Argentina (Northern Monte Desert) A gt B = M Mares and Rosenzweig 1978aExpanded from Vaacutesquez et al (1995)bAccording to Vaacutesquez et al (1995) we considered two taxa to have different granivory intensities when the average seed removal rate of one was at leasttwice that of the othercThis study was carried out only during springndashsummer birds were thought to have a negligible influence and were therefore not studied

Table 2a Rankings of the relative importance of the three main granivore taxa (A ants B birds M small mammals) assuggested by bait removal experiments carried out in different arid regions of the worldb

Low population densities of Pogonomyrmex ants andgeneralized food habits among some other ant speciesmight explain why the Monte Desertrsquos granivorous antsappear to remove fewer seeds from experimental baitsthan do North American ants But it does not follow thatthe ants of the Monte Desert ldquoare depauperate and notusually granivorousrdquo (Mares and Rosenzweig 1978) Tounderstand whether differences in seed removal from arti-ficial baits reflect intercontinental differences in antgranivory it will be necessary to examine more closely theforaging behavior of the Monte Desertrsquos ants For examplepreliminary observations indicate that some Pogono-myrmex species of the Monte Desert harvest the majorityof their seeds directly from plant stalks At the same timethe frequency of individuals of these highly specializedseed-eating species was very low at experimental seed sta-tions located on the soil (Javier Lopez de Casenave SilviaClaver Viacutector R Cueto Luis Marone unpublished data)Subtle differences in ant foraging behavior among conti-nents might reduce the comparability of results from thiskind of experiment thus affecting the conclusions aboutthe importance of granivorous ants as seed harvesters

Studies of seed removal from bait stations and of foodhabits of putative granivorous animals are necessary butnot sufficient to make inferences about the communityrole of granivores One straightforward approach to deter-mine the community role of those animals is to directlyassess the extent to which the dynamics of the resource(ie seeds) is affected by the activity of the consumer (iebirds ants or mammals) That is the importance ofgranivory can be better addressed through mechanismicstudies of the effects of seed consumption on the fate ofnaturally dispersed seeds (Price and Joyner 1997 Maroneet al 1998b)

Granivorous mammal assemblagesThe absence of functional analogues of North Americarsquosheteromyid rodents and the low diversity and abundanceof other mammalian granivores in South Americandeserts have been blamed for the ldquoinsignificantrdquo mam-malian seed consumption recorded in the northern MonteDesert (Mares et al 1977 Mares and Rosenzweig 1978Brown and Ojeda 1987) Recent studies however suggestthat this rate of seed consumption does not apply to theentire Monte Desert rodents remove almost an order ofmagnitude more seeds in the central Monte Desert than inthe northern Monte Desert (Lopez de Casenave et al1998) Mammalian seed removal is also markedly higherin the southern Monte than in Andalgalaacute (Sergio L Sabapersonal communication) Thus even if South Americatruly lacks analogues of heteromyids the premise thatrodent granivory is insignificant in the Monte Desert over-all deserves scrutiny for at least two reasons

First the spacious cheek pouches of heteromyidsenhance their fabled proficiency at gathering and hoard-ing seeds In a study of several heteromyid species indi-

viduals on average filled their cheek pouches to more than90 of pouch capacity during a single feeding bout in thefield (Vander Wall et al 1997) On a daily basis thereforethese rodents may harvest far more seeds than they needto fulfill their immediate energy requirements Althoughsome South American rodents have been shown to hoardsome seeds at least under laborator y conditions (Vaacutesquez1996) these species lack cheek pouches (Nowak and Par-adiso 1983) It follows that on average South Americanrodents would be expected to harvest fewer seeds frombaits than do heteromyids Some indirect evidence seemsto corroborate this assertion Predavecrsquos (1997) estimatesof seed consumption by Australian desert rodents (whichlike South American rodents lack cheek pouches) weredramatically higher when based on calculations of ener-getics than when based on bait removal experiments

Another reason for caution with previous generaliza-tions about mammal granivory in South America is thatbasic dietary information is still lacking for South Ameri-can desert rodents and desert ecologists often disagreeabout their food habits Although this discrepancy some-times simply reflects the fact that the proportion of seedsin animalsrsquo diets varies widely in time and space disagree-ment is also fostered by the lack of dietary informationThis lack of information is a major problem because somecalculatio ns of seed consumption (eg those based onenergetics) are sensitive to subtle variations in dietary val-ues (Kerley 1992) Hence terms such as ldquogranivorerdquo arenot always used in a consistent way Strictly speaking aselective consumer (eg a granivorous mammal) is ananimal that takes some or all food items in different pro-portions than the proportions at which they are present inthe patches where the animal feeds within the size limitsimposed by the perceptive handling and swallowingcapabilities of the consumer (Jaksic 1989)

Because this definition is difficult to apply in natureother more rudimentary ones could be used providedthat they are used only as a basis of comparative assess-ments For example Kerley and Whitford (1994) suggest-ed that mammals can be designated as granivores folivoresor insectivores when their diets are dominated by therespective dietary category (ie more than 50 of the dietconsists of the category) whereas those of more mixed dietscan be termed omnivores Using this criterion Meserve(1981a) showed that two rodent species in the southernfringe of the Atacama Desert of Chile Oligoryzomys longi-caudatus and Phyllotis darwini were granivorous especiallyin the dry season when 73 and 59 respectively of theiridentified diets consisted of seeds Abrothrix (Akodon) oli-vaceus almost achieved granivore status with 45 of itsdiet consisting of seeds Similarly Pizzimenti and De Salle(1980) found that in several localities of the Andes ofsouthern Peruacute more than 50 of the diet of some rodentspecies consisted of seeds (eg Phyllotis darwini 53 Ppictus 60) Given that some heteromyid rodents that areusually considered specialized seedeaters also consume sig-

128 BioScience February 2000 Vol 50 No 2

Articles

nificant amounts of insects and green vegetation duringsome seasons (Mares 1993a) it appears that some of theabove-mentioned Atacama and Altiplano rodent speciesshould also be considered granivores

In the Monte Desert Mares et al (1977) and Mares(1993b) reported finding no granivorous small mammalsIn some localities of the central Monte Desert howeverCalomys musculinus may be the most abundant rodentspecies (Ojeda 1989) and data from other semi-arid habi-tats of Argentina show that the dry-season diet of C mus-culinus consists of approximately 90 seeds (Dellafioreand Polop 1994) In a recent study in the central MonteDesert Campos (1997) found that during the dry seasonC musculinus appeared to consume a relatively high pro-portion of seeds (50) and that the diets of other smallmammals included few seeds (less than 5 in the diets ofGraomys griseoflavus Eligmodontia typus Thylamys pusil-lus and Akodon molinae) However these low values mayseverely underestimate the proportion of seeds in the dietof C musculinus and the other small mammals FirstCampos (1997) indicated that the microhistological tech-nique that she had employed underestimates food itemsother than leavesmdashin particular seeds Second Campos(1997) tallied seeds in stomach contents by counting onlythe glume remains of grass diaspores however rodentsoften dehusk grass diaspores and discard the glume beforeconsumption (Martha J Piantanida Divisioacuten Mastozo-ologiacutea Museo Argentino de Ciencias Naturales BuenosAires Argentina personal communication) Finallyrodents consume forb seeds as well as grass seeds Forinstance 43 of the diet of C musculinus in west-centralArgentina consists of Chenopodium seeds and 22 of itconsists of Amaranthus seeds (Dellafiore and Polop 1994)

North American species of the heteromyid generaMicrodipodops and Dipodomys are usually labeled as spe-cialized granivores (eg Kelt et al 1996) Neverthelessthey also consume insects and green vegetation (Mares1993a Kerley and Whitford 1994) Moreover Kerley et al(1997) have proposed that the keystone status of kangaroorats in the Chihuahuan Desert might be due tograminivory (ie herbivory) rather than to granivory Bycontrast those South American rodents (eg several Olig-oryzomys Calomys and Phyllotis species) that appear todisplay similar seasonal changes in diet (granivorous atsome times herbivorousinsectivorous at others) arealmost never labeled ldquogranivoresrdquo in the literature

This semantic inconsistency which has implications forthe conclusions of comparative studies may reflect anunfortunate attribute of research practice that deserves thescrutiny of the sociologists of science when basic empiri-cal information on a particular subject is lacking or frag-mentary unproven assertions may gain credence as factseven though such assertions are only at best plausibleassumptions This problem however should fade awaywhen these basic assumptions (eg that the ability ofrodents to harvest clumped seeds is similar in North andSouth America or that the incidence of seeds in the diet ofSouth American rodents is negligible) are carefully testedbefore deciding about the suitability of the specifichypothesis under scrutiny (eg that seed-eating mammalsin the Monte Desert and other South American desertshave a significant impact on seed reserves) This researchstrategy is essential to preventing ldquonaive refutationismrdquo(Lakatos 1978) in which a specific hypothesis is consid-ered false simply by the refutation of just one of its pre-dictions (eg that South American small mammalsremove similar amounts of seeds offered in bait experi-ments as their North American counterparts)

Granivorous bird assemblagesThe low rates of seed removal by birds observed in baitremoval experiments seemed to suggest that birds areeither unimportant seedeaters in deserts or that they fail todetect the experimentally proffered trays For examplebirds ate few of the test seeds in the South African Karoo(Kerley 1991) the Chihuahuan Desert (Parmenter et al1984) and the Australian Desert (Morton 1985) Giventhe diverse and abundant avian granivores of Australiandeserts Morton (1985 1993) conjectured that these birdsshould have a major community role in Australian desertseven though they did not visit any of his seed stations Sev-eral authors have suggested that the short time span of baitremoval experiments (2ndash3 days) may be inadequate for

February 2000 Vol 50 No 2 BioScience 129

Articles

Figure 4 Seasonal rates of seed removal by granivores inthe central Monte Desert Birds open circles ants solid

circles mammals open triangles Mean rates of removalfor the 23ndash25 trays available only to the respective taxonare shown Within a season means with the same letter

are not significantly different according to Tukeyrsquos test ( Plt 005) Figure redrawn from Lopez de Casenave et al

(1998) and used with permission from Blackwell Science

measuring seed consumption by desert birds (Mares andRosenzweig 1978 Morton 1985)

In most bait experiments carried out in South Americandeserts however avian granivores quickly discovered baitsand consumed seeds Indeed birds often consumed moreseeds than did the other granivore taxa (Table 2) We knowof no idiosyncratic characteristic of South American birdsthat may explain this pattern Thus to control for anypropensity of the Monte avifauna to detect seed trays withunusual skills we used an approach that did not rely on arti-ficial baits to assess whether birds are important seedeatersin the central Monte Desert (Marone et al 1998b)

Bait experiments have shown that bird granivores arethe main autumnndashwinter seed consumers in the centralMonte Desert (Figure 4 see Lopez de Casenave et al1998) To assess the impact of seed-eating birds on theautumnndashwinter soil seed reserves we compared the soilseed bank in the late summer of 1995 (12 February) withthat present the following early spring (25 October) alsotaking into account the total number of seeds that enteredthe soil from late summer to early spring (ie we mea-sured seed rain Marone et al 1998b) In late summerbefore consumption by birds the mean seed density ofgrass seed banks was 2400 seedsm2 or 036 gm2 The nextspringmdashfollowing the input of approximately 3000 grassseedsm2 or 071 gm2 as well as the period of bird con-sumption in autumn and wintermdashthe density of grassseeds was 2700 seedsm2 or 039 gm2 Medium and largegrass seeds suffered higher postdispersal losses than didsmall seeds Likewise densities of forb seeds in the seedbank were statistically indistinguishable between late sum-mer (5500 seedsm2 or 134 gm2) and spring (6500seedsm2 or 153 gm2) although forb seed productionduring the study period had been relatively low (400seedsm2 or 012 gm 2) These results suggest thatautumnndashwinter seed predators in the central MonteDesert favor grass seeds over forb seeds

Several lines of evidence confirm that postdispersalgrass seed loss during autumnndashwinter in the centralMonte Desert is due mainly to vertebrate consumptionFirst granivorous ants are active almost exclusively during

the spring and summer (Figure 4 Lopez de Casenave et al1998) Furthermore C4 grasses germinate mostly in latespring and summer and total grass seed germinationwhich usually does not surpass 05 of previous soil seedreserves (Marone et al 1998b) reached only 5 of previ-ous reserves during the exceptionally wet summer of 1998which was associated with a strong El NintildeoSouthernOscillation event (Luis Marone Manuel E Horno RafaelGonzaacutelez del Solar unpublished data) Finally given thecomposition of the seed bank at different depths (0ndash2 cm2ndash4 cm and 4ndash6 cm) Marone et al (1998a) concludedthat grass seeds especially the medium and large seedswould suffer negligible loss by deep burial

Therefore it was not surprising that the pattern of seedlosses coincided with the pattern of seed consumption bygranivorous birds in the autumns and winters of 1993through 1995 Nearly 93 of the seed mass in bird stom-achs came from grass seeds and only 7 came from forbseeds Furthermore medium and large grass seeds sufferedthe highest losses from the soil seed bank and were also themain target of foraging by granivores Moreover a signifi-cant positive correlation existed across grass speciesbetween the mass decrease of seed species from the soiltoward spring and the mass of those seed species in birddiets in autumnndashwinter (Figure 5 Marone et al 1998b)This positive correlation suggests that bird consumptioncould explain a great deal of the autumnndashwinter grass seedloss observed in soils of the central Monte Desert

These lines of evidence indicate that vertebrate grani-vores (particularly birds) have a major impact on theabundance floristic composition and size distribution ofseed reserves in the Monte Desert where vertebrategranivory in general and avian granivory in particularhad previously been considered unimportant Moreovernewly produced seeds from perennial grasses constitute amajor fraction of autumnndashwinter bird diet This findingsupports the proposal (Marone 1992) that the timing andamount of rainfall in the central Monte Desert may great-ly influence the abundance and migrations of granivorousbirds via the opportunistic response of seed production bygrasses to variations in rainfall Population interactions

130 BioScience February 2000 Vol 50 No 2

Articles

Figure 5 Relationship between the mass of seeds fromperennial grasses in the autumn and winter diets (in1993ndash1995) of four granivorous bird species in the centralMonte Desert and the loss of seeds of each species during theautumn and winter of 1995 The bird species are Zonotrichiacapensis Phrygilus carbonarius Diuca diuca andSaltatricula multicolor The overall correlation wassignificant (r = 087 n = 11 P lt 0001) Grass species are asfollows Pap Pappophorum spp Set Setaria leucopila DigDigitaria californica Tri Trichloris crinita Dip Diplachnedubia Spo Sporobolus cryptandrus Ari Aristida spp NeoNeobouteloua lophostachya Chl Chloris castilloniana BouBouteloua spp The point for Stipa spp is not shown on thefigure but overlaps with that for Bouteloua spp

between seeds and avian granivores in this South Ameri-can desert may therefore be more important than hithertoappreciated

Concluding remarksThe relative importance of seed consumption or granivo-rous assemblages in deserts around the world cannot beassessed through one research approach alone (eg baitremoval experiments energetics approaches descriptionsof the species composition of granivorous assemblages orquantification of individualsrsquo diets) Instead research pro-grams that include multiple approaches involving redun-dancy and cross-checks of hypotheses and methods maylead to the most robust conclusions and therefore to syn-thesis and integration (Pickett et al 1994) Furthermoreany such program should involve long-term studies thattake into account the spatial and temporal variability ofnatural communities

Partly as a consequence of such a lack of integrationnatural rates of seed consumption and the abundance anddiversity of granivorous assemblages in some South Amer-ican deserts may have been underestimated in the pastThe evidence we have discussed in this article comes fromvarious desert locations of southern South America andwas obtained by using different research approaches Thisevidence suggests that birds and ants are importantseedeaters during the colder and warmer months respec-tively and that the role of small mammals as granivores inthe central Monte Desert of Argentina deserves moredetailed assessment These results should be readily incor-porated into comparative studies to distinguish betweenidiosyncratic and general processes molding desert com-munities worldwide Although ecological ldquolawsrdquo are by nomeans universal ecological understanding will continueto depend on theory development (Pickett et al 1994Mahner and Bunge 1997) To develop ecological theoryresearchers need good observations combined with rigor-ous and realistic experiments carried out in the context ofresearch programs that are focused whenever possible ontesting mechanisms to account for ecological phenomena(Werner 1998)

AcknowledgmentsWe acknowledge Sergio Camiacuten Silvia Claver RafaelGonzaacutelez del Solar Fernando Milesi Martha J PiantanidaBertilde Rossi Eduardo Tomaacutes-Mezquida and GualbertoZalazar for their constructive and pleasant cooperationduring field and laborator y work Manuel E Horno andIris Peralta contributed partnership and stimulating dis-cussion at the initial (and more chaotic) stages of ourstudies we are especially indebted to both of them SergioL Saba was kind enough to let us use his unpublisheddata First drafts of the manuscript were greatly improvedthrough critical review from Rebecca Chasan Chris Dick-man Pete Feinsinger Lali Guichoacuten Rafael Gonzaacutelez delSolar Fabiaacuten Jaksic Graham Kerley Fernando Milesi

Stephen Morton Mary V Price Julian Reid AlejandraRibichich Rodrigo Vaacutesquez and four anonymous review-ers At different stages field and laboratory work werefinanced by the Man and the Biosphere Programme Unit-ed Nations Educational Scientific and Cultural Organiza-tion the Association of Field Ornithologists Programa deCiencias Naturales Museo Argentino de Ciencias Natu-rales ldquoBernardino Rivadaviardquo IADIZA-Provincia de Men-doza and the Argentine funding agencies CONICET (PEI032797) and Agencia Nacional de Promocioacuten Cientiacutefica yTecnoloacutegica (PICT 01-03187) L M acknowledges CON-ICET and the Canadian Government for financial sup-port and Mario Bunge for the stimulating environment atMcGill University where the final version of this paperwas written This article is Contribution No 8 of theDesert Community Ecology Research Team Plant Eco-physiology Department IADIZA Institute

References citedAbramsky Z 1983 Experiments on seed predation by rodents and ants in

the Israeli desert Oecologia 57 328ndash332

Brown JH Ojeda RA 1987 Granivory Patterns processes and conse-

quences of seed consumption on two continents Revista Chilena de

Historia Natural 60 337ndash349

Campos CM 1997 Utilizacioacuten de recursos alimentarios por mamiacuteferos

medianos y pequentildeos del desierto del Monte PhD dissertation Uni-

versidad Nacional de Coacuterdoba Coacuterdoba Argentina

Capurro HA Bucher EH 1982 Poblaciones de aves graniacutevoras y disponi-

bilidad de semillas en el bosque chaquentildeo de Chamical Ecosur 9

117ndash131

Childs S Goodall DW 1973 Seed reserves of desert soils Logan (UT)

Utah State University USIBP Desert Biome Research Memorandum

73-5

Claver S Fowler HG 1993 The ant fauna (Hymenoptera Formicidae) of

the Ntildeacuntildeaacuten Biosphere Reserve Naturalia 18 189ndash193

Dellafiore CM Polop JJ 1994 Feeding habits of Calomys musculinus in the

crop fields and its borders Mastozoolog iacutea Neotropical (Argentina) 1

45ndash50

Dye AJ 1969 Germination potentials and accumulation of native plant

seeds from southern New Mexico Masterrsquos thesis New Mexico State

University Las Cruces NM

Holldobler B Wilson EO 1990 The Ants Cambridge (MA) Harvard Uni-

versity Press

Jaksic FM 1989 Opportunist selective and other often-confused terms in

the predation literature Revista Chilena de Historia Natural 62 7ndash8

Kelrick MI MacMahon JA Parmenter RR Sisson DV 1986 Native seed

preferences of shrubndashsteppe rodents birds and ants The relationships

of seed attributes and seed use Oecologia 68 327ndash337

Kelt DA Brown JH Heske EJ Marquet PA Morton SR Reid JRW Rogovin

KA Shenbrot G 1996 Community structure of desert small mam-

mals Comparisons across four continents Ecology 77 746ndash761

Kemp PR 1989 Seed bank and vegetation processes in deserts Pages

257ndash281 in Allessio-Leck M Parker VT Simpson RL eds Ecology of

Soil Seed Banks San Diego (CA) Academic Press

Kerley GIH 1991 Seed removal by rodents birds and ants in the semi-arid

Karoo South Africa Journal of Arid Environments 20 63ndash69

______ 1992 Small mammal seed consumption in the Karoo South

Africa Further evidence for divergence in desert biotic processes

Oecologia 89 471ndash475

Kerley GIH Whitford WG 1994 Desert-dwelling small mammals as grani-

vores Intercontinental variations Australian Journal of Zoology 42

543ndash555

Kerley GIH Whitford WG Kay FR 1997 Mechanisms for the keystone sta-

February 2000 Vol 50 No 2 BioScience 131

Articles

lagids were mutualists with food plants shared with antsperhaps storing some of the seeds of these plants in sur-face caches and thereby enhancing germination as hasbeen shown among North American heteromyid rodents(Mares and Rosenzweig 1978) After the extinction ofargyrolagids those plants would have suffered a decreasein their populations and the ant assemblages would alsohave declined in abundance and richness

Although these historical explanations about the role ofextinct argyrolagids cannot be tested directly they do leadto testable predictions about the status of present-day seedreserves in the Monte Desert (Mares and Rosenzweig1978 Brown and Ojeda 1987) For example the seeds con-sumed by present-day ants as well as those presumablyinvolved with marsupials in the past are predicted to beless abundant in seed banks of South American thanNorth American deserts (Marone and Horno 1997) Wetested this assertion by comparing seed reserves in wood-land and shrubland of the central Monte Desert with thosein several other South and North American deserts(Marone and Horno 1997) Densities of seeds in soil bankswere similar in arid North and South America at the habi-tat scale (Table 1) Regardless of continent most reportsfall within the range of 8000ndash30000 seedsm2 proposedby Kemp (1989) with the exception of one extraordinari-ly high value in the eastern Mojave Desert of California(Price and Joyner 1997)

Moreover with respect to production of seeds in SouthAmerica the few available data suggest seed productionrates similar to those in North America By using seedtraps to catch the seed rain during primary dispersal weestimated grass seed production in years of moderate rain-fall in the central Monte Desert to be 125 kgha (Maroneet al 1998a) Using similar methods Pulliam and Parker

(1979) and Pulliam and Dunning (1987) reported averagegrass seed production of 130ndash158 kgha in moderatelyrainy years in grasslands of the North American Chi-huahuan Desert of southeastern Arizona Finally seednumbers at the microhabitat scale as well as the propor-tion of small seeds (ie those presumably preferred byants) also appear to be similar in deserts of North andSouth America (Marone and Horno 1997) Overall thesefindings fail to support the hypothesis of a seed decline inthe South American sites Therefore differences in theresource base should not be invoked to account for differ-ences in granivorous assemblages (Mares and Rosenzweig1978) or in the foraging behavior of particular species(Medel and Vaacutesquez 1994) between South and NorthAmerican deserts Morton (1985 1993) also ruled out dif-ferences in the resource base as an explanation for differ-ences in granivorous assemblages between Australia andNorth America

Bait removal experimentsThe results of Mares and Rosenzweig (1978) on present-day consumption of seeds in the northern Monte Desertby different granivorous taxa in bait removal experimentsare still often extrapolated to the entire Monte Desert (egWurm 1998) To assess the applicability of those results tothe central Monte Desert (Figure 2) we therefore used thesame kinds of experiments in which seed consumption isestimated by comparing the amounts of seeds taken bydifferent taxa from feeding stations (dishes) placed in thedesert (Figure 3) There can be problems however incomparing results from bait removal experiments becausesuch experiments often lack standardized procedures Forinstance different authors have offered a variable assort-ment of seeds to granivores and have placed seed dishes

February 2000 Vol 50 No 2 BioScience 125

Articles

Desert General descriptionc Seed number (per m2) Seed mass (gm2) Reference

North AmericaSonora Shrubland dryndashrainy year 400ndash7700 Kemp 1989Mojave Shrubland dry year 430 05 Childs and Goodall 1973Mojave Shrubland dryndashrainy year 800ndash12100 05ndash52 Nelson and Chew 1977Mojave Shrubland 106000 380 Price and Joyner 1997Chihuahua Shrubland 13000ndash22000 Dye 1969Chihuahua Shrubland fine soils 8800ndash24500 Kemp 1989Chihuahua Shrubland coarse soils 1300ndash6000 Kemp 1989

South AmericaArid Chaco Open forest gt20000 Capurro and Bucher 1982Central Chile Thorn scrub seasonal 10700ndash23900 83ndash249 Meserve 1981bCentral Chile Matorral seasonal 13100ndash20500 Loacutepez-Calleja 1995Central Monte Open forest seasonal 14900ndash22900 36ndash60 Marone and Horno 1997Central Monte Shrubland seasonal 9300ndash15600 21ndash35 Marone and Horno 1997

aReprinted in modified form from Marone and Horno (1997) with permission of Academic PressbA single value for seed number or mass signifies an average calculated over several seasons or years Two numbers signify the extreme values of arangecThe habitat type and the contrasting conditions when the measurements were made are indicated where available These conditions account for theextreme values of each range (eg different seasons years or soil types)

Table 1a Average total seed number and seed mass in soil seed banks in different habitats from several South and NorthAmerican warm desertsb

among microhabitats in unspecified ways even thoughthe rate of seed consumption by mammals birds and antsmay differ with the type of seed (Kelrick et al 1986) or themicrohabitat (Lopez de Casenave et al 1998) Conse-quently researchers need to use caution when comparingseed removal rates quantitatively (Parmenter et al 1984Kelrick et al 1986 Vaacutesquez et al 1995)

Even when we used the most conservative measure ofseed consumption (ie the average seed removal rate inexposed microhabitats in which seed consumption bybirds and ants in the summer was significantly lower thanin microhabitats located under the canopy of shrubs andtrees) we found that the total rate of seed consumption inthe central Monte (Lopez de Casenave et al 1998) wasmore than five times greater than in the northern Monte(Mares and Rosenzweig 1978) Indeed if data from thecentral Monte Desert are incorporated into global com-parisons of the impact of desert granivores on seedresources the most logical conclusion appears to be thattotal granivory in the Monte is not abnormally depressed(Lopez de Casenave et al 1998) rather total seed removal aswell as seed removal by mammals and ants is exceptionallyhigh in North American deserts (see Morton 1985)

To avoid troublesome quantitative contrasts Vaacutesquez etal (1995) compared rankings of the relative importance ofmammals birds and ants among bait removal experi-ments worldwide We summarize their findings in Table 2adding our own results from the central Monte Desert as

well as an independent data set from the southern MonteDesert near Puerto Madryn Chubut Argentina (Figure 1Sergio L Saba Centro Nacional Patagoacutenico PuertoMadryn Chubut Argentina personal communication)Although these rankings show only the relative impacts ofevery taxa in every study site (ie they tell us nothingabout absolute granivory rates) they corroborate previousgeneralizations that the relative impact of mammals isgreater in northern continents and that the relative impactof ants is greater in southern continents The rankings alsoreveal a novel finding granivorous birds are major seedconsumers in several South American locations

The likely importance of seed-eating birds calls atten-tion to some underappreciated mechanisms of seed lossTo assess the similarities of the impact of granivores onseed resources in deserts around the world it is necessaryto simultaneou sly evaluate both seed availability and allplausible mechanisms of seed loss (which may vary amongdeserts even when total seed loss remains constant) Somemechanisms that have received far less attention thanmammal and ant consumption include avian granivoryseed germination and burial and seed mortality caused byfungi and bacteria These and other possible sources ofseed output should be carefully quantified before conjec-turing whether historical or ecological causes are morelikely to explain the organization of the seedndashgranivoresystem at regional and intercontinental scales (Kerley andWhitford 1994 Marone and Horno 1997)

Granivorous ant assemblagesResearchers have often assumed that assemblages ofgranivorous ants are substantially less diverse in aridSouth America than in similar habitats of North America(eg Mares et al 1977 Mares and Rosenzweig 1978Brown and Ojeda 1987 Holldobler and Wilson 1990) Forexample James Hunt (in Mares et al 1977) compared antcommunities of a Sonoran Desert site near Silver Bell Ari-zona and the northern Monte Desert site near AndalgalaacuteHe recorded a higher species richness of ants in total butfewer granivorous species at Andalgalaacute The granivore sta-tus of ants however was grounded not on direct foragingobservations but on assumptions based on taxonomy

When the granivore status of ants was defined accord-ing to foraging records however the conclusions changedMedel (1995) compared seed-harvester ant assemblages ofNorth America Australia and South America by usingseed removal experiments following the methods of Mor-ton and Davidson (1988) He sampled ants in 11 locationsin the central and northern Monte Desert includingAndalgalaacute and found that these assemblages were in factmore diverse and abundant than their North Americancounterparts (Medel and Vaacutesquez 1994 Medel 1995)Using the same method we assessed the composition ofseed-harvester ant assemblages in the central MonteDesert (Javier Lopez de Casenave Silvia Claver Viacutector RCueto Luis Marone unpublished data) In December

126 BioScience February 2000 Vol 50 No 2

Articles

Figure 2 The open Prosopis flexuosa woodland in theBiosphere Reserve of Ntildeacuntildeaacuten in the central Monte DesertArgentina We carried out fieldwork in open woodlands andin Larrea cuneifolia shrublands of the reserve between 1993and 1998 Ntildeacuntildeaacutenrsquos climate is dry and temperate with coldwinters and most annual rainfall occurs in springndashsummer(OctoberndashMarch) Perennial C4 grasses mainly of the generaTrichloris Pappophorum Setaria Sporobolus Digitariaand Aristida are abundant in both open woodland andshrubland Grass seed production and dispersal are mostlyrestricted to late summer and early autumn (Marone et al1998a)

1995 we recorded 12 and 14 species removing seeds fromtwo nearby sites This species richness exceeded the meanof 98 (n = 11 sites) and 28 (n = 5 sites) reported for thenorthern Monte Desert and central Chile respectively(Medel and Vaacutesquez 1994) as well as the mean of 52 (n =10 sites) and 85 (n = 16 sites) reported for North Ameri-can and Australian deserts respectively (Morton andDavidson 1988) In summary direct foraging observationof ants is not in agreement with previous assertions thatgranivorous ants are depauperate in the Monte Desert

The bait removal method employed in all these studiesis sensitive to the definition of ldquoharvester antrdquo used If antspecies are considered to be seed harvesters simply becausethey are seen at seed stations then the number of har-vester ant species may be overestimated By contrast wecounted only ants that effectively loaded seeds from seedstations Consequently we conclude that assemblages ofpotentially seed-harvesting ants are not depauperate atleast in the central Monte Desert

The South American ant assemblages however includeseveral species with more generalist diets than those of the

obligate seed-harvester ants of the genus Pogonomyrmexwhich make up the bulk of ant assemblages in NorthAmerican deserts Although Mares and Rosenzweig(1978) Medel (1995) and Medel and Vaacutesquez (1994) allhypothesized that omnivory of the ant species in SouthAmerican deserts results from a lower seed availability inthese deserts than in North American deserts the figuresin Table 1 do not support this explanation Indeed Pogon-omyrmex species exist in South America as well The threePogonomyrmex species (P rastratus P pronotalis and Pinermis) that occur in the central Monte Desert (Claverand Fowler 1993) appear to be highly specialized grani-vores (Javier Lopez de Casenave Silvia Claver Viacutector RCueto Luis Marone unpublished data) However giventhat the South American species of this genus seem to dis-play smaller colonies and lower population densities thanthose in North America (Holldobler and Wilson 1990) thehypothesis of a lower impact of South American Pogono-myrmex species on seeds (naturally available as well asoffered in baits) is a plausible although still unexploredhypothesis

February 2000 Vol 50 No 2 BioScience 127

Articles

Figure 3 A feeding station used in bait removalexperiments (Lopez de Casenave et al 1998) A known

amount of seeds is offered in each station at the start of thetrial Every station consists of three plastic Petri dishes (9cm in diameter) a ldquomammalrdquo tray a ldquobirdrdquo tray and an

ldquoantrdquo tray Vertebrate trays are glued to the top of longplastic cylinders and set 2ndash3 cm above the ground to

prevent access by ants Seeds for birds are available onlyduring the day and seeds for mammals are available only

at night Ant trays are buried with the rim of the Petri dishlevel with the soil surface and covered with mesh hardware

cloth to prevent access by vertebrates (these trays remainactive 24 hours a day) The stations are periodically

replenished with known amounts of seeds to avoidtotaldepletion (total duration of the experiment is 48 hours)

Region Granivore ranking Reference

North America (Sonora Desert) M gt A gt B Mares and Rosenzweig 1978Israel (Negev Desert) M gt Ac Abramsky 1983South Africa (Karoo Desert) A gt M gt B Kerley 1991Australia (Simpson Desert) A gt B gt M Morton 1985Chile (dense matorral) A gt B gt M Vaacutesquez et al 1995Chile (sparse matorral) B = A gt M Vaacutesquez et al 1995Argentina (central Monte Desert)

Under-canopy sites A gt B gt M Lopez de Casenave et al 1998Open sites B = A = M Lopez de Casenave et al 1998

Argentina (Southern Monte Desert) B gt M = A Sergio L Saba personalcommunication

Argentina (Northern Monte Desert) A gt B = M Mares and Rosenzweig 1978aExpanded from Vaacutesquez et al (1995)bAccording to Vaacutesquez et al (1995) we considered two taxa to have different granivory intensities when the average seed removal rate of one was at leasttwice that of the othercThis study was carried out only during springndashsummer birds were thought to have a negligible influence and were therefore not studied

Table 2a Rankings of the relative importance of the three main granivore taxa (A ants B birds M small mammals) assuggested by bait removal experiments carried out in different arid regions of the worldb

Low population densities of Pogonomyrmex ants andgeneralized food habits among some other ant speciesmight explain why the Monte Desertrsquos granivorous antsappear to remove fewer seeds from experimental baitsthan do North American ants But it does not follow thatthe ants of the Monte Desert ldquoare depauperate and notusually granivorousrdquo (Mares and Rosenzweig 1978) Tounderstand whether differences in seed removal from arti-ficial baits reflect intercontinental differences in antgranivory it will be necessary to examine more closely theforaging behavior of the Monte Desertrsquos ants For examplepreliminary observations indicate that some Pogono-myrmex species of the Monte Desert harvest the majorityof their seeds directly from plant stalks At the same timethe frequency of individuals of these highly specializedseed-eating species was very low at experimental seed sta-tions located on the soil (Javier Lopez de Casenave SilviaClaver Viacutector R Cueto Luis Marone unpublished data)Subtle differences in ant foraging behavior among conti-nents might reduce the comparability of results from thiskind of experiment thus affecting the conclusions aboutthe importance of granivorous ants as seed harvesters

Studies of seed removal from bait stations and of foodhabits of putative granivorous animals are necessary butnot sufficient to make inferences about the communityrole of granivores One straightforward approach to deter-mine the community role of those animals is to directlyassess the extent to which the dynamics of the resource(ie seeds) is affected by the activity of the consumer (iebirds ants or mammals) That is the importance ofgranivory can be better addressed through mechanismicstudies of the effects of seed consumption on the fate ofnaturally dispersed seeds (Price and Joyner 1997 Maroneet al 1998b)

Granivorous mammal assemblagesThe absence of functional analogues of North Americarsquosheteromyid rodents and the low diversity and abundanceof other mammalian granivores in South Americandeserts have been blamed for the ldquoinsignificantrdquo mam-malian seed consumption recorded in the northern MonteDesert (Mares et al 1977 Mares and Rosenzweig 1978Brown and Ojeda 1987) Recent studies however suggestthat this rate of seed consumption does not apply to theentire Monte Desert rodents remove almost an order ofmagnitude more seeds in the central Monte Desert than inthe northern Monte Desert (Lopez de Casenave et al1998) Mammalian seed removal is also markedly higherin the southern Monte than in Andalgalaacute (Sergio L Sabapersonal communication) Thus even if South Americatruly lacks analogues of heteromyids the premise thatrodent granivory is insignificant in the Monte Desert over-all deserves scrutiny for at least two reasons

First the spacious cheek pouches of heteromyidsenhance their fabled proficiency at gathering and hoard-ing seeds In a study of several heteromyid species indi-

viduals on average filled their cheek pouches to more than90 of pouch capacity during a single feeding bout in thefield (Vander Wall et al 1997) On a daily basis thereforethese rodents may harvest far more seeds than they needto fulfill their immediate energy requirements Althoughsome South American rodents have been shown to hoardsome seeds at least under laborator y conditions (Vaacutesquez1996) these species lack cheek pouches (Nowak and Par-adiso 1983) It follows that on average South Americanrodents would be expected to harvest fewer seeds frombaits than do heteromyids Some indirect evidence seemsto corroborate this assertion Predavecrsquos (1997) estimatesof seed consumption by Australian desert rodents (whichlike South American rodents lack cheek pouches) weredramatically higher when based on calculations of ener-getics than when based on bait removal experiments

Another reason for caution with previous generaliza-tions about mammal granivory in South America is thatbasic dietary information is still lacking for South Ameri-can desert rodents and desert ecologists often disagreeabout their food habits Although this discrepancy some-times simply reflects the fact that the proportion of seedsin animalsrsquo diets varies widely in time and space disagree-ment is also fostered by the lack of dietary informationThis lack of information is a major problem because somecalculatio ns of seed consumption (eg those based onenergetics) are sensitive to subtle variations in dietary val-ues (Kerley 1992) Hence terms such as ldquogranivorerdquo arenot always used in a consistent way Strictly speaking aselective consumer (eg a granivorous mammal) is ananimal that takes some or all food items in different pro-portions than the proportions at which they are present inthe patches where the animal feeds within the size limitsimposed by the perceptive handling and swallowingcapabilities of the consumer (Jaksic 1989)

Because this definition is difficult to apply in natureother more rudimentary ones could be used providedthat they are used only as a basis of comparative assess-ments For example Kerley and Whitford (1994) suggest-ed that mammals can be designated as granivores folivoresor insectivores when their diets are dominated by therespective dietary category (ie more than 50 of the dietconsists of the category) whereas those of more mixed dietscan be termed omnivores Using this criterion Meserve(1981a) showed that two rodent species in the southernfringe of the Atacama Desert of Chile Oligoryzomys longi-caudatus and Phyllotis darwini were granivorous especiallyin the dry season when 73 and 59 respectively of theiridentified diets consisted of seeds Abrothrix (Akodon) oli-vaceus almost achieved granivore status with 45 of itsdiet consisting of seeds Similarly Pizzimenti and De Salle(1980) found that in several localities of the Andes ofsouthern Peruacute more than 50 of the diet of some rodentspecies consisted of seeds (eg Phyllotis darwini 53 Ppictus 60) Given that some heteromyid rodents that areusually considered specialized seedeaters also consume sig-

128 BioScience February 2000 Vol 50 No 2

Articles

nificant amounts of insects and green vegetation duringsome seasons (Mares 1993a) it appears that some of theabove-mentioned Atacama and Altiplano rodent speciesshould also be considered granivores

In the Monte Desert Mares et al (1977) and Mares(1993b) reported finding no granivorous small mammalsIn some localities of the central Monte Desert howeverCalomys musculinus may be the most abundant rodentspecies (Ojeda 1989) and data from other semi-arid habi-tats of Argentina show that the dry-season diet of C mus-culinus consists of approximately 90 seeds (Dellafioreand Polop 1994) In a recent study in the central MonteDesert Campos (1997) found that during the dry seasonC musculinus appeared to consume a relatively high pro-portion of seeds (50) and that the diets of other smallmammals included few seeds (less than 5 in the diets ofGraomys griseoflavus Eligmodontia typus Thylamys pusil-lus and Akodon molinae) However these low values mayseverely underestimate the proportion of seeds in the dietof C musculinus and the other small mammals FirstCampos (1997) indicated that the microhistological tech-nique that she had employed underestimates food itemsother than leavesmdashin particular seeds Second Campos(1997) tallied seeds in stomach contents by counting onlythe glume remains of grass diaspores however rodentsoften dehusk grass diaspores and discard the glume beforeconsumption (Martha J Piantanida Divisioacuten Mastozo-ologiacutea Museo Argentino de Ciencias Naturales BuenosAires Argentina personal communication) Finallyrodents consume forb seeds as well as grass seeds Forinstance 43 of the diet of C musculinus in west-centralArgentina consists of Chenopodium seeds and 22 of itconsists of Amaranthus seeds (Dellafiore and Polop 1994)

North American species of the heteromyid generaMicrodipodops and Dipodomys are usually labeled as spe-cialized granivores (eg Kelt et al 1996) Neverthelessthey also consume insects and green vegetation (Mares1993a Kerley and Whitford 1994) Moreover Kerley et al(1997) have proposed that the keystone status of kangaroorats in the Chihuahuan Desert might be due tograminivory (ie herbivory) rather than to granivory Bycontrast those South American rodents (eg several Olig-oryzomys Calomys and Phyllotis species) that appear todisplay similar seasonal changes in diet (granivorous atsome times herbivorousinsectivorous at others) arealmost never labeled ldquogranivoresrdquo in the literature

This semantic inconsistency which has implications forthe conclusions of comparative studies may reflect anunfortunate attribute of research practice that deserves thescrutiny of the sociologists of science when basic empiri-cal information on a particular subject is lacking or frag-mentary unproven assertions may gain credence as factseven though such assertions are only at best plausibleassumptions This problem however should fade awaywhen these basic assumptions (eg that the ability ofrodents to harvest clumped seeds is similar in North andSouth America or that the incidence of seeds in the diet ofSouth American rodents is negligible) are carefully testedbefore deciding about the suitability of the specifichypothesis under scrutiny (eg that seed-eating mammalsin the Monte Desert and other South American desertshave a significant impact on seed reserves) This researchstrategy is essential to preventing ldquonaive refutationismrdquo(Lakatos 1978) in which a specific hypothesis is consid-ered false simply by the refutation of just one of its pre-dictions (eg that South American small mammalsremove similar amounts of seeds offered in bait experi-ments as their North American counterparts)

Granivorous bird assemblagesThe low rates of seed removal by birds observed in baitremoval experiments seemed to suggest that birds areeither unimportant seedeaters in deserts or that they fail todetect the experimentally proffered trays For examplebirds ate few of the test seeds in the South African Karoo(Kerley 1991) the Chihuahuan Desert (Parmenter et al1984) and the Australian Desert (Morton 1985) Giventhe diverse and abundant avian granivores of Australiandeserts Morton (1985 1993) conjectured that these birdsshould have a major community role in Australian desertseven though they did not visit any of his seed stations Sev-eral authors have suggested that the short time span of baitremoval experiments (2ndash3 days) may be inadequate for

February 2000 Vol 50 No 2 BioScience 129

Articles

Figure 4 Seasonal rates of seed removal by granivores inthe central Monte Desert Birds open circles ants solid

circles mammals open triangles Mean rates of removalfor the 23ndash25 trays available only to the respective taxonare shown Within a season means with the same letter

are not significantly different according to Tukeyrsquos test ( Plt 005) Figure redrawn from Lopez de Casenave et al

(1998) and used with permission from Blackwell Science

measuring seed consumption by desert birds (Mares andRosenzweig 1978 Morton 1985)

In most bait experiments carried out in South Americandeserts however avian granivores quickly discovered baitsand consumed seeds Indeed birds often consumed moreseeds than did the other granivore taxa (Table 2) We knowof no idiosyncratic characteristic of South American birdsthat may explain this pattern Thus to control for anypropensity of the Monte avifauna to detect seed trays withunusual skills we used an approach that did not rely on arti-ficial baits to assess whether birds are important seedeatersin the central Monte Desert (Marone et al 1998b)

Bait experiments have shown that bird granivores arethe main autumnndashwinter seed consumers in the centralMonte Desert (Figure 4 see Lopez de Casenave et al1998) To assess the impact of seed-eating birds on theautumnndashwinter soil seed reserves we compared the soilseed bank in the late summer of 1995 (12 February) withthat present the following early spring (25 October) alsotaking into account the total number of seeds that enteredthe soil from late summer to early spring (ie we mea-sured seed rain Marone et al 1998b) In late summerbefore consumption by birds the mean seed density ofgrass seed banks was 2400 seedsm2 or 036 gm2 The nextspringmdashfollowing the input of approximately 3000 grassseedsm2 or 071 gm2 as well as the period of bird con-sumption in autumn and wintermdashthe density of grassseeds was 2700 seedsm2 or 039 gm2 Medium and largegrass seeds suffered higher postdispersal losses than didsmall seeds Likewise densities of forb seeds in the seedbank were statistically indistinguishable between late sum-mer (5500 seedsm2 or 134 gm2) and spring (6500seedsm2 or 153 gm2) although forb seed productionduring the study period had been relatively low (400seedsm2 or 012 gm 2) These results suggest thatautumnndashwinter seed predators in the central MonteDesert favor grass seeds over forb seeds

Several lines of evidence confirm that postdispersalgrass seed loss during autumnndashwinter in the centralMonte Desert is due mainly to vertebrate consumptionFirst granivorous ants are active almost exclusively during

the spring and summer (Figure 4 Lopez de Casenave et al1998) Furthermore C4 grasses germinate mostly in latespring and summer and total grass seed germinationwhich usually does not surpass 05 of previous soil seedreserves (Marone et al 1998b) reached only 5 of previ-ous reserves during the exceptionally wet summer of 1998which was associated with a strong El NintildeoSouthernOscillation event (Luis Marone Manuel E Horno RafaelGonzaacutelez del Solar unpublished data) Finally given thecomposition of the seed bank at different depths (0ndash2 cm2ndash4 cm and 4ndash6 cm) Marone et al (1998a) concludedthat grass seeds especially the medium and large seedswould suffer negligible loss by deep burial

Therefore it was not surprising that the pattern of seedlosses coincided with the pattern of seed consumption bygranivorous birds in the autumns and winters of 1993through 1995 Nearly 93 of the seed mass in bird stom-achs came from grass seeds and only 7 came from forbseeds Furthermore medium and large grass seeds sufferedthe highest losses from the soil seed bank and were also themain target of foraging by granivores Moreover a signifi-cant positive correlation existed across grass speciesbetween the mass decrease of seed species from the soiltoward spring and the mass of those seed species in birddiets in autumnndashwinter (Figure 5 Marone et al 1998b)This positive correlation suggests that bird consumptioncould explain a great deal of the autumnndashwinter grass seedloss observed in soils of the central Monte Desert

These lines of evidence indicate that vertebrate grani-vores (particularly birds) have a major impact on theabundance floristic composition and size distribution ofseed reserves in the Monte Desert where vertebrategranivory in general and avian granivory in particularhad previously been considered unimportant Moreovernewly produced seeds from perennial grasses constitute amajor fraction of autumnndashwinter bird diet This findingsupports the proposal (Marone 1992) that the timing andamount of rainfall in the central Monte Desert may great-ly influence the abundance and migrations of granivorousbirds via the opportunistic response of seed production bygrasses to variations in rainfall Population interactions

130 BioScience February 2000 Vol 50 No 2

Articles

Figure 5 Relationship between the mass of seeds fromperennial grasses in the autumn and winter diets (in1993ndash1995) of four granivorous bird species in the centralMonte Desert and the loss of seeds of each species during theautumn and winter of 1995 The bird species are Zonotrichiacapensis Phrygilus carbonarius Diuca diuca andSaltatricula multicolor The overall correlation wassignificant (r = 087 n = 11 P lt 0001) Grass species are asfollows Pap Pappophorum spp Set Setaria leucopila DigDigitaria californica Tri Trichloris crinita Dip Diplachnedubia Spo Sporobolus cryptandrus Ari Aristida spp NeoNeobouteloua lophostachya Chl Chloris castilloniana BouBouteloua spp The point for Stipa spp is not shown on thefigure but overlaps with that for Bouteloua spp

between seeds and avian granivores in this South Ameri-can desert may therefore be more important than hithertoappreciated

Concluding remarksThe relative importance of seed consumption or granivo-rous assemblages in deserts around the world cannot beassessed through one research approach alone (eg baitremoval experiments energetics approaches descriptionsof the species composition of granivorous assemblages orquantification of individualsrsquo diets) Instead research pro-grams that include multiple approaches involving redun-dancy and cross-checks of hypotheses and methods maylead to the most robust conclusions and therefore to syn-thesis and integration (Pickett et al 1994) Furthermoreany such program should involve long-term studies thattake into account the spatial and temporal variability ofnatural communities

Partly as a consequence of such a lack of integrationnatural rates of seed consumption and the abundance anddiversity of granivorous assemblages in some South Amer-ican deserts may have been underestimated in the pastThe evidence we have discussed in this article comes fromvarious desert locations of southern South America andwas obtained by using different research approaches Thisevidence suggests that birds and ants are importantseedeaters during the colder and warmer months respec-tively and that the role of small mammals as granivores inthe central Monte Desert of Argentina deserves moredetailed assessment These results should be readily incor-porated into comparative studies to distinguish betweenidiosyncratic and general processes molding desert com-munities worldwide Although ecological ldquolawsrdquo are by nomeans universal ecological understanding will continueto depend on theory development (Pickett et al 1994Mahner and Bunge 1997) To develop ecological theoryresearchers need good observations combined with rigor-ous and realistic experiments carried out in the context ofresearch programs that are focused whenever possible ontesting mechanisms to account for ecological phenomena(Werner 1998)

AcknowledgmentsWe acknowledge Sergio Camiacuten Silvia Claver RafaelGonzaacutelez del Solar Fernando Milesi Martha J PiantanidaBertilde Rossi Eduardo Tomaacutes-Mezquida and GualbertoZalazar for their constructive and pleasant cooperationduring field and laborator y work Manuel E Horno andIris Peralta contributed partnership and stimulating dis-cussion at the initial (and more chaotic) stages of ourstudies we are especially indebted to both of them SergioL Saba was kind enough to let us use his unpublisheddata First drafts of the manuscript were greatly improvedthrough critical review from Rebecca Chasan Chris Dick-man Pete Feinsinger Lali Guichoacuten Rafael Gonzaacutelez delSolar Fabiaacuten Jaksic Graham Kerley Fernando Milesi

Stephen Morton Mary V Price Julian Reid AlejandraRibichich Rodrigo Vaacutesquez and four anonymous review-ers At different stages field and laboratory work werefinanced by the Man and the Biosphere Programme Unit-ed Nations Educational Scientific and Cultural Organiza-tion the Association of Field Ornithologists Programa deCiencias Naturales Museo Argentino de Ciencias Natu-rales ldquoBernardino Rivadaviardquo IADIZA-Provincia de Men-doza and the Argentine funding agencies CONICET (PEI032797) and Agencia Nacional de Promocioacuten Cientiacutefica yTecnoloacutegica (PICT 01-03187) L M acknowledges CON-ICET and the Canadian Government for financial sup-port and Mario Bunge for the stimulating environment atMcGill University where the final version of this paperwas written This article is Contribution No 8 of theDesert Community Ecology Research Team Plant Eco-physiology Department IADIZA Institute

References citedAbramsky Z 1983 Experiments on seed predation by rodents and ants in

the Israeli desert Oecologia 57 328ndash332

Brown JH Ojeda RA 1987 Granivory Patterns processes and conse-

quences of seed consumption on two continents Revista Chilena de

Historia Natural 60 337ndash349

Campos CM 1997 Utilizacioacuten de recursos alimentarios por mamiacuteferos

medianos y pequentildeos del desierto del Monte PhD dissertation Uni-

versidad Nacional de Coacuterdoba Coacuterdoba Argentina

Capurro HA Bucher EH 1982 Poblaciones de aves graniacutevoras y disponi-

bilidad de semillas en el bosque chaquentildeo de Chamical Ecosur 9

117ndash131

Childs S Goodall DW 1973 Seed reserves of desert soils Logan (UT)

Utah State University USIBP Desert Biome Research Memorandum

73-5

Claver S Fowler HG 1993 The ant fauna (Hymenoptera Formicidae) of

the Ntildeacuntildeaacuten Biosphere Reserve Naturalia 18 189ndash193

Dellafiore CM Polop JJ 1994 Feeding habits of Calomys musculinus in the

crop fields and its borders Mastozoolog iacutea Neotropical (Argentina) 1

45ndash50

Dye AJ 1969 Germination potentials and accumulation of native plant

seeds from southern New Mexico Masterrsquos thesis New Mexico State

University Las Cruces NM

Holldobler B Wilson EO 1990 The Ants Cambridge (MA) Harvard Uni-

versity Press

Jaksic FM 1989 Opportunist selective and other often-confused terms in

the predation literature Revista Chilena de Historia Natural 62 7ndash8

Kelrick MI MacMahon JA Parmenter RR Sisson DV 1986 Native seed

preferences of shrubndashsteppe rodents birds and ants The relationships

of seed attributes and seed use Oecologia 68 327ndash337

Kelt DA Brown JH Heske EJ Marquet PA Morton SR Reid JRW Rogovin

KA Shenbrot G 1996 Community structure of desert small mam-

mals Comparisons across four continents Ecology 77 746ndash761

Kemp PR 1989 Seed bank and vegetation processes in deserts Pages

257ndash281 in Allessio-Leck M Parker VT Simpson RL eds Ecology of

Soil Seed Banks San Diego (CA) Academic Press

Kerley GIH 1991 Seed removal by rodents birds and ants in the semi-arid

Karoo South Africa Journal of Arid Environments 20 63ndash69

______ 1992 Small mammal seed consumption in the Karoo South

Africa Further evidence for divergence in desert biotic processes

Oecologia 89 471ndash475

Kerley GIH Whitford WG 1994 Desert-dwelling small mammals as grani-

vores Intercontinental variations Australian Journal of Zoology 42

543ndash555

Kerley GIH Whitford WG Kay FR 1997 Mechanisms for the keystone sta-

February 2000 Vol 50 No 2 BioScience 131

Articles

among microhabitats in unspecified ways even thoughthe rate of seed consumption by mammals birds and antsmay differ with the type of seed (Kelrick et al 1986) or themicrohabitat (Lopez de Casenave et al 1998) Conse-quently researchers need to use caution when comparingseed removal rates quantitatively (Parmenter et al 1984Kelrick et al 1986 Vaacutesquez et al 1995)

Even when we used the most conservative measure ofseed consumption (ie the average seed removal rate inexposed microhabitats in which seed consumption bybirds and ants in the summer was significantly lower thanin microhabitats located under the canopy of shrubs andtrees) we found that the total rate of seed consumption inthe central Monte (Lopez de Casenave et al 1998) wasmore than five times greater than in the northern Monte(Mares and Rosenzweig 1978) Indeed if data from thecentral Monte Desert are incorporated into global com-parisons of the impact of desert granivores on seedresources the most logical conclusion appears to be thattotal granivory in the Monte is not abnormally depressed(Lopez de Casenave et al 1998) rather total seed removal aswell as seed removal by mammals and ants is exceptionallyhigh in North American deserts (see Morton 1985)

To avoid troublesome quantitative contrasts Vaacutesquez etal (1995) compared rankings of the relative importance ofmammals birds and ants among bait removal experi-ments worldwide We summarize their findings in Table 2adding our own results from the central Monte Desert as

well as an independent data set from the southern MonteDesert near Puerto Madryn Chubut Argentina (Figure 1Sergio L Saba Centro Nacional Patagoacutenico PuertoMadryn Chubut Argentina personal communication)Although these rankings show only the relative impacts ofevery taxa in every study site (ie they tell us nothingabout absolute granivory rates) they corroborate previousgeneralizations that the relative impact of mammals isgreater in northern continents and that the relative impactof ants is greater in southern continents The rankings alsoreveal a novel finding granivorous birds are major seedconsumers in several South American locations

The likely importance of seed-eating birds calls atten-tion to some underappreciated mechanisms of seed lossTo assess the similarities of the impact of granivores onseed resources in deserts around the world it is necessaryto simultaneou sly evaluate both seed availability and allplausible mechanisms of seed loss (which may vary amongdeserts even when total seed loss remains constant) Somemechanisms that have received far less attention thanmammal and ant consumption include avian granivoryseed germination and burial and seed mortality caused byfungi and bacteria These and other possible sources ofseed output should be carefully quantified before conjec-turing whether historical or ecological causes are morelikely to explain the organization of the seedndashgranivoresystem at regional and intercontinental scales (Kerley andWhitford 1994 Marone and Horno 1997)

Granivorous ant assemblagesResearchers have often assumed that assemblages ofgranivorous ants are substantially less diverse in aridSouth America than in similar habitats of North America(eg Mares et al 1977 Mares and Rosenzweig 1978Brown and Ojeda 1987 Holldobler and Wilson 1990) Forexample James Hunt (in Mares et al 1977) compared antcommunities of a Sonoran Desert site near Silver Bell Ari-zona and the northern Monte Desert site near AndalgalaacuteHe recorded a higher species richness of ants in total butfewer granivorous species at Andalgalaacute The granivore sta-tus of ants however was grounded not on direct foragingobservations but on assumptions based on taxonomy

When the granivore status of ants was defined accord-ing to foraging records however the conclusions changedMedel (1995) compared seed-harvester ant assemblages ofNorth America Australia and South America by usingseed removal experiments following the methods of Mor-ton and Davidson (1988) He sampled ants in 11 locationsin the central and northern Monte Desert includingAndalgalaacute and found that these assemblages were in factmore diverse and abundant than their North Americancounterparts (Medel and Vaacutesquez 1994 Medel 1995)Using the same method we assessed the composition ofseed-harvester ant assemblages in the central MonteDesert (Javier Lopez de Casenave Silvia Claver Viacutector RCueto Luis Marone unpublished data) In December

126 BioScience February 2000 Vol 50 No 2

Articles

Figure 2 The open Prosopis flexuosa woodland in theBiosphere Reserve of Ntildeacuntildeaacuten in the central Monte DesertArgentina We carried out fieldwork in open woodlands andin Larrea cuneifolia shrublands of the reserve between 1993and 1998 Ntildeacuntildeaacutenrsquos climate is dry and temperate with coldwinters and most annual rainfall occurs in springndashsummer(OctoberndashMarch) Perennial C4 grasses mainly of the generaTrichloris Pappophorum Setaria Sporobolus Digitariaand Aristida are abundant in both open woodland andshrubland Grass seed production and dispersal are mostlyrestricted to late summer and early autumn (Marone et al1998a)

1995 we recorded 12 and 14 species removing seeds fromtwo nearby sites This species richness exceeded the meanof 98 (n = 11 sites) and 28 (n = 5 sites) reported for thenorthern Monte Desert and central Chile respectively(Medel and Vaacutesquez 1994) as well as the mean of 52 (n =10 sites) and 85 (n = 16 sites) reported for North Ameri-can and Australian deserts respectively (Morton andDavidson 1988) In summary direct foraging observationof ants is not in agreement with previous assertions thatgranivorous ants are depauperate in the Monte Desert

The bait removal method employed in all these studiesis sensitive to the definition of ldquoharvester antrdquo used If antspecies are considered to be seed harvesters simply becausethey are seen at seed stations then the number of har-vester ant species may be overestimated By contrast wecounted only ants that effectively loaded seeds from seedstations Consequently we conclude that assemblages ofpotentially seed-harvesting ants are not depauperate atleast in the central Monte Desert

The South American ant assemblages however includeseveral species with more generalist diets than those of the

obligate seed-harvester ants of the genus Pogonomyrmexwhich make up the bulk of ant assemblages in NorthAmerican deserts Although Mares and Rosenzweig(1978) Medel (1995) and Medel and Vaacutesquez (1994) allhypothesized that omnivory of the ant species in SouthAmerican deserts results from a lower seed availability inthese deserts than in North American deserts the figuresin Table 1 do not support this explanation Indeed Pogon-omyrmex species exist in South America as well The threePogonomyrmex species (P rastratus P pronotalis and Pinermis) that occur in the central Monte Desert (Claverand Fowler 1993) appear to be highly specialized grani-vores (Javier Lopez de Casenave Silvia Claver Viacutector RCueto Luis Marone unpublished data) However giventhat the South American species of this genus seem to dis-play smaller colonies and lower population densities thanthose in North America (Holldobler and Wilson 1990) thehypothesis of a lower impact of South American Pogono-myrmex species on seeds (naturally available as well asoffered in baits) is a plausible although still unexploredhypothesis

February 2000 Vol 50 No 2 BioScience 127

Articles

Figure 3 A feeding station used in bait removalexperiments (Lopez de Casenave et al 1998) A known

amount of seeds is offered in each station at the start of thetrial Every station consists of three plastic Petri dishes (9cm in diameter) a ldquomammalrdquo tray a ldquobirdrdquo tray and an

ldquoantrdquo tray Vertebrate trays are glued to the top of longplastic cylinders and set 2ndash3 cm above the ground to

prevent access by ants Seeds for birds are available onlyduring the day and seeds for mammals are available only

at night Ant trays are buried with the rim of the Petri dishlevel with the soil surface and covered with mesh hardware

cloth to prevent access by vertebrates (these trays remainactive 24 hours a day) The stations are periodically

replenished with known amounts of seeds to avoidtotaldepletion (total duration of the experiment is 48 hours)

Region Granivore ranking Reference

North America (Sonora Desert) M gt A gt B Mares and Rosenzweig 1978Israel (Negev Desert) M gt Ac Abramsky 1983South Africa (Karoo Desert) A gt M gt B Kerley 1991Australia (Simpson Desert) A gt B gt M Morton 1985Chile (dense matorral) A gt B gt M Vaacutesquez et al 1995Chile (sparse matorral) B = A gt M Vaacutesquez et al 1995Argentina (central Monte Desert)

Under-canopy sites A gt B gt M Lopez de Casenave et al 1998Open sites B = A = M Lopez de Casenave et al 1998

Argentina (Southern Monte Desert) B gt M = A Sergio L Saba personalcommunication

Argentina (Northern Monte Desert) A gt B = M Mares and Rosenzweig 1978aExpanded from Vaacutesquez et al (1995)bAccording to Vaacutesquez et al (1995) we considered two taxa to have different granivory intensities when the average seed removal rate of one was at leasttwice that of the othercThis study was carried out only during springndashsummer birds were thought to have a negligible influence and were therefore not studied

Table 2a Rankings of the relative importance of the three main granivore taxa (A ants B birds M small mammals) assuggested by bait removal experiments carried out in different arid regions of the worldb

Low population densities of Pogonomyrmex ants andgeneralized food habits among some other ant speciesmight explain why the Monte Desertrsquos granivorous antsappear to remove fewer seeds from experimental baitsthan do North American ants But it does not follow thatthe ants of the Monte Desert ldquoare depauperate and notusually granivorousrdquo (Mares and Rosenzweig 1978) Tounderstand whether differences in seed removal from arti-ficial baits reflect intercontinental differences in antgranivory it will be necessary to examine more closely theforaging behavior of the Monte Desertrsquos ants For examplepreliminary observations indicate that some Pogono-myrmex species of the Monte Desert harvest the majorityof their seeds directly from plant stalks At the same timethe frequency of individuals of these highly specializedseed-eating species was very low at experimental seed sta-tions located on the soil (Javier Lopez de Casenave SilviaClaver Viacutector R Cueto Luis Marone unpublished data)Subtle differences in ant foraging behavior among conti-nents might reduce the comparability of results from thiskind of experiment thus affecting the conclusions aboutthe importance of granivorous ants as seed harvesters

Studies of seed removal from bait stations and of foodhabits of putative granivorous animals are necessary butnot sufficient to make inferences about the communityrole of granivores One straightforward approach to deter-mine the community role of those animals is to directlyassess the extent to which the dynamics of the resource(ie seeds) is affected by the activity of the consumer (iebirds ants or mammals) That is the importance ofgranivory can be better addressed through mechanismicstudies of the effects of seed consumption on the fate ofnaturally dispersed seeds (Price and Joyner 1997 Maroneet al 1998b)

Granivorous mammal assemblagesThe absence of functional analogues of North Americarsquosheteromyid rodents and the low diversity and abundanceof other mammalian granivores in South Americandeserts have been blamed for the ldquoinsignificantrdquo mam-malian seed consumption recorded in the northern MonteDesert (Mares et al 1977 Mares and Rosenzweig 1978Brown and Ojeda 1987) Recent studies however suggestthat this rate of seed consumption does not apply to theentire Monte Desert rodents remove almost an order ofmagnitude more seeds in the central Monte Desert than inthe northern Monte Desert (Lopez de Casenave et al1998) Mammalian seed removal is also markedly higherin the southern Monte than in Andalgalaacute (Sergio L Sabapersonal communication) Thus even if South Americatruly lacks analogues of heteromyids the premise thatrodent granivory is insignificant in the Monte Desert over-all deserves scrutiny for at least two reasons

First the spacious cheek pouches of heteromyidsenhance their fabled proficiency at gathering and hoard-ing seeds In a study of several heteromyid species indi-

viduals on average filled their cheek pouches to more than90 of pouch capacity during a single feeding bout in thefield (Vander Wall et al 1997) On a daily basis thereforethese rodents may harvest far more seeds than they needto fulfill their immediate energy requirements Althoughsome South American rodents have been shown to hoardsome seeds at least under laborator y conditions (Vaacutesquez1996) these species lack cheek pouches (Nowak and Par-adiso 1983) It follows that on average South Americanrodents would be expected to harvest fewer seeds frombaits than do heteromyids Some indirect evidence seemsto corroborate this assertion Predavecrsquos (1997) estimatesof seed consumption by Australian desert rodents (whichlike South American rodents lack cheek pouches) weredramatically higher when based on calculations of ener-getics than when based on bait removal experiments

Another reason for caution with previous generaliza-tions about mammal granivory in South America is thatbasic dietary information is still lacking for South Ameri-can desert rodents and desert ecologists often disagreeabout their food habits Although this discrepancy some-times simply reflects the fact that the proportion of seedsin animalsrsquo diets varies widely in time and space disagree-ment is also fostered by the lack of dietary informationThis lack of information is a major problem because somecalculatio ns of seed consumption (eg those based onenergetics) are sensitive to subtle variations in dietary val-ues (Kerley 1992) Hence terms such as ldquogranivorerdquo arenot always used in a consistent way Strictly speaking aselective consumer (eg a granivorous mammal) is ananimal that takes some or all food items in different pro-portions than the proportions at which they are present inthe patches where the animal feeds within the size limitsimposed by the perceptive handling and swallowingcapabilities of the consumer (Jaksic 1989)

Because this definition is difficult to apply in natureother more rudimentary ones could be used providedthat they are used only as a basis of comparative assess-ments For example Kerley and Whitford (1994) suggest-ed that mammals can be designated as granivores folivoresor insectivores when their diets are dominated by therespective dietary category (ie more than 50 of the dietconsists of the category) whereas those of more mixed dietscan be termed omnivores Using this criterion Meserve(1981a) showed that two rodent species in the southernfringe of the Atacama Desert of Chile Oligoryzomys longi-caudatus and Phyllotis darwini were granivorous especiallyin the dry season when 73 and 59 respectively of theiridentified diets consisted of seeds Abrothrix (Akodon) oli-vaceus almost achieved granivore status with 45 of itsdiet consisting of seeds Similarly Pizzimenti and De Salle(1980) found that in several localities of the Andes ofsouthern Peruacute more than 50 of the diet of some rodentspecies consisted of seeds (eg Phyllotis darwini 53 Ppictus 60) Given that some heteromyid rodents that areusually considered specialized seedeaters also consume sig-

128 BioScience February 2000 Vol 50 No 2

Articles

nificant amounts of insects and green vegetation duringsome seasons (Mares 1993a) it appears that some of theabove-mentioned Atacama and Altiplano rodent speciesshould also be considered granivores

In the Monte Desert Mares et al (1977) and Mares(1993b) reported finding no granivorous small mammalsIn some localities of the central Monte Desert howeverCalomys musculinus may be the most abundant rodentspecies (Ojeda 1989) and data from other semi-arid habi-tats of Argentina show that the dry-season diet of C mus-culinus consists of approximately 90 seeds (Dellafioreand Polop 1994) In a recent study in the central MonteDesert Campos (1997) found that during the dry seasonC musculinus appeared to consume a relatively high pro-portion of seeds (50) and that the diets of other smallmammals included few seeds (less than 5 in the diets ofGraomys griseoflavus Eligmodontia typus Thylamys pusil-lus and Akodon molinae) However these low values mayseverely underestimate the proportion of seeds in the dietof C musculinus and the other small mammals FirstCampos (1997) indicated that the microhistological tech-nique that she had employed underestimates food itemsother than leavesmdashin particular seeds Second Campos(1997) tallied seeds in stomach contents by counting onlythe glume remains of grass diaspores however rodentsoften dehusk grass diaspores and discard the glume beforeconsumption (Martha J Piantanida Divisioacuten Mastozo-ologiacutea Museo Argentino de Ciencias Naturales BuenosAires Argentina personal communication) Finallyrodents consume forb seeds as well as grass seeds Forinstance 43 of the diet of C musculinus in west-centralArgentina consists of Chenopodium seeds and 22 of itconsists of Amaranthus seeds (Dellafiore and Polop 1994)

North American species of the heteromyid generaMicrodipodops and Dipodomys are usually labeled as spe-cialized granivores (eg Kelt et al 1996) Neverthelessthey also consume insects and green vegetation (Mares1993a Kerley and Whitford 1994) Moreover Kerley et al(1997) have proposed that the keystone status of kangaroorats in the Chihuahuan Desert might be due tograminivory (ie herbivory) rather than to granivory Bycontrast those South American rodents (eg several Olig-oryzomys Calomys and Phyllotis species) that appear todisplay similar seasonal changes in diet (granivorous atsome times herbivorousinsectivorous at others) arealmost never labeled ldquogranivoresrdquo in the literature

This semantic inconsistency which has implications forthe conclusions of comparative studies may reflect anunfortunate attribute of research practice that deserves thescrutiny of the sociologists of science when basic empiri-cal information on a particular subject is lacking or frag-mentary unproven assertions may gain credence as factseven though such assertions are only at best plausibleassumptions This problem however should fade awaywhen these basic assumptions (eg that the ability ofrodents to harvest clumped seeds is similar in North andSouth America or that the incidence of seeds in the diet ofSouth American rodents is negligible) are carefully testedbefore deciding about the suitability of the specifichypothesis under scrutiny (eg that seed-eating mammalsin the Monte Desert and other South American desertshave a significant impact on seed reserves) This researchstrategy is essential to preventing ldquonaive refutationismrdquo(Lakatos 1978) in which a specific hypothesis is consid-ered false simply by the refutation of just one of its pre-dictions (eg that South American small mammalsremove similar amounts of seeds offered in bait experi-ments as their North American counterparts)

Granivorous bird assemblagesThe low rates of seed removal by birds observed in baitremoval experiments seemed to suggest that birds areeither unimportant seedeaters in deserts or that they fail todetect the experimentally proffered trays For examplebirds ate few of the test seeds in the South African Karoo(Kerley 1991) the Chihuahuan Desert (Parmenter et al1984) and the Australian Desert (Morton 1985) Giventhe diverse and abundant avian granivores of Australiandeserts Morton (1985 1993) conjectured that these birdsshould have a major community role in Australian desertseven though they did not visit any of his seed stations Sev-eral authors have suggested that the short time span of baitremoval experiments (2ndash3 days) may be inadequate for

February 2000 Vol 50 No 2 BioScience 129

Articles

Figure 4 Seasonal rates of seed removal by granivores inthe central Monte Desert Birds open circles ants solid

circles mammals open triangles Mean rates of removalfor the 23ndash25 trays available only to the respective taxonare shown Within a season means with the same letter

are not significantly different according to Tukeyrsquos test ( Plt 005) Figure redrawn from Lopez de Casenave et al

(1998) and used with permission from Blackwell Science

measuring seed consumption by desert birds (Mares andRosenzweig 1978 Morton 1985)

In most bait experiments carried out in South Americandeserts however avian granivores quickly discovered baitsand consumed seeds Indeed birds often consumed moreseeds than did the other granivore taxa (Table 2) We knowof no idiosyncratic characteristic of South American birdsthat may explain this pattern Thus to control for anypropensity of the Monte avifauna to detect seed trays withunusual skills we used an approach that did not rely on arti-ficial baits to assess whether birds are important seedeatersin the central Monte Desert (Marone et al 1998b)

Bait experiments have shown that bird granivores arethe main autumnndashwinter seed consumers in the centralMonte Desert (Figure 4 see Lopez de Casenave et al1998) To assess the impact of seed-eating birds on theautumnndashwinter soil seed reserves we compared the soilseed bank in the late summer of 1995 (12 February) withthat present the following early spring (25 October) alsotaking into account the total number of seeds that enteredthe soil from late summer to early spring (ie we mea-sured seed rain Marone et al 1998b) In late summerbefore consumption by birds the mean seed density ofgrass seed banks was 2400 seedsm2 or 036 gm2 The nextspringmdashfollowing the input of approximately 3000 grassseedsm2 or 071 gm2 as well as the period of bird con-sumption in autumn and wintermdashthe density of grassseeds was 2700 seedsm2 or 039 gm2 Medium and largegrass seeds suffered higher postdispersal losses than didsmall seeds Likewise densities of forb seeds in the seedbank were statistically indistinguishable between late sum-mer (5500 seedsm2 or 134 gm2) and spring (6500seedsm2 or 153 gm2) although forb seed productionduring the study period had been relatively low (400seedsm2 or 012 gm 2) These results suggest thatautumnndashwinter seed predators in the central MonteDesert favor grass seeds over forb seeds

Several lines of evidence confirm that postdispersalgrass seed loss during autumnndashwinter in the centralMonte Desert is due mainly to vertebrate consumptionFirst granivorous ants are active almost exclusively during

the spring and summer (Figure 4 Lopez de Casenave et al1998) Furthermore C4 grasses germinate mostly in latespring and summer and total grass seed germinationwhich usually does not surpass 05 of previous soil seedreserves (Marone et al 1998b) reached only 5 of previ-ous reserves during the exceptionally wet summer of 1998which was associated with a strong El NintildeoSouthernOscillation event (Luis Marone Manuel E Horno RafaelGonzaacutelez del Solar unpublished data) Finally given thecomposition of the seed bank at different depths (0ndash2 cm2ndash4 cm and 4ndash6 cm) Marone et al (1998a) concludedthat grass seeds especially the medium and large seedswould suffer negligible loss by deep burial

Therefore it was not surprising that the pattern of seedlosses coincided with the pattern of seed consumption bygranivorous birds in the autumns and winters of 1993through 1995 Nearly 93 of the seed mass in bird stom-achs came from grass seeds and only 7 came from forbseeds Furthermore medium and large grass seeds sufferedthe highest losses from the soil seed bank and were also themain target of foraging by granivores Moreover a signifi-cant positive correlation existed across grass speciesbetween the mass decrease of seed species from the soiltoward spring and the mass of those seed species in birddiets in autumnndashwinter (Figure 5 Marone et al 1998b)This positive correlation suggests that bird consumptioncould explain a great deal of the autumnndashwinter grass seedloss observed in soils of the central Monte Desert

These lines of evidence indicate that vertebrate grani-vores (particularly birds) have a major impact on theabundance floristic composition and size distribution ofseed reserves in the Monte Desert where vertebrategranivory in general and avian granivory in particularhad previously been considered unimportant Moreovernewly produced seeds from perennial grasses constitute amajor fraction of autumnndashwinter bird diet This findingsupports the proposal (Marone 1992) that the timing andamount of rainfall in the central Monte Desert may great-ly influence the abundance and migrations of granivorousbirds via the opportunistic response of seed production bygrasses to variations in rainfall Population interactions

130 BioScience February 2000 Vol 50 No 2

Articles

Figure 5 Relationship between the mass of seeds fromperennial grasses in the autumn and winter diets (in1993ndash1995) of four granivorous bird species in the centralMonte Desert and the loss of seeds of each species during theautumn and winter of 1995 The bird species are Zonotrichiacapensis Phrygilus carbonarius Diuca diuca andSaltatricula multicolor The overall correlation wassignificant (r = 087 n = 11 P lt 0001) Grass species are asfollows Pap Pappophorum spp Set Setaria leucopila DigDigitaria californica Tri Trichloris crinita Dip Diplachnedubia Spo Sporobolus cryptandrus Ari Aristida spp NeoNeobouteloua lophostachya Chl Chloris castilloniana BouBouteloua spp The point for Stipa spp is not shown on thefigure but overlaps with that for Bouteloua spp

between seeds and avian granivores in this South Ameri-can desert may therefore be more important than hithertoappreciated

Concluding remarksThe relative importance of seed consumption or granivo-rous assemblages in deserts around the world cannot beassessed through one research approach alone (eg baitremoval experiments energetics approaches descriptionsof the species composition of granivorous assemblages orquantification of individualsrsquo diets) Instead research pro-grams that include multiple approaches involving redun-dancy and cross-checks of hypotheses and methods maylead to the most robust conclusions and therefore to syn-thesis and integration (Pickett et al 1994) Furthermoreany such program should involve long-term studies thattake into account the spatial and temporal variability ofnatural communities

Partly as a consequence of such a lack of integrationnatural rates of seed consumption and the abundance anddiversity of granivorous assemblages in some South Amer-ican deserts may have been underestimated in the pastThe evidence we have discussed in this article comes fromvarious desert locations of southern South America andwas obtained by using different research approaches Thisevidence suggests that birds and ants are importantseedeaters during the colder and warmer months respec-tively and that the role of small mammals as granivores inthe central Monte Desert of Argentina deserves moredetailed assessment These results should be readily incor-porated into comparative studies to distinguish betweenidiosyncratic and general processes molding desert com-munities worldwide Although ecological ldquolawsrdquo are by nomeans universal ecological understanding will continueto depend on theory development (Pickett et al 1994Mahner and Bunge 1997) To develop ecological theoryresearchers need good observations combined with rigor-ous and realistic experiments carried out in the context ofresearch programs that are focused whenever possible ontesting mechanisms to account for ecological phenomena(Werner 1998)

AcknowledgmentsWe acknowledge Sergio Camiacuten Silvia Claver RafaelGonzaacutelez del Solar Fernando Milesi Martha J PiantanidaBertilde Rossi Eduardo Tomaacutes-Mezquida and GualbertoZalazar for their constructive and pleasant cooperationduring field and laborator y work Manuel E Horno andIris Peralta contributed partnership and stimulating dis-cussion at the initial (and more chaotic) stages of ourstudies we are especially indebted to both of them SergioL Saba was kind enough to let us use his unpublisheddata First drafts of the manuscript were greatly improvedthrough critical review from Rebecca Chasan Chris Dick-man Pete Feinsinger Lali Guichoacuten Rafael Gonzaacutelez delSolar Fabiaacuten Jaksic Graham Kerley Fernando Milesi

Stephen Morton Mary V Price Julian Reid AlejandraRibichich Rodrigo Vaacutesquez and four anonymous review-ers At different stages field and laboratory work werefinanced by the Man and the Biosphere Programme Unit-ed Nations Educational Scientific and Cultural Organiza-tion the Association of Field Ornithologists Programa deCiencias Naturales Museo Argentino de Ciencias Natu-rales ldquoBernardino Rivadaviardquo IADIZA-Provincia de Men-doza and the Argentine funding agencies CONICET (PEI032797) and Agencia Nacional de Promocioacuten Cientiacutefica yTecnoloacutegica (PICT 01-03187) L M acknowledges CON-ICET and the Canadian Government for financial sup-port and Mario Bunge for the stimulating environment atMcGill University where the final version of this paperwas written This article is Contribution No 8 of theDesert Community Ecology Research Team Plant Eco-physiology Department IADIZA Institute

References citedAbramsky Z 1983 Experiments on seed predation by rodents and ants in

the Israeli desert Oecologia 57 328ndash332

Brown JH Ojeda RA 1987 Granivory Patterns processes and conse-

quences of seed consumption on two continents Revista Chilena de

Historia Natural 60 337ndash349

Campos CM 1997 Utilizacioacuten de recursos alimentarios por mamiacuteferos

medianos y pequentildeos del desierto del Monte PhD dissertation Uni-

versidad Nacional de Coacuterdoba Coacuterdoba Argentina

Capurro HA Bucher EH 1982 Poblaciones de aves graniacutevoras y disponi-

bilidad de semillas en el bosque chaquentildeo de Chamical Ecosur 9

117ndash131

Childs S Goodall DW 1973 Seed reserves of desert soils Logan (UT)

Utah State University USIBP Desert Biome Research Memorandum

73-5

Claver S Fowler HG 1993 The ant fauna (Hymenoptera Formicidae) of

the Ntildeacuntildeaacuten Biosphere Reserve Naturalia 18 189ndash193

Dellafiore CM Polop JJ 1994 Feeding habits of Calomys musculinus in the

crop fields and its borders Mastozoolog iacutea Neotropical (Argentina) 1

45ndash50

Dye AJ 1969 Germination potentials and accumulation of native plant

seeds from southern New Mexico Masterrsquos thesis New Mexico State

University Las Cruces NM

Holldobler B Wilson EO 1990 The Ants Cambridge (MA) Harvard Uni-

versity Press

Jaksic FM 1989 Opportunist selective and other often-confused terms in

the predation literature Revista Chilena de Historia Natural 62 7ndash8

Kelrick MI MacMahon JA Parmenter RR Sisson DV 1986 Native seed

preferences of shrubndashsteppe rodents birds and ants The relationships

of seed attributes and seed use Oecologia 68 327ndash337

Kelt DA Brown JH Heske EJ Marquet PA Morton SR Reid JRW Rogovin

KA Shenbrot G 1996 Community structure of desert small mam-

mals Comparisons across four continents Ecology 77 746ndash761

Kemp PR 1989 Seed bank and vegetation processes in deserts Pages

257ndash281 in Allessio-Leck M Parker VT Simpson RL eds Ecology of

Soil Seed Banks San Diego (CA) Academic Press

Kerley GIH 1991 Seed removal by rodents birds and ants in the semi-arid

Karoo South Africa Journal of Arid Environments 20 63ndash69

______ 1992 Small mammal seed consumption in the Karoo South

Africa Further evidence for divergence in desert biotic processes

Oecologia 89 471ndash475

Kerley GIH Whitford WG 1994 Desert-dwelling small mammals as grani-

vores Intercontinental variations Australian Journal of Zoology 42

543ndash555

Kerley GIH Whitford WG Kay FR 1997 Mechanisms for the keystone sta-

February 2000 Vol 50 No 2 BioScience 131

Articles

1995 we recorded 12 and 14 species removing seeds fromtwo nearby sites This species richness exceeded the meanof 98 (n = 11 sites) and 28 (n = 5 sites) reported for thenorthern Monte Desert and central Chile respectively(Medel and Vaacutesquez 1994) as well as the mean of 52 (n =10 sites) and 85 (n = 16 sites) reported for North Ameri-can and Australian deserts respectively (Morton andDavidson 1988) In summary direct foraging observationof ants is not in agreement with previous assertions thatgranivorous ants are depauperate in the Monte Desert

The bait removal method employed in all these studiesis sensitive to the definition of ldquoharvester antrdquo used If antspecies are considered to be seed harvesters simply becausethey are seen at seed stations then the number of har-vester ant species may be overestimated By contrast wecounted only ants that effectively loaded seeds from seedstations Consequently we conclude that assemblages ofpotentially seed-harvesting ants are not depauperate atleast in the central Monte Desert

The South American ant assemblages however includeseveral species with more generalist diets than those of the

obligate seed-harvester ants of the genus Pogonomyrmexwhich make up the bulk of ant assemblages in NorthAmerican deserts Although Mares and Rosenzweig(1978) Medel (1995) and Medel and Vaacutesquez (1994) allhypothesized that omnivory of the ant species in SouthAmerican deserts results from a lower seed availability inthese deserts than in North American deserts the figuresin Table 1 do not support this explanation Indeed Pogon-omyrmex species exist in South America as well The threePogonomyrmex species (P rastratus P pronotalis and Pinermis) that occur in the central Monte Desert (Claverand Fowler 1993) appear to be highly specialized grani-vores (Javier Lopez de Casenave Silvia Claver Viacutector RCueto Luis Marone unpublished data) However giventhat the South American species of this genus seem to dis-play smaller colonies and lower population densities thanthose in North America (Holldobler and Wilson 1990) thehypothesis of a lower impact of South American Pogono-myrmex species on seeds (naturally available as well asoffered in baits) is a plausible although still unexploredhypothesis

February 2000 Vol 50 No 2 BioScience 127

Articles

Figure 3 A feeding station used in bait removalexperiments (Lopez de Casenave et al 1998) A known

amount of seeds is offered in each station at the start of thetrial Every station consists of three plastic Petri dishes (9cm in diameter) a ldquomammalrdquo tray a ldquobirdrdquo tray and an

ldquoantrdquo tray Vertebrate trays are glued to the top of longplastic cylinders and set 2ndash3 cm above the ground to

prevent access by ants Seeds for birds are available onlyduring the day and seeds for mammals are available only

at night Ant trays are buried with the rim of the Petri dishlevel with the soil surface and covered with mesh hardware

cloth to prevent access by vertebrates (these trays remainactive 24 hours a day) The stations are periodically

replenished with known amounts of seeds to avoidtotaldepletion (total duration of the experiment is 48 hours)

Region Granivore ranking Reference

North America (Sonora Desert) M gt A gt B Mares and Rosenzweig 1978Israel (Negev Desert) M gt Ac Abramsky 1983South Africa (Karoo Desert) A gt M gt B Kerley 1991Australia (Simpson Desert) A gt B gt M Morton 1985Chile (dense matorral) A gt B gt M Vaacutesquez et al 1995Chile (sparse matorral) B = A gt M Vaacutesquez et al 1995Argentina (central Monte Desert)

Under-canopy sites A gt B gt M Lopez de Casenave et al 1998Open sites B = A = M Lopez de Casenave et al 1998

Argentina (Southern Monte Desert) B gt M = A Sergio L Saba personalcommunication

Argentina (Northern Monte Desert) A gt B = M Mares and Rosenzweig 1978aExpanded from Vaacutesquez et al (1995)bAccording to Vaacutesquez et al (1995) we considered two taxa to have different granivory intensities when the average seed removal rate of one was at leasttwice that of the othercThis study was carried out only during springndashsummer birds were thought to have a negligible influence and were therefore not studied

Table 2a Rankings of the relative importance of the three main granivore taxa (A ants B birds M small mammals) assuggested by bait removal experiments carried out in different arid regions of the worldb

Low population densities of Pogonomyrmex ants andgeneralized food habits among some other ant speciesmight explain why the Monte Desertrsquos granivorous antsappear to remove fewer seeds from experimental baitsthan do North American ants But it does not follow thatthe ants of the Monte Desert ldquoare depauperate and notusually granivorousrdquo (Mares and Rosenzweig 1978) Tounderstand whether differences in seed removal from arti-ficial baits reflect intercontinental differences in antgranivory it will be necessary to examine more closely theforaging behavior of the Monte Desertrsquos ants For examplepreliminary observations indicate that some Pogono-myrmex species of the Monte Desert harvest the majorityof their seeds directly from plant stalks At the same timethe frequency of individuals of these highly specializedseed-eating species was very low at experimental seed sta-tions located on the soil (Javier Lopez de Casenave SilviaClaver Viacutector R Cueto Luis Marone unpublished data)Subtle differences in ant foraging behavior among conti-nents might reduce the comparability of results from thiskind of experiment thus affecting the conclusions aboutthe importance of granivorous ants as seed harvesters

Studies of seed removal from bait stations and of foodhabits of putative granivorous animals are necessary butnot sufficient to make inferences about the communityrole of granivores One straightforward approach to deter-mine the community role of those animals is to directlyassess the extent to which the dynamics of the resource(ie seeds) is affected by the activity of the consumer (iebirds ants or mammals) That is the importance ofgranivory can be better addressed through mechanismicstudies of the effects of seed consumption on the fate ofnaturally dispersed seeds (Price and Joyner 1997 Maroneet al 1998b)

Granivorous mammal assemblagesThe absence of functional analogues of North Americarsquosheteromyid rodents and the low diversity and abundanceof other mammalian granivores in South Americandeserts have been blamed for the ldquoinsignificantrdquo mam-malian seed consumption recorded in the northern MonteDesert (Mares et al 1977 Mares and Rosenzweig 1978Brown and Ojeda 1987) Recent studies however suggestthat this rate of seed consumption does not apply to theentire Monte Desert rodents remove almost an order ofmagnitude more seeds in the central Monte Desert than inthe northern Monte Desert (Lopez de Casenave et al1998) Mammalian seed removal is also markedly higherin the southern Monte than in Andalgalaacute (Sergio L Sabapersonal communication) Thus even if South Americatruly lacks analogues of heteromyids the premise thatrodent granivory is insignificant in the Monte Desert over-all deserves scrutiny for at least two reasons

First the spacious cheek pouches of heteromyidsenhance their fabled proficiency at gathering and hoard-ing seeds In a study of several heteromyid species indi-

viduals on average filled their cheek pouches to more than90 of pouch capacity during a single feeding bout in thefield (Vander Wall et al 1997) On a daily basis thereforethese rodents may harvest far more seeds than they needto fulfill their immediate energy requirements Althoughsome South American rodents have been shown to hoardsome seeds at least under laborator y conditions (Vaacutesquez1996) these species lack cheek pouches (Nowak and Par-adiso 1983) It follows that on average South Americanrodents would be expected to harvest fewer seeds frombaits than do heteromyids Some indirect evidence seemsto corroborate this assertion Predavecrsquos (1997) estimatesof seed consumption by Australian desert rodents (whichlike South American rodents lack cheek pouches) weredramatically higher when based on calculations of ener-getics than when based on bait removal experiments

Another reason for caution with previous generaliza-tions about mammal granivory in South America is thatbasic dietary information is still lacking for South Ameri-can desert rodents and desert ecologists often disagreeabout their food habits Although this discrepancy some-times simply reflects the fact that the proportion of seedsin animalsrsquo diets varies widely in time and space disagree-ment is also fostered by the lack of dietary informationThis lack of information is a major problem because somecalculatio ns of seed consumption (eg those based onenergetics) are sensitive to subtle variations in dietary val-ues (Kerley 1992) Hence terms such as ldquogranivorerdquo arenot always used in a consistent way Strictly speaking aselective consumer (eg a granivorous mammal) is ananimal that takes some or all food items in different pro-portions than the proportions at which they are present inthe patches where the animal feeds within the size limitsimposed by the perceptive handling and swallowingcapabilities of the consumer (Jaksic 1989)

Because this definition is difficult to apply in natureother more rudimentary ones could be used providedthat they are used only as a basis of comparative assess-ments For example Kerley and Whitford (1994) suggest-ed that mammals can be designated as granivores folivoresor insectivores when their diets are dominated by therespective dietary category (ie more than 50 of the dietconsists of the category) whereas those of more mixed dietscan be termed omnivores Using this criterion Meserve(1981a) showed that two rodent species in the southernfringe of the Atacama Desert of Chile Oligoryzomys longi-caudatus and Phyllotis darwini were granivorous especiallyin the dry season when 73 and 59 respectively of theiridentified diets consisted of seeds Abrothrix (Akodon) oli-vaceus almost achieved granivore status with 45 of itsdiet consisting of seeds Similarly Pizzimenti and De Salle(1980) found that in several localities of the Andes ofsouthern Peruacute more than 50 of the diet of some rodentspecies consisted of seeds (eg Phyllotis darwini 53 Ppictus 60) Given that some heteromyid rodents that areusually considered specialized seedeaters also consume sig-

128 BioScience February 2000 Vol 50 No 2

Articles

nificant amounts of insects and green vegetation duringsome seasons (Mares 1993a) it appears that some of theabove-mentioned Atacama and Altiplano rodent speciesshould also be considered granivores

In the Monte Desert Mares et al (1977) and Mares(1993b) reported finding no granivorous small mammalsIn some localities of the central Monte Desert howeverCalomys musculinus may be the most abundant rodentspecies (Ojeda 1989) and data from other semi-arid habi-tats of Argentina show that the dry-season diet of C mus-culinus consists of approximately 90 seeds (Dellafioreand Polop 1994) In a recent study in the central MonteDesert Campos (1997) found that during the dry seasonC musculinus appeared to consume a relatively high pro-portion of seeds (50) and that the diets of other smallmammals included few seeds (less than 5 in the diets ofGraomys griseoflavus Eligmodontia typus Thylamys pusil-lus and Akodon molinae) However these low values mayseverely underestimate the proportion of seeds in the dietof C musculinus and the other small mammals FirstCampos (1997) indicated that the microhistological tech-nique that she had employed underestimates food itemsother than leavesmdashin particular seeds Second Campos(1997) tallied seeds in stomach contents by counting onlythe glume remains of grass diaspores however rodentsoften dehusk grass diaspores and discard the glume beforeconsumption (Martha J Piantanida Divisioacuten Mastozo-ologiacutea Museo Argentino de Ciencias Naturales BuenosAires Argentina personal communication) Finallyrodents consume forb seeds as well as grass seeds Forinstance 43 of the diet of C musculinus in west-centralArgentina consists of Chenopodium seeds and 22 of itconsists of Amaranthus seeds (Dellafiore and Polop 1994)

North American species of the heteromyid generaMicrodipodops and Dipodomys are usually labeled as spe-cialized granivores (eg Kelt et al 1996) Neverthelessthey also consume insects and green vegetation (Mares1993a Kerley and Whitford 1994) Moreover Kerley et al(1997) have proposed that the keystone status of kangaroorats in the Chihuahuan Desert might be due tograminivory (ie herbivory) rather than to granivory Bycontrast those South American rodents (eg several Olig-oryzomys Calomys and Phyllotis species) that appear todisplay similar seasonal changes in diet (granivorous atsome times herbivorousinsectivorous at others) arealmost never labeled ldquogranivoresrdquo in the literature

This semantic inconsistency which has implications forthe conclusions of comparative studies may reflect anunfortunate attribute of research practice that deserves thescrutiny of the sociologists of science when basic empiri-cal information on a particular subject is lacking or frag-mentary unproven assertions may gain credence as factseven though such assertions are only at best plausibleassumptions This problem however should fade awaywhen these basic assumptions (eg that the ability ofrodents to harvest clumped seeds is similar in North andSouth America or that the incidence of seeds in the diet ofSouth American rodents is negligible) are carefully testedbefore deciding about the suitability of the specifichypothesis under scrutiny (eg that seed-eating mammalsin the Monte Desert and other South American desertshave a significant impact on seed reserves) This researchstrategy is essential to preventing ldquonaive refutationismrdquo(Lakatos 1978) in which a specific hypothesis is consid-ered false simply by the refutation of just one of its pre-dictions (eg that South American small mammalsremove similar amounts of seeds offered in bait experi-ments as their North American counterparts)

Granivorous bird assemblagesThe low rates of seed removal by birds observed in baitremoval experiments seemed to suggest that birds areeither unimportant seedeaters in deserts or that they fail todetect the experimentally proffered trays For examplebirds ate few of the test seeds in the South African Karoo(Kerley 1991) the Chihuahuan Desert (Parmenter et al1984) and the Australian Desert (Morton 1985) Giventhe diverse and abundant avian granivores of Australiandeserts Morton (1985 1993) conjectured that these birdsshould have a major community role in Australian desertseven though they did not visit any of his seed stations Sev-eral authors have suggested that the short time span of baitremoval experiments (2ndash3 days) may be inadequate for

February 2000 Vol 50 No 2 BioScience 129

Articles

Figure 4 Seasonal rates of seed removal by granivores inthe central Monte Desert Birds open circles ants solid

circles mammals open triangles Mean rates of removalfor the 23ndash25 trays available only to the respective taxonare shown Within a season means with the same letter

are not significantly different according to Tukeyrsquos test ( Plt 005) Figure redrawn from Lopez de Casenave et al

(1998) and used with permission from Blackwell Science

measuring seed consumption by desert birds (Mares andRosenzweig 1978 Morton 1985)

In most bait experiments carried out in South Americandeserts however avian granivores quickly discovered baitsand consumed seeds Indeed birds often consumed moreseeds than did the other granivore taxa (Table 2) We knowof no idiosyncratic characteristic of South American birdsthat may explain this pattern Thus to control for anypropensity of the Monte avifauna to detect seed trays withunusual skills we used an approach that did not rely on arti-ficial baits to assess whether birds are important seedeatersin the central Monte Desert (Marone et al 1998b)

Bait experiments have shown that bird granivores arethe main autumnndashwinter seed consumers in the centralMonte Desert (Figure 4 see Lopez de Casenave et al1998) To assess the impact of seed-eating birds on theautumnndashwinter soil seed reserves we compared the soilseed bank in the late summer of 1995 (12 February) withthat present the following early spring (25 October) alsotaking into account the total number of seeds that enteredthe soil from late summer to early spring (ie we mea-sured seed rain Marone et al 1998b) In late summerbefore consumption by birds the mean seed density ofgrass seed banks was 2400 seedsm2 or 036 gm2 The nextspringmdashfollowing the input of approximately 3000 grassseedsm2 or 071 gm2 as well as the period of bird con-sumption in autumn and wintermdashthe density of grassseeds was 2700 seedsm2 or 039 gm2 Medium and largegrass seeds suffered higher postdispersal losses than didsmall seeds Likewise densities of forb seeds in the seedbank were statistically indistinguishable between late sum-mer (5500 seedsm2 or 134 gm2) and spring (6500seedsm2 or 153 gm2) although forb seed productionduring the study period had been relatively low (400seedsm2 or 012 gm 2) These results suggest thatautumnndashwinter seed predators in the central MonteDesert favor grass seeds over forb seeds

Several lines of evidence confirm that postdispersalgrass seed loss during autumnndashwinter in the centralMonte Desert is due mainly to vertebrate consumptionFirst granivorous ants are active almost exclusively during

the spring and summer (Figure 4 Lopez de Casenave et al1998) Furthermore C4 grasses germinate mostly in latespring and summer and total grass seed germinationwhich usually does not surpass 05 of previous soil seedreserves (Marone et al 1998b) reached only 5 of previ-ous reserves during the exceptionally wet summer of 1998which was associated with a strong El NintildeoSouthernOscillation event (Luis Marone Manuel E Horno RafaelGonzaacutelez del Solar unpublished data) Finally given thecomposition of the seed bank at different depths (0ndash2 cm2ndash4 cm and 4ndash6 cm) Marone et al (1998a) concludedthat grass seeds especially the medium and large seedswould suffer negligible loss by deep burial

Therefore it was not surprising that the pattern of seedlosses coincided with the pattern of seed consumption bygranivorous birds in the autumns and winters of 1993through 1995 Nearly 93 of the seed mass in bird stom-achs came from grass seeds and only 7 came from forbseeds Furthermore medium and large grass seeds sufferedthe highest losses from the soil seed bank and were also themain target of foraging by granivores Moreover a signifi-cant positive correlation existed across grass speciesbetween the mass decrease of seed species from the soiltoward spring and the mass of those seed species in birddiets in autumnndashwinter (Figure 5 Marone et al 1998b)This positive correlation suggests that bird consumptioncould explain a great deal of the autumnndashwinter grass seedloss observed in soils of the central Monte Desert

These lines of evidence indicate that vertebrate grani-vores (particularly birds) have a major impact on theabundance floristic composition and size distribution ofseed reserves in the Monte Desert where vertebrategranivory in general and avian granivory in particularhad previously been considered unimportant Moreovernewly produced seeds from perennial grasses constitute amajor fraction of autumnndashwinter bird diet This findingsupports the proposal (Marone 1992) that the timing andamount of rainfall in the central Monte Desert may great-ly influence the abundance and migrations of granivorousbirds via the opportunistic response of seed production bygrasses to variations in rainfall Population interactions

130 BioScience February 2000 Vol 50 No 2

Articles

Figure 5 Relationship between the mass of seeds fromperennial grasses in the autumn and winter diets (in1993ndash1995) of four granivorous bird species in the centralMonte Desert and the loss of seeds of each species during theautumn and winter of 1995 The bird species are Zonotrichiacapensis Phrygilus carbonarius Diuca diuca andSaltatricula multicolor The overall correlation wassignificant (r = 087 n = 11 P lt 0001) Grass species are asfollows Pap Pappophorum spp Set Setaria leucopila DigDigitaria californica Tri Trichloris crinita Dip Diplachnedubia Spo Sporobolus cryptandrus Ari Aristida spp NeoNeobouteloua lophostachya Chl Chloris castilloniana BouBouteloua spp The point for Stipa spp is not shown on thefigure but overlaps with that for Bouteloua spp

between seeds and avian granivores in this South Ameri-can desert may therefore be more important than hithertoappreciated

Concluding remarksThe relative importance of seed consumption or granivo-rous assemblages in deserts around the world cannot beassessed through one research approach alone (eg baitremoval experiments energetics approaches descriptionsof the species composition of granivorous assemblages orquantification of individualsrsquo diets) Instead research pro-grams that include multiple approaches involving redun-dancy and cross-checks of hypotheses and methods maylead to the most robust conclusions and therefore to syn-thesis and integration (Pickett et al 1994) Furthermoreany such program should involve long-term studies thattake into account the spatial and temporal variability ofnatural communities

Partly as a consequence of such a lack of integrationnatural rates of seed consumption and the abundance anddiversity of granivorous assemblages in some South Amer-ican deserts may have been underestimated in the pastThe evidence we have discussed in this article comes fromvarious desert locations of southern South America andwas obtained by using different research approaches Thisevidence suggests that birds and ants are importantseedeaters during the colder and warmer months respec-tively and that the role of small mammals as granivores inthe central Monte Desert of Argentina deserves moredetailed assessment These results should be readily incor-porated into comparative studies to distinguish betweenidiosyncratic and general processes molding desert com-munities worldwide Although ecological ldquolawsrdquo are by nomeans universal ecological understanding will continueto depend on theory development (Pickett et al 1994Mahner and Bunge 1997) To develop ecological theoryresearchers need good observations combined with rigor-ous and realistic experiments carried out in the context ofresearch programs that are focused whenever possible ontesting mechanisms to account for ecological phenomena(Werner 1998)

AcknowledgmentsWe acknowledge Sergio Camiacuten Silvia Claver RafaelGonzaacutelez del Solar Fernando Milesi Martha J PiantanidaBertilde Rossi Eduardo Tomaacutes-Mezquida and GualbertoZalazar for their constructive and pleasant cooperationduring field and laborator y work Manuel E Horno andIris Peralta contributed partnership and stimulating dis-cussion at the initial (and more chaotic) stages of ourstudies we are especially indebted to both of them SergioL Saba was kind enough to let us use his unpublisheddata First drafts of the manuscript were greatly improvedthrough critical review from Rebecca Chasan Chris Dick-man Pete Feinsinger Lali Guichoacuten Rafael Gonzaacutelez delSolar Fabiaacuten Jaksic Graham Kerley Fernando Milesi

Stephen Morton Mary V Price Julian Reid AlejandraRibichich Rodrigo Vaacutesquez and four anonymous review-ers At different stages field and laboratory work werefinanced by the Man and the Biosphere Programme Unit-ed Nations Educational Scientific and Cultural Organiza-tion the Association of Field Ornithologists Programa deCiencias Naturales Museo Argentino de Ciencias Natu-rales ldquoBernardino Rivadaviardquo IADIZA-Provincia de Men-doza and the Argentine funding agencies CONICET (PEI032797) and Agencia Nacional de Promocioacuten Cientiacutefica yTecnoloacutegica (PICT 01-03187) L M acknowledges CON-ICET and the Canadian Government for financial sup-port and Mario Bunge for the stimulating environment atMcGill University where the final version of this paperwas written This article is Contribution No 8 of theDesert Community Ecology Research Team Plant Eco-physiology Department IADIZA Institute

References citedAbramsky Z 1983 Experiments on seed predation by rodents and ants in

the Israeli desert Oecologia 57 328ndash332

Brown JH Ojeda RA 1987 Granivory Patterns processes and conse-

quences of seed consumption on two continents Revista Chilena de

Historia Natural 60 337ndash349

Campos CM 1997 Utilizacioacuten de recursos alimentarios por mamiacuteferos

medianos y pequentildeos del desierto del Monte PhD dissertation Uni-

versidad Nacional de Coacuterdoba Coacuterdoba Argentina

Capurro HA Bucher EH 1982 Poblaciones de aves graniacutevoras y disponi-

bilidad de semillas en el bosque chaquentildeo de Chamical Ecosur 9

117ndash131

Childs S Goodall DW 1973 Seed reserves of desert soils Logan (UT)

Utah State University USIBP Desert Biome Research Memorandum

73-5

Claver S Fowler HG 1993 The ant fauna (Hymenoptera Formicidae) of

the Ntildeacuntildeaacuten Biosphere Reserve Naturalia 18 189ndash193

Dellafiore CM Polop JJ 1994 Feeding habits of Calomys musculinus in the

crop fields and its borders Mastozoolog iacutea Neotropical (Argentina) 1

45ndash50

Dye AJ 1969 Germination potentials and accumulation of native plant

seeds from southern New Mexico Masterrsquos thesis New Mexico State

University Las Cruces NM

Holldobler B Wilson EO 1990 The Ants Cambridge (MA) Harvard Uni-

versity Press

Jaksic FM 1989 Opportunist selective and other often-confused terms in

the predation literature Revista Chilena de Historia Natural 62 7ndash8

Kelrick MI MacMahon JA Parmenter RR Sisson DV 1986 Native seed

preferences of shrubndashsteppe rodents birds and ants The relationships

of seed attributes and seed use Oecologia 68 327ndash337

Kelt DA Brown JH Heske EJ Marquet PA Morton SR Reid JRW Rogovin

KA Shenbrot G 1996 Community structure of desert small mam-

mals Comparisons across four continents Ecology 77 746ndash761

Kemp PR 1989 Seed bank and vegetation processes in deserts Pages

257ndash281 in Allessio-Leck M Parker VT Simpson RL eds Ecology of

Soil Seed Banks San Diego (CA) Academic Press

Kerley GIH 1991 Seed removal by rodents birds and ants in the semi-arid

Karoo South Africa Journal of Arid Environments 20 63ndash69

______ 1992 Small mammal seed consumption in the Karoo South

Africa Further evidence for divergence in desert biotic processes

Oecologia 89 471ndash475

Kerley GIH Whitford WG 1994 Desert-dwelling small mammals as grani-

vores Intercontinental variations Australian Journal of Zoology 42

543ndash555

Kerley GIH Whitford WG Kay FR 1997 Mechanisms for the keystone sta-

February 2000 Vol 50 No 2 BioScience 131

Articles

Low population densities of Pogonomyrmex ants andgeneralized food habits among some other ant speciesmight explain why the Monte Desertrsquos granivorous antsappear to remove fewer seeds from experimental baitsthan do North American ants But it does not follow thatthe ants of the Monte Desert ldquoare depauperate and notusually granivorousrdquo (Mares and Rosenzweig 1978) Tounderstand whether differences in seed removal from arti-ficial baits reflect intercontinental differences in antgranivory it will be necessary to examine more closely theforaging behavior of the Monte Desertrsquos ants For examplepreliminary observations indicate that some Pogono-myrmex species of the Monte Desert harvest the majorityof their seeds directly from plant stalks At the same timethe frequency of individuals of these highly specializedseed-eating species was very low at experimental seed sta-tions located on the soil (Javier Lopez de Casenave SilviaClaver Viacutector R Cueto Luis Marone unpublished data)Subtle differences in ant foraging behavior among conti-nents might reduce the comparability of results from thiskind of experiment thus affecting the conclusions aboutthe importance of granivorous ants as seed harvesters

Studies of seed removal from bait stations and of foodhabits of putative granivorous animals are necessary butnot sufficient to make inferences about the communityrole of granivores One straightforward approach to deter-mine the community role of those animals is to directlyassess the extent to which the dynamics of the resource(ie seeds) is affected by the activity of the consumer (iebirds ants or mammals) That is the importance ofgranivory can be better addressed through mechanismicstudies of the effects of seed consumption on the fate ofnaturally dispersed seeds (Price and Joyner 1997 Maroneet al 1998b)

Granivorous mammal assemblagesThe absence of functional analogues of North Americarsquosheteromyid rodents and the low diversity and abundanceof other mammalian granivores in South Americandeserts have been blamed for the ldquoinsignificantrdquo mam-malian seed consumption recorded in the northern MonteDesert (Mares et al 1977 Mares and Rosenzweig 1978Brown and Ojeda 1987) Recent studies however suggestthat this rate of seed consumption does not apply to theentire Monte Desert rodents remove almost an order ofmagnitude more seeds in the central Monte Desert than inthe northern Monte Desert (Lopez de Casenave et al1998) Mammalian seed removal is also markedly higherin the southern Monte than in Andalgalaacute (Sergio L Sabapersonal communication) Thus even if South Americatruly lacks analogues of heteromyids the premise thatrodent granivory is insignificant in the Monte Desert over-all deserves scrutiny for at least two reasons

First the spacious cheek pouches of heteromyidsenhance their fabled proficiency at gathering and hoard-ing seeds In a study of several heteromyid species indi-

viduals on average filled their cheek pouches to more than90 of pouch capacity during a single feeding bout in thefield (Vander Wall et al 1997) On a daily basis thereforethese rodents may harvest far more seeds than they needto fulfill their immediate energy requirements Althoughsome South American rodents have been shown to hoardsome seeds at least under laborator y conditions (Vaacutesquez1996) these species lack cheek pouches (Nowak and Par-adiso 1983) It follows that on average South Americanrodents would be expected to harvest fewer seeds frombaits than do heteromyids Some indirect evidence seemsto corroborate this assertion Predavecrsquos (1997) estimatesof seed consumption by Australian desert rodents (whichlike South American rodents lack cheek pouches) weredramatically higher when based on calculations of ener-getics than when based on bait removal experiments

Another reason for caution with previous generaliza-tions about mammal granivory in South America is thatbasic dietary information is still lacking for South Ameri-can desert rodents and desert ecologists often disagreeabout their food habits Although this discrepancy some-times simply reflects the fact that the proportion of seedsin animalsrsquo diets varies widely in time and space disagree-ment is also fostered by the lack of dietary informationThis lack of information is a major problem because somecalculatio ns of seed consumption (eg those based onenergetics) are sensitive to subtle variations in dietary val-ues (Kerley 1992) Hence terms such as ldquogranivorerdquo arenot always used in a consistent way Strictly speaking aselective consumer (eg a granivorous mammal) is ananimal that takes some or all food items in different pro-portions than the proportions at which they are present inthe patches where the animal feeds within the size limitsimposed by the perceptive handling and swallowingcapabilities of the consumer (Jaksic 1989)

Because this definition is difficult to apply in natureother more rudimentary ones could be used providedthat they are used only as a basis of comparative assess-ments For example Kerley and Whitford (1994) suggest-ed that mammals can be designated as granivores folivoresor insectivores when their diets are dominated by therespective dietary category (ie more than 50 of the dietconsists of the category) whereas those of more mixed dietscan be termed omnivores Using this criterion Meserve(1981a) showed that two rodent species in the southernfringe of the Atacama Desert of Chile Oligoryzomys longi-caudatus and Phyllotis darwini were granivorous especiallyin the dry season when 73 and 59 respectively of theiridentified diets consisted of seeds Abrothrix (Akodon) oli-vaceus almost achieved granivore status with 45 of itsdiet consisting of seeds Similarly Pizzimenti and De Salle(1980) found that in several localities of the Andes ofsouthern Peruacute more than 50 of the diet of some rodentspecies consisted of seeds (eg Phyllotis darwini 53 Ppictus 60) Given that some heteromyid rodents that areusually considered specialized seedeaters also consume sig-

128 BioScience February 2000 Vol 50 No 2

Articles

nificant amounts of insects and green vegetation duringsome seasons (Mares 1993a) it appears that some of theabove-mentioned Atacama and Altiplano rodent speciesshould also be considered granivores

In the Monte Desert Mares et al (1977) and Mares(1993b) reported finding no granivorous small mammalsIn some localities of the central Monte Desert howeverCalomys musculinus may be the most abundant rodentspecies (Ojeda 1989) and data from other semi-arid habi-tats of Argentina show that the dry-season diet of C mus-culinus consists of approximately 90 seeds (Dellafioreand Polop 1994) In a recent study in the central MonteDesert Campos (1997) found that during the dry seasonC musculinus appeared to consume a relatively high pro-portion of seeds (50) and that the diets of other smallmammals included few seeds (less than 5 in the diets ofGraomys griseoflavus Eligmodontia typus Thylamys pusil-lus and Akodon molinae) However these low values mayseverely underestimate the proportion of seeds in the dietof C musculinus and the other small mammals FirstCampos (1997) indicated that the microhistological tech-nique that she had employed underestimates food itemsother than leavesmdashin particular seeds Second Campos(1997) tallied seeds in stomach contents by counting onlythe glume remains of grass diaspores however rodentsoften dehusk grass diaspores and discard the glume beforeconsumption (Martha J Piantanida Divisioacuten Mastozo-ologiacutea Museo Argentino de Ciencias Naturales BuenosAires Argentina personal communication) Finallyrodents consume forb seeds as well as grass seeds Forinstance 43 of the diet of C musculinus in west-centralArgentina consists of Chenopodium seeds and 22 of itconsists of Amaranthus seeds (Dellafiore and Polop 1994)

North American species of the heteromyid generaMicrodipodops and Dipodomys are usually labeled as spe-cialized granivores (eg Kelt et al 1996) Neverthelessthey also consume insects and green vegetation (Mares1993a Kerley and Whitford 1994) Moreover Kerley et al(1997) have proposed that the keystone status of kangaroorats in the Chihuahuan Desert might be due tograminivory (ie herbivory) rather than to granivory Bycontrast those South American rodents (eg several Olig-oryzomys Calomys and Phyllotis species) that appear todisplay similar seasonal changes in diet (granivorous atsome times herbivorousinsectivorous at others) arealmost never labeled ldquogranivoresrdquo in the literature

This semantic inconsistency which has implications forthe conclusions of comparative studies may reflect anunfortunate attribute of research practice that deserves thescrutiny of the sociologists of science when basic empiri-cal information on a particular subject is lacking or frag-mentary unproven assertions may gain credence as factseven though such assertions are only at best plausibleassumptions This problem however should fade awaywhen these basic assumptions (eg that the ability ofrodents to harvest clumped seeds is similar in North andSouth America or that the incidence of seeds in the diet ofSouth American rodents is negligible) are carefully testedbefore deciding about the suitability of the specifichypothesis under scrutiny (eg that seed-eating mammalsin the Monte Desert and other South American desertshave a significant impact on seed reserves) This researchstrategy is essential to preventing ldquonaive refutationismrdquo(Lakatos 1978) in which a specific hypothesis is consid-ered false simply by the refutation of just one of its pre-dictions (eg that South American small mammalsremove similar amounts of seeds offered in bait experi-ments as their North American counterparts)

Granivorous bird assemblagesThe low rates of seed removal by birds observed in baitremoval experiments seemed to suggest that birds areeither unimportant seedeaters in deserts or that they fail todetect the experimentally proffered trays For examplebirds ate few of the test seeds in the South African Karoo(Kerley 1991) the Chihuahuan Desert (Parmenter et al1984) and the Australian Desert (Morton 1985) Giventhe diverse and abundant avian granivores of Australiandeserts Morton (1985 1993) conjectured that these birdsshould have a major community role in Australian desertseven though they did not visit any of his seed stations Sev-eral authors have suggested that the short time span of baitremoval experiments (2ndash3 days) may be inadequate for

February 2000 Vol 50 No 2 BioScience 129

Articles

Figure 4 Seasonal rates of seed removal by granivores inthe central Monte Desert Birds open circles ants solid

circles mammals open triangles Mean rates of removalfor the 23ndash25 trays available only to the respective taxonare shown Within a season means with the same letter

are not significantly different according to Tukeyrsquos test ( Plt 005) Figure redrawn from Lopez de Casenave et al

(1998) and used with permission from Blackwell Science

measuring seed consumption by desert birds (Mares andRosenzweig 1978 Morton 1985)

In most bait experiments carried out in South Americandeserts however avian granivores quickly discovered baitsand consumed seeds Indeed birds often consumed moreseeds than did the other granivore taxa (Table 2) We knowof no idiosyncratic characteristic of South American birdsthat may explain this pattern Thus to control for anypropensity of the Monte avifauna to detect seed trays withunusual skills we used an approach that did not rely on arti-ficial baits to assess whether birds are important seedeatersin the central Monte Desert (Marone et al 1998b)

Bait experiments have shown that bird granivores arethe main autumnndashwinter seed consumers in the centralMonte Desert (Figure 4 see Lopez de Casenave et al1998) To assess the impact of seed-eating birds on theautumnndashwinter soil seed reserves we compared the soilseed bank in the late summer of 1995 (12 February) withthat present the following early spring (25 October) alsotaking into account the total number of seeds that enteredthe soil from late summer to early spring (ie we mea-sured seed rain Marone et al 1998b) In late summerbefore consumption by birds the mean seed density ofgrass seed banks was 2400 seedsm2 or 036 gm2 The nextspringmdashfollowing the input of approximately 3000 grassseedsm2 or 071 gm2 as well as the period of bird con-sumption in autumn and wintermdashthe density of grassseeds was 2700 seedsm2 or 039 gm2 Medium and largegrass seeds suffered higher postdispersal losses than didsmall seeds Likewise densities of forb seeds in the seedbank were statistically indistinguishable between late sum-mer (5500 seedsm2 or 134 gm2) and spring (6500seedsm2 or 153 gm2) although forb seed productionduring the study period had been relatively low (400seedsm2 or 012 gm 2) These results suggest thatautumnndashwinter seed predators in the central MonteDesert favor grass seeds over forb seeds

Several lines of evidence confirm that postdispersalgrass seed loss during autumnndashwinter in the centralMonte Desert is due mainly to vertebrate consumptionFirst granivorous ants are active almost exclusively during

the spring and summer (Figure 4 Lopez de Casenave et al1998) Furthermore C4 grasses germinate mostly in latespring and summer and total grass seed germinationwhich usually does not surpass 05 of previous soil seedreserves (Marone et al 1998b) reached only 5 of previ-ous reserves during the exceptionally wet summer of 1998which was associated with a strong El NintildeoSouthernOscillation event (Luis Marone Manuel E Horno RafaelGonzaacutelez del Solar unpublished data) Finally given thecomposition of the seed bank at different depths (0ndash2 cm2ndash4 cm and 4ndash6 cm) Marone et al (1998a) concludedthat grass seeds especially the medium and large seedswould suffer negligible loss by deep burial

Therefore it was not surprising that the pattern of seedlosses coincided with the pattern of seed consumption bygranivorous birds in the autumns and winters of 1993through 1995 Nearly 93 of the seed mass in bird stom-achs came from grass seeds and only 7 came from forbseeds Furthermore medium and large grass seeds sufferedthe highest losses from the soil seed bank and were also themain target of foraging by granivores Moreover a signifi-cant positive correlation existed across grass speciesbetween the mass decrease of seed species from the soiltoward spring and the mass of those seed species in birddiets in autumnndashwinter (Figure 5 Marone et al 1998b)This positive correlation suggests that bird consumptioncould explain a great deal of the autumnndashwinter grass seedloss observed in soils of the central Monte Desert

These lines of evidence indicate that vertebrate grani-vores (particularly birds) have a major impact on theabundance floristic composition and size distribution ofseed reserves in the Monte Desert where vertebrategranivory in general and avian granivory in particularhad previously been considered unimportant Moreovernewly produced seeds from perennial grasses constitute amajor fraction of autumnndashwinter bird diet This findingsupports the proposal (Marone 1992) that the timing andamount of rainfall in the central Monte Desert may great-ly influence the abundance and migrations of granivorousbirds via the opportunistic response of seed production bygrasses to variations in rainfall Population interactions

130 BioScience February 2000 Vol 50 No 2

Articles

Figure 5 Relationship between the mass of seeds fromperennial grasses in the autumn and winter diets (in1993ndash1995) of four granivorous bird species in the centralMonte Desert and the loss of seeds of each species during theautumn and winter of 1995 The bird species are Zonotrichiacapensis Phrygilus carbonarius Diuca diuca andSaltatricula multicolor The overall correlation wassignificant (r = 087 n = 11 P lt 0001) Grass species are asfollows Pap Pappophorum spp Set Setaria leucopila DigDigitaria californica Tri Trichloris crinita Dip Diplachnedubia Spo Sporobolus cryptandrus Ari Aristida spp NeoNeobouteloua lophostachya Chl Chloris castilloniana BouBouteloua spp The point for Stipa spp is not shown on thefigure but overlaps with that for Bouteloua spp

between seeds and avian granivores in this South Ameri-can desert may therefore be more important than hithertoappreciated

Concluding remarksThe relative importance of seed consumption or granivo-rous assemblages in deserts around the world cannot beassessed through one research approach alone (eg baitremoval experiments energetics approaches descriptionsof the species composition of granivorous assemblages orquantification of individualsrsquo diets) Instead research pro-grams that include multiple approaches involving redun-dancy and cross-checks of hypotheses and methods maylead to the most robust conclusions and therefore to syn-thesis and integration (Pickett et al 1994) Furthermoreany such program should involve long-term studies thattake into account the spatial and temporal variability ofnatural communities

Partly as a consequence of such a lack of integrationnatural rates of seed consumption and the abundance anddiversity of granivorous assemblages in some South Amer-ican deserts may have been underestimated in the pastThe evidence we have discussed in this article comes fromvarious desert locations of southern South America andwas obtained by using different research approaches Thisevidence suggests that birds and ants are importantseedeaters during the colder and warmer months respec-tively and that the role of small mammals as granivores inthe central Monte Desert of Argentina deserves moredetailed assessment These results should be readily incor-porated into comparative studies to distinguish betweenidiosyncratic and general processes molding desert com-munities worldwide Although ecological ldquolawsrdquo are by nomeans universal ecological understanding will continueto depend on theory development (Pickett et al 1994Mahner and Bunge 1997) To develop ecological theoryresearchers need good observations combined with rigor-ous and realistic experiments carried out in the context ofresearch programs that are focused whenever possible ontesting mechanisms to account for ecological phenomena(Werner 1998)

AcknowledgmentsWe acknowledge Sergio Camiacuten Silvia Claver RafaelGonzaacutelez del Solar Fernando Milesi Martha J PiantanidaBertilde Rossi Eduardo Tomaacutes-Mezquida and GualbertoZalazar for their constructive and pleasant cooperationduring field and laborator y work Manuel E Horno andIris Peralta contributed partnership and stimulating dis-cussion at the initial (and more chaotic) stages of ourstudies we are especially indebted to both of them SergioL Saba was kind enough to let us use his unpublisheddata First drafts of the manuscript were greatly improvedthrough critical review from Rebecca Chasan Chris Dick-man Pete Feinsinger Lali Guichoacuten Rafael Gonzaacutelez delSolar Fabiaacuten Jaksic Graham Kerley Fernando Milesi

Stephen Morton Mary V Price Julian Reid AlejandraRibichich Rodrigo Vaacutesquez and four anonymous review-ers At different stages field and laboratory work werefinanced by the Man and the Biosphere Programme Unit-ed Nations Educational Scientific and Cultural Organiza-tion the Association of Field Ornithologists Programa deCiencias Naturales Museo Argentino de Ciencias Natu-rales ldquoBernardino Rivadaviardquo IADIZA-Provincia de Men-doza and the Argentine funding agencies CONICET (PEI032797) and Agencia Nacional de Promocioacuten Cientiacutefica yTecnoloacutegica (PICT 01-03187) L M acknowledges CON-ICET and the Canadian Government for financial sup-port and Mario Bunge for the stimulating environment atMcGill University where the final version of this paperwas written This article is Contribution No 8 of theDesert Community Ecology Research Team Plant Eco-physiology Department IADIZA Institute

References citedAbramsky Z 1983 Experiments on seed predation by rodents and ants in

the Israeli desert Oecologia 57 328ndash332

Brown JH Ojeda RA 1987 Granivory Patterns processes and conse-

quences of seed consumption on two continents Revista Chilena de

Historia Natural 60 337ndash349

Campos CM 1997 Utilizacioacuten de recursos alimentarios por mamiacuteferos

medianos y pequentildeos del desierto del Monte PhD dissertation Uni-

versidad Nacional de Coacuterdoba Coacuterdoba Argentina

Capurro HA Bucher EH 1982 Poblaciones de aves graniacutevoras y disponi-

bilidad de semillas en el bosque chaquentildeo de Chamical Ecosur 9

117ndash131

Childs S Goodall DW 1973 Seed reserves of desert soils Logan (UT)

Utah State University USIBP Desert Biome Research Memorandum

73-5

Claver S Fowler HG 1993 The ant fauna (Hymenoptera Formicidae) of

the Ntildeacuntildeaacuten Biosphere Reserve Naturalia 18 189ndash193

Dellafiore CM Polop JJ 1994 Feeding habits of Calomys musculinus in the

crop fields and its borders Mastozoolog iacutea Neotropical (Argentina) 1

45ndash50

Dye AJ 1969 Germination potentials and accumulation of native plant

seeds from southern New Mexico Masterrsquos thesis New Mexico State

University Las Cruces NM

Holldobler B Wilson EO 1990 The Ants Cambridge (MA) Harvard Uni-

versity Press

Jaksic FM 1989 Opportunist selective and other often-confused terms in

the predation literature Revista Chilena de Historia Natural 62 7ndash8

Kelrick MI MacMahon JA Parmenter RR Sisson DV 1986 Native seed

preferences of shrubndashsteppe rodents birds and ants The relationships

of seed attributes and seed use Oecologia 68 327ndash337

Kelt DA Brown JH Heske EJ Marquet PA Morton SR Reid JRW Rogovin

KA Shenbrot G 1996 Community structure of desert small mam-

mals Comparisons across four continents Ecology 77 746ndash761

Kemp PR 1989 Seed bank and vegetation processes in deserts Pages

257ndash281 in Allessio-Leck M Parker VT Simpson RL eds Ecology of

Soil Seed Banks San Diego (CA) Academic Press

Kerley GIH 1991 Seed removal by rodents birds and ants in the semi-arid

Karoo South Africa Journal of Arid Environments 20 63ndash69

______ 1992 Small mammal seed consumption in the Karoo South

Africa Further evidence for divergence in desert biotic processes

Oecologia 89 471ndash475

Kerley GIH Whitford WG 1994 Desert-dwelling small mammals as grani-

vores Intercontinental variations Australian Journal of Zoology 42

543ndash555

Kerley GIH Whitford WG Kay FR 1997 Mechanisms for the keystone sta-

February 2000 Vol 50 No 2 BioScience 131

Articles

nificant amounts of insects and green vegetation duringsome seasons (Mares 1993a) it appears that some of theabove-mentioned Atacama and Altiplano rodent speciesshould also be considered granivores

In the Monte Desert Mares et al (1977) and Mares(1993b) reported finding no granivorous small mammalsIn some localities of the central Monte Desert howeverCalomys musculinus may be the most abundant rodentspecies (Ojeda 1989) and data from other semi-arid habi-tats of Argentina show that the dry-season diet of C mus-culinus consists of approximately 90 seeds (Dellafioreand Polop 1994) In a recent study in the central MonteDesert Campos (1997) found that during the dry seasonC musculinus appeared to consume a relatively high pro-portion of seeds (50) and that the diets of other smallmammals included few seeds (less than 5 in the diets ofGraomys griseoflavus Eligmodontia typus Thylamys pusil-lus and Akodon molinae) However these low values mayseverely underestimate the proportion of seeds in the dietof C musculinus and the other small mammals FirstCampos (1997) indicated that the microhistological tech-nique that she had employed underestimates food itemsother than leavesmdashin particular seeds Second Campos(1997) tallied seeds in stomach contents by counting onlythe glume remains of grass diaspores however rodentsoften dehusk grass diaspores and discard the glume beforeconsumption (Martha J Piantanida Divisioacuten Mastozo-ologiacutea Museo Argentino de Ciencias Naturales BuenosAires Argentina personal communication) Finallyrodents consume forb seeds as well as grass seeds Forinstance 43 of the diet of C musculinus in west-centralArgentina consists of Chenopodium seeds and 22 of itconsists of Amaranthus seeds (Dellafiore and Polop 1994)

North American species of the heteromyid generaMicrodipodops and Dipodomys are usually labeled as spe-cialized granivores (eg Kelt et al 1996) Neverthelessthey also consume insects and green vegetation (Mares1993a Kerley and Whitford 1994) Moreover Kerley et al(1997) have proposed that the keystone status of kangaroorats in the Chihuahuan Desert might be due tograminivory (ie herbivory) rather than to granivory Bycontrast those South American rodents (eg several Olig-oryzomys Calomys and Phyllotis species) that appear todisplay similar seasonal changes in diet (granivorous atsome times herbivorousinsectivorous at others) arealmost never labeled ldquogranivoresrdquo in the literature

This semantic inconsistency which has implications forthe conclusions of comparative studies may reflect anunfortunate attribute of research practice that deserves thescrutiny of the sociologists of science when basic empiri-cal information on a particular subject is lacking or frag-mentary unproven assertions may gain credence as factseven though such assertions are only at best plausibleassumptions This problem however should fade awaywhen these basic assumptions (eg that the ability ofrodents to harvest clumped seeds is similar in North andSouth America or that the incidence of seeds in the diet ofSouth American rodents is negligible) are carefully testedbefore deciding about the suitability of the specifichypothesis under scrutiny (eg that seed-eating mammalsin the Monte Desert and other South American desertshave a significant impact on seed reserves) This researchstrategy is essential to preventing ldquonaive refutationismrdquo(Lakatos 1978) in which a specific hypothesis is consid-ered false simply by the refutation of just one of its pre-dictions (eg that South American small mammalsremove similar amounts of seeds offered in bait experi-ments as their North American counterparts)

Granivorous bird assemblagesThe low rates of seed removal by birds observed in baitremoval experiments seemed to suggest that birds areeither unimportant seedeaters in deserts or that they fail todetect the experimentally proffered trays For examplebirds ate few of the test seeds in the South African Karoo(Kerley 1991) the Chihuahuan Desert (Parmenter et al1984) and the Australian Desert (Morton 1985) Giventhe diverse and abundant avian granivores of Australiandeserts Morton (1985 1993) conjectured that these birdsshould have a major community role in Australian desertseven though they did not visit any of his seed stations Sev-eral authors have suggested that the short time span of baitremoval experiments (2ndash3 days) may be inadequate for

February 2000 Vol 50 No 2 BioScience 129

Articles

Figure 4 Seasonal rates of seed removal by granivores inthe central Monte Desert Birds open circles ants solid

circles mammals open triangles Mean rates of removalfor the 23ndash25 trays available only to the respective taxonare shown Within a season means with the same letter

are not significantly different according to Tukeyrsquos test ( Plt 005) Figure redrawn from Lopez de Casenave et al

(1998) and used with permission from Blackwell Science

measuring seed consumption by desert birds (Mares andRosenzweig 1978 Morton 1985)

In most bait experiments carried out in South Americandeserts however avian granivores quickly discovered baitsand consumed seeds Indeed birds often consumed moreseeds than did the other granivore taxa (Table 2) We knowof no idiosyncratic characteristic of South American birdsthat may explain this pattern Thus to control for anypropensity of the Monte avifauna to detect seed trays withunusual skills we used an approach that did not rely on arti-ficial baits to assess whether birds are important seedeatersin the central Monte Desert (Marone et al 1998b)

Bait experiments have shown that bird granivores arethe main autumnndashwinter seed consumers in the centralMonte Desert (Figure 4 see Lopez de Casenave et al1998) To assess the impact of seed-eating birds on theautumnndashwinter soil seed reserves we compared the soilseed bank in the late summer of 1995 (12 February) withthat present the following early spring (25 October) alsotaking into account the total number of seeds that enteredthe soil from late summer to early spring (ie we mea-sured seed rain Marone et al 1998b) In late summerbefore consumption by birds the mean seed density ofgrass seed banks was 2400 seedsm2 or 036 gm2 The nextspringmdashfollowing the input of approximately 3000 grassseedsm2 or 071 gm2 as well as the period of bird con-sumption in autumn and wintermdashthe density of grassseeds was 2700 seedsm2 or 039 gm2 Medium and largegrass seeds suffered higher postdispersal losses than didsmall seeds Likewise densities of forb seeds in the seedbank were statistically indistinguishable between late sum-mer (5500 seedsm2 or 134 gm2) and spring (6500seedsm2 or 153 gm2) although forb seed productionduring the study period had been relatively low (400seedsm2 or 012 gm 2) These results suggest thatautumnndashwinter seed predators in the central MonteDesert favor grass seeds over forb seeds

Several lines of evidence confirm that postdispersalgrass seed loss during autumnndashwinter in the centralMonte Desert is due mainly to vertebrate consumptionFirst granivorous ants are active almost exclusively during

the spring and summer (Figure 4 Lopez de Casenave et al1998) Furthermore C4 grasses germinate mostly in latespring and summer and total grass seed germinationwhich usually does not surpass 05 of previous soil seedreserves (Marone et al 1998b) reached only 5 of previ-ous reserves during the exceptionally wet summer of 1998which was associated with a strong El NintildeoSouthernOscillation event (Luis Marone Manuel E Horno RafaelGonzaacutelez del Solar unpublished data) Finally given thecomposition of the seed bank at different depths (0ndash2 cm2ndash4 cm and 4ndash6 cm) Marone et al (1998a) concludedthat grass seeds especially the medium and large seedswould suffer negligible loss by deep burial

Therefore it was not surprising that the pattern of seedlosses coincided with the pattern of seed consumption bygranivorous birds in the autumns and winters of 1993through 1995 Nearly 93 of the seed mass in bird stom-achs came from grass seeds and only 7 came from forbseeds Furthermore medium and large grass seeds sufferedthe highest losses from the soil seed bank and were also themain target of foraging by granivores Moreover a signifi-cant positive correlation existed across grass speciesbetween the mass decrease of seed species from the soiltoward spring and the mass of those seed species in birddiets in autumnndashwinter (Figure 5 Marone et al 1998b)This positive correlation suggests that bird consumptioncould explain a great deal of the autumnndashwinter grass seedloss observed in soils of the central Monte Desert

These lines of evidence indicate that vertebrate grani-vores (particularly birds) have a major impact on theabundance floristic composition and size distribution ofseed reserves in the Monte Desert where vertebrategranivory in general and avian granivory in particularhad previously been considered unimportant Moreovernewly produced seeds from perennial grasses constitute amajor fraction of autumnndashwinter bird diet This findingsupports the proposal (Marone 1992) that the timing andamount of rainfall in the central Monte Desert may great-ly influence the abundance and migrations of granivorousbirds via the opportunistic response of seed production bygrasses to variations in rainfall Population interactions

130 BioScience February 2000 Vol 50 No 2

Articles

Figure 5 Relationship between the mass of seeds fromperennial grasses in the autumn and winter diets (in1993ndash1995) of four granivorous bird species in the centralMonte Desert and the loss of seeds of each species during theautumn and winter of 1995 The bird species are Zonotrichiacapensis Phrygilus carbonarius Diuca diuca andSaltatricula multicolor The overall correlation wassignificant (r = 087 n = 11 P lt 0001) Grass species are asfollows Pap Pappophorum spp Set Setaria leucopila DigDigitaria californica Tri Trichloris crinita Dip Diplachnedubia Spo Sporobolus cryptandrus Ari Aristida spp NeoNeobouteloua lophostachya Chl Chloris castilloniana BouBouteloua spp The point for Stipa spp is not shown on thefigure but overlaps with that for Bouteloua spp

between seeds and avian granivores in this South Ameri-can desert may therefore be more important than hithertoappreciated

Concluding remarksThe relative importance of seed consumption or granivo-rous assemblages in deserts around the world cannot beassessed through one research approach alone (eg baitremoval experiments energetics approaches descriptionsof the species composition of granivorous assemblages orquantification of individualsrsquo diets) Instead research pro-grams that include multiple approaches involving redun-dancy and cross-checks of hypotheses and methods maylead to the most robust conclusions and therefore to syn-thesis and integration (Pickett et al 1994) Furthermoreany such program should involve long-term studies thattake into account the spatial and temporal variability ofnatural communities

Partly as a consequence of such a lack of integrationnatural rates of seed consumption and the abundance anddiversity of granivorous assemblages in some South Amer-ican deserts may have been underestimated in the pastThe evidence we have discussed in this article comes fromvarious desert locations of southern South America andwas obtained by using different research approaches Thisevidence suggests that birds and ants are importantseedeaters during the colder and warmer months respec-tively and that the role of small mammals as granivores inthe central Monte Desert of Argentina deserves moredetailed assessment These results should be readily incor-porated into comparative studies to distinguish betweenidiosyncratic and general processes molding desert com-munities worldwide Although ecological ldquolawsrdquo are by nomeans universal ecological understanding will continueto depend on theory development (Pickett et al 1994Mahner and Bunge 1997) To develop ecological theoryresearchers need good observations combined with rigor-ous and realistic experiments carried out in the context ofresearch programs that are focused whenever possible ontesting mechanisms to account for ecological phenomena(Werner 1998)

AcknowledgmentsWe acknowledge Sergio Camiacuten Silvia Claver RafaelGonzaacutelez del Solar Fernando Milesi Martha J PiantanidaBertilde Rossi Eduardo Tomaacutes-Mezquida and GualbertoZalazar for their constructive and pleasant cooperationduring field and laborator y work Manuel E Horno andIris Peralta contributed partnership and stimulating dis-cussion at the initial (and more chaotic) stages of ourstudies we are especially indebted to both of them SergioL Saba was kind enough to let us use his unpublisheddata First drafts of the manuscript were greatly improvedthrough critical review from Rebecca Chasan Chris Dick-man Pete Feinsinger Lali Guichoacuten Rafael Gonzaacutelez delSolar Fabiaacuten Jaksic Graham Kerley Fernando Milesi

Stephen Morton Mary V Price Julian Reid AlejandraRibichich Rodrigo Vaacutesquez and four anonymous review-ers At different stages field and laboratory work werefinanced by the Man and the Biosphere Programme Unit-ed Nations Educational Scientific and Cultural Organiza-tion the Association of Field Ornithologists Programa deCiencias Naturales Museo Argentino de Ciencias Natu-rales ldquoBernardino Rivadaviardquo IADIZA-Provincia de Men-doza and the Argentine funding agencies CONICET (PEI032797) and Agencia Nacional de Promocioacuten Cientiacutefica yTecnoloacutegica (PICT 01-03187) L M acknowledges CON-ICET and the Canadian Government for financial sup-port and Mario Bunge for the stimulating environment atMcGill University where the final version of this paperwas written This article is Contribution No 8 of theDesert Community Ecology Research Team Plant Eco-physiology Department IADIZA Institute

References citedAbramsky Z 1983 Experiments on seed predation by rodents and ants in

the Israeli desert Oecologia 57 328ndash332

Brown JH Ojeda RA 1987 Granivory Patterns processes and conse-

quences of seed consumption on two continents Revista Chilena de

Historia Natural 60 337ndash349

Campos CM 1997 Utilizacioacuten de recursos alimentarios por mamiacuteferos

medianos y pequentildeos del desierto del Monte PhD dissertation Uni-

versidad Nacional de Coacuterdoba Coacuterdoba Argentina

Capurro HA Bucher EH 1982 Poblaciones de aves graniacutevoras y disponi-

bilidad de semillas en el bosque chaquentildeo de Chamical Ecosur 9

117ndash131

Childs S Goodall DW 1973 Seed reserves of desert soils Logan (UT)

Utah State University USIBP Desert Biome Research Memorandum

73-5

Claver S Fowler HG 1993 The ant fauna (Hymenoptera Formicidae) of

the Ntildeacuntildeaacuten Biosphere Reserve Naturalia 18 189ndash193

Dellafiore CM Polop JJ 1994 Feeding habits of Calomys musculinus in the

crop fields and its borders Mastozoolog iacutea Neotropical (Argentina) 1

45ndash50

Dye AJ 1969 Germination potentials and accumulation of native plant

seeds from southern New Mexico Masterrsquos thesis New Mexico State

University Las Cruces NM

Holldobler B Wilson EO 1990 The Ants Cambridge (MA) Harvard Uni-

versity Press

Jaksic FM 1989 Opportunist selective and other often-confused terms in

the predation literature Revista Chilena de Historia Natural 62 7ndash8

Kelrick MI MacMahon JA Parmenter RR Sisson DV 1986 Native seed

preferences of shrubndashsteppe rodents birds and ants The relationships

of seed attributes and seed use Oecologia 68 327ndash337

Kelt DA Brown JH Heske EJ Marquet PA Morton SR Reid JRW Rogovin

KA Shenbrot G 1996 Community structure of desert small mam-

mals Comparisons across four continents Ecology 77 746ndash761

Kemp PR 1989 Seed bank and vegetation processes in deserts Pages

257ndash281 in Allessio-Leck M Parker VT Simpson RL eds Ecology of

Soil Seed Banks San Diego (CA) Academic Press

Kerley GIH 1991 Seed removal by rodents birds and ants in the semi-arid

Karoo South Africa Journal of Arid Environments 20 63ndash69

______ 1992 Small mammal seed consumption in the Karoo South

Africa Further evidence for divergence in desert biotic processes

Oecologia 89 471ndash475

Kerley GIH Whitford WG 1994 Desert-dwelling small mammals as grani-

vores Intercontinental variations Australian Journal of Zoology 42

543ndash555

Kerley GIH Whitford WG Kay FR 1997 Mechanisms for the keystone sta-

February 2000 Vol 50 No 2 BioScience 131

Articles

measuring seed consumption by desert birds (Mares andRosenzweig 1978 Morton 1985)

In most bait experiments carried out in South Americandeserts however avian granivores quickly discovered baitsand consumed seeds Indeed birds often consumed moreseeds than did the other granivore taxa (Table 2) We knowof no idiosyncratic characteristic of South American birdsthat may explain this pattern Thus to control for anypropensity of the Monte avifauna to detect seed trays withunusual skills we used an approach that did not rely on arti-ficial baits to assess whether birds are important seedeatersin the central Monte Desert (Marone et al 1998b)

Bait experiments have shown that bird granivores arethe main autumnndashwinter seed consumers in the centralMonte Desert (Figure 4 see Lopez de Casenave et al1998) To assess the impact of seed-eating birds on theautumnndashwinter soil seed reserves we compared the soilseed bank in the late summer of 1995 (12 February) withthat present the following early spring (25 October) alsotaking into account the total number of seeds that enteredthe soil from late summer to early spring (ie we mea-sured seed rain Marone et al 1998b) In late summerbefore consumption by birds the mean seed density ofgrass seed banks was 2400 seedsm2 or 036 gm2 The nextspringmdashfollowing the input of approximately 3000 grassseedsm2 or 071 gm2 as well as the period of bird con-sumption in autumn and wintermdashthe density of grassseeds was 2700 seedsm2 or 039 gm2 Medium and largegrass seeds suffered higher postdispersal losses than didsmall seeds Likewise densities of forb seeds in the seedbank were statistically indistinguishable between late sum-mer (5500 seedsm2 or 134 gm2) and spring (6500seedsm2 or 153 gm2) although forb seed productionduring the study period had been relatively low (400seedsm2 or 012 gm 2) These results suggest thatautumnndashwinter seed predators in the central MonteDesert favor grass seeds over forb seeds

Several lines of evidence confirm that postdispersalgrass seed loss during autumnndashwinter in the centralMonte Desert is due mainly to vertebrate consumptionFirst granivorous ants are active almost exclusively during

the spring and summer (Figure 4 Lopez de Casenave et al1998) Furthermore C4 grasses germinate mostly in latespring and summer and total grass seed germinationwhich usually does not surpass 05 of previous soil seedreserves (Marone et al 1998b) reached only 5 of previ-ous reserves during the exceptionally wet summer of 1998which was associated with a strong El NintildeoSouthernOscillation event (Luis Marone Manuel E Horno RafaelGonzaacutelez del Solar unpublished data) Finally given thecomposition of the seed bank at different depths (0ndash2 cm2ndash4 cm and 4ndash6 cm) Marone et al (1998a) concludedthat grass seeds especially the medium and large seedswould suffer negligible loss by deep burial

Therefore it was not surprising that the pattern of seedlosses coincided with the pattern of seed consumption bygranivorous birds in the autumns and winters of 1993through 1995 Nearly 93 of the seed mass in bird stom-achs came from grass seeds and only 7 came from forbseeds Furthermore medium and large grass seeds sufferedthe highest losses from the soil seed bank and were also themain target of foraging by granivores Moreover a signifi-cant positive correlation existed across grass speciesbetween the mass decrease of seed species from the soiltoward spring and the mass of those seed species in birddiets in autumnndashwinter (Figure 5 Marone et al 1998b)This positive correlation suggests that bird consumptioncould explain a great deal of the autumnndashwinter grass seedloss observed in soils of the central Monte Desert

These lines of evidence indicate that vertebrate grani-vores (particularly birds) have a major impact on theabundance floristic composition and size distribution ofseed reserves in the Monte Desert where vertebrategranivory in general and avian granivory in particularhad previously been considered unimportant Moreovernewly produced seeds from perennial grasses constitute amajor fraction of autumnndashwinter bird diet This findingsupports the proposal (Marone 1992) that the timing andamount of rainfall in the central Monte Desert may great-ly influence the abundance and migrations of granivorousbirds via the opportunistic response of seed production bygrasses to variations in rainfall Population interactions

130 BioScience February 2000 Vol 50 No 2

Articles

Figure 5 Relationship between the mass of seeds fromperennial grasses in the autumn and winter diets (in1993ndash1995) of four granivorous bird species in the centralMonte Desert and the loss of seeds of each species during theautumn and winter of 1995 The bird species are Zonotrichiacapensis Phrygilus carbonarius Diuca diuca andSaltatricula multicolor The overall correlation wassignificant (r = 087 n = 11 P lt 0001) Grass species are asfollows Pap Pappophorum spp Set Setaria leucopila DigDigitaria californica Tri Trichloris crinita Dip Diplachnedubia Spo Sporobolus cryptandrus Ari Aristida spp NeoNeobouteloua lophostachya Chl Chloris castilloniana BouBouteloua spp The point for Stipa spp is not shown on thefigure but overlaps with that for Bouteloua spp

between seeds and avian granivores in this South Ameri-can desert may therefore be more important than hithertoappreciated

Concluding remarksThe relative importance of seed consumption or granivo-rous assemblages in deserts around the world cannot beassessed through one research approach alone (eg baitremoval experiments energetics approaches descriptionsof the species composition of granivorous assemblages orquantification of individualsrsquo diets) Instead research pro-grams that include multiple approaches involving redun-dancy and cross-checks of hypotheses and methods maylead to the most robust conclusions and therefore to syn-thesis and integration (Pickett et al 1994) Furthermoreany such program should involve long-term studies thattake into account the spatial and temporal variability ofnatural communities

Partly as a consequence of such a lack of integrationnatural rates of seed consumption and the abundance anddiversity of granivorous assemblages in some South Amer-ican deserts may have been underestimated in the pastThe evidence we have discussed in this article comes fromvarious desert locations of southern South America andwas obtained by using different research approaches Thisevidence suggests that birds and ants are importantseedeaters during the colder and warmer months respec-tively and that the role of small mammals as granivores inthe central Monte Desert of Argentina deserves moredetailed assessment These results should be readily incor-porated into comparative studies to distinguish betweenidiosyncratic and general processes molding desert com-munities worldwide Although ecological ldquolawsrdquo are by nomeans universal ecological understanding will continueto depend on theory development (Pickett et al 1994Mahner and Bunge 1997) To develop ecological theoryresearchers need good observations combined with rigor-ous and realistic experiments carried out in the context ofresearch programs that are focused whenever possible ontesting mechanisms to account for ecological phenomena(Werner 1998)

AcknowledgmentsWe acknowledge Sergio Camiacuten Silvia Claver RafaelGonzaacutelez del Solar Fernando Milesi Martha J PiantanidaBertilde Rossi Eduardo Tomaacutes-Mezquida and GualbertoZalazar for their constructive and pleasant cooperationduring field and laborator y work Manuel E Horno andIris Peralta contributed partnership and stimulating dis-cussion at the initial (and more chaotic) stages of ourstudies we are especially indebted to both of them SergioL Saba was kind enough to let us use his unpublisheddata First drafts of the manuscript were greatly improvedthrough critical review from Rebecca Chasan Chris Dick-man Pete Feinsinger Lali Guichoacuten Rafael Gonzaacutelez delSolar Fabiaacuten Jaksic Graham Kerley Fernando Milesi

Stephen Morton Mary V Price Julian Reid AlejandraRibichich Rodrigo Vaacutesquez and four anonymous review-ers At different stages field and laboratory work werefinanced by the Man and the Biosphere Programme Unit-ed Nations Educational Scientific and Cultural Organiza-tion the Association of Field Ornithologists Programa deCiencias Naturales Museo Argentino de Ciencias Natu-rales ldquoBernardino Rivadaviardquo IADIZA-Provincia de Men-doza and the Argentine funding agencies CONICET (PEI032797) and Agencia Nacional de Promocioacuten Cientiacutefica yTecnoloacutegica (PICT 01-03187) L M acknowledges CON-ICET and the Canadian Government for financial sup-port and Mario Bunge for the stimulating environment atMcGill University where the final version of this paperwas written This article is Contribution No 8 of theDesert Community Ecology Research Team Plant Eco-physiology Department IADIZA Institute

References citedAbramsky Z 1983 Experiments on seed predation by rodents and ants in

the Israeli desert Oecologia 57 328ndash332

Brown JH Ojeda RA 1987 Granivory Patterns processes and conse-

quences of seed consumption on two continents Revista Chilena de

Historia Natural 60 337ndash349

Campos CM 1997 Utilizacioacuten de recursos alimentarios por mamiacuteferos

medianos y pequentildeos del desierto del Monte PhD dissertation Uni-

versidad Nacional de Coacuterdoba Coacuterdoba Argentina

Capurro HA Bucher EH 1982 Poblaciones de aves graniacutevoras y disponi-

bilidad de semillas en el bosque chaquentildeo de Chamical Ecosur 9

117ndash131

Childs S Goodall DW 1973 Seed reserves of desert soils Logan (UT)

Utah State University USIBP Desert Biome Research Memorandum

73-5

Claver S Fowler HG 1993 The ant fauna (Hymenoptera Formicidae) of

the Ntildeacuntildeaacuten Biosphere Reserve Naturalia 18 189ndash193

Dellafiore CM Polop JJ 1994 Feeding habits of Calomys musculinus in the

crop fields and its borders Mastozoolog iacutea Neotropical (Argentina) 1

45ndash50

Dye AJ 1969 Germination potentials and accumulation of native plant

seeds from southern New Mexico Masterrsquos thesis New Mexico State

University Las Cruces NM

Holldobler B Wilson EO 1990 The Ants Cambridge (MA) Harvard Uni-

versity Press

Jaksic FM 1989 Opportunist selective and other often-confused terms in

the predation literature Revista Chilena de Historia Natural 62 7ndash8

Kelrick MI MacMahon JA Parmenter RR Sisson DV 1986 Native seed

preferences of shrubndashsteppe rodents birds and ants The relationships

of seed attributes and seed use Oecologia 68 327ndash337

Kelt DA Brown JH Heske EJ Marquet PA Morton SR Reid JRW Rogovin

KA Shenbrot G 1996 Community structure of desert small mam-

mals Comparisons across four continents Ecology 77 746ndash761

Kemp PR 1989 Seed bank and vegetation processes in deserts Pages

257ndash281 in Allessio-Leck M Parker VT Simpson RL eds Ecology of

Soil Seed Banks San Diego (CA) Academic Press

Kerley GIH 1991 Seed removal by rodents birds and ants in the semi-arid

Karoo South Africa Journal of Arid Environments 20 63ndash69

______ 1992 Small mammal seed consumption in the Karoo South

Africa Further evidence for divergence in desert biotic processes

Oecologia 89 471ndash475

Kerley GIH Whitford WG 1994 Desert-dwelling small mammals as grani-

vores Intercontinental variations Australian Journal of Zoology 42

543ndash555

Kerley GIH Whitford WG Kay FR 1997 Mechanisms for the keystone sta-

February 2000 Vol 50 No 2 BioScience 131

Articles

between seeds and avian granivores in this South Ameri-can desert may therefore be more important than hithertoappreciated

Concluding remarksThe relative importance of seed consumption or granivo-rous assemblages in deserts around the world cannot beassessed through one research approach alone (eg baitremoval experiments energetics approaches descriptionsof the species composition of granivorous assemblages orquantification of individualsrsquo diets) Instead research pro-grams that include multiple approaches involving redun-dancy and cross-checks of hypotheses and methods maylead to the most robust conclusions and therefore to syn-thesis and integration (Pickett et al 1994) Furthermoreany such program should involve long-term studies thattake into account the spatial and temporal variability ofnatural communities

Partly as a consequence of such a lack of integrationnatural rates of seed consumption and the abundance anddiversity of granivorous assemblages in some South Amer-ican deserts may have been underestimated in the pastThe evidence we have discussed in this article comes fromvarious desert locations of southern South America andwas obtained by using different research approaches Thisevidence suggests that birds and ants are importantseedeaters during the colder and warmer months respec-tively and that the role of small mammals as granivores inthe central Monte Desert of Argentina deserves moredetailed assessment These results should be readily incor-porated into comparative studies to distinguish betweenidiosyncratic and general processes molding desert com-munities worldwide Although ecological ldquolawsrdquo are by nomeans universal ecological understanding will continueto depend on theory development (Pickett et al 1994Mahner and Bunge 1997) To develop ecological theoryresearchers need good observations combined with rigor-ous and realistic experiments carried out in the context ofresearch programs that are focused whenever possible ontesting mechanisms to account for ecological phenomena(Werner 1998)

AcknowledgmentsWe acknowledge Sergio Camiacuten Silvia Claver RafaelGonzaacutelez del Solar Fernando Milesi Martha J PiantanidaBertilde Rossi Eduardo Tomaacutes-Mezquida and GualbertoZalazar for their constructive and pleasant cooperationduring field and laborator y work Manuel E Horno andIris Peralta contributed partnership and stimulating dis-cussion at the initial (and more chaotic) stages of ourstudies we are especially indebted to both of them SergioL Saba was kind enough to let us use his unpublisheddata First drafts of the manuscript were greatly improvedthrough critical review from Rebecca Chasan Chris Dick-man Pete Feinsinger Lali Guichoacuten Rafael Gonzaacutelez delSolar Fabiaacuten Jaksic Graham Kerley Fernando Milesi

Stephen Morton Mary V Price Julian Reid AlejandraRibichich Rodrigo Vaacutesquez and four anonymous review-ers At different stages field and laboratory work werefinanced by the Man and the Biosphere Programme Unit-ed Nations Educational Scientific and Cultural Organiza-tion the Association of Field Ornithologists Programa deCiencias Naturales Museo Argentino de Ciencias Natu-rales ldquoBernardino Rivadaviardquo IADIZA-Provincia de Men-doza and the Argentine funding agencies CONICET (PEI032797) and Agencia Nacional de Promocioacuten Cientiacutefica yTecnoloacutegica (PICT 01-03187) L M acknowledges CON-ICET and the Canadian Government for financial sup-port and Mario Bunge for the stimulating environment atMcGill University where the final version of this paperwas written This article is Contribution No 8 of theDesert Community Ecology Research Team Plant Eco-physiology Department IADIZA Institute

References citedAbramsky Z 1983 Experiments on seed predation by rodents and ants in

the Israeli desert Oecologia 57 328ndash332

Brown JH Ojeda RA 1987 Granivory Patterns processes and conse-

quences of seed consumption on two continents Revista Chilena de

Historia Natural 60 337ndash349

Campos CM 1997 Utilizacioacuten de recursos alimentarios por mamiacuteferos

medianos y pequentildeos del desierto del Monte PhD dissertation Uni-

versidad Nacional de Coacuterdoba Coacuterdoba Argentina

Capurro HA Bucher EH 1982 Poblaciones de aves graniacutevoras y disponi-

bilidad de semillas en el bosque chaquentildeo de Chamical Ecosur 9

117ndash131

Childs S Goodall DW 1973 Seed reserves of desert soils Logan (UT)

Utah State University USIBP Desert Biome Research Memorandum

73-5

Claver S Fowler HG 1993 The ant fauna (Hymenoptera Formicidae) of

the Ntildeacuntildeaacuten Biosphere Reserve Naturalia 18 189ndash193

Dellafiore CM Polop JJ 1994 Feeding habits of Calomys musculinus in the

crop fields and its borders Mastozoolog iacutea Neotropical (Argentina) 1

45ndash50

Dye AJ 1969 Germination potentials and accumulation of native plant

seeds from southern New Mexico Masterrsquos thesis New Mexico State

University Las Cruces NM

Holldobler B Wilson EO 1990 The Ants Cambridge (MA) Harvard Uni-

versity Press

Jaksic FM 1989 Opportunist selective and other often-confused terms in

the predation literature Revista Chilena de Historia Natural 62 7ndash8

Kelrick MI MacMahon JA Parmenter RR Sisson DV 1986 Native seed

preferences of shrubndashsteppe rodents birds and ants The relationships

of seed attributes and seed use Oecologia 68 327ndash337

Kelt DA Brown JH Heske EJ Marquet PA Morton SR Reid JRW Rogovin

KA Shenbrot G 1996 Community structure of desert small mam-

mals Comparisons across four continents Ecology 77 746ndash761

Kemp PR 1989 Seed bank and vegetation processes in deserts Pages

257ndash281 in Allessio-Leck M Parker VT Simpson RL eds Ecology of

Soil Seed Banks San Diego (CA) Academic Press

Kerley GIH 1991 Seed removal by rodents birds and ants in the semi-arid

Karoo South Africa Journal of Arid Environments 20 63ndash69

______ 1992 Small mammal seed consumption in the Karoo South

Africa Further evidence for divergence in desert biotic processes

Oecologia 89 471ndash475

Kerley GIH Whitford WG 1994 Desert-dwelling small mammals as grani-

vores Intercontinental variations Australian Journal of Zoology 42

543ndash555

Kerley GIH Whitford WG Kay FR 1997 Mechanisms for the keystone sta-

February 2000 Vol 50 No 2 BioScience 131

Articles

132 BioScience February 2000 Vol 50 No 2

Articles

tus of kangaroo rats Graminivory rather than granivory Oecologia

111 422ndash428

Lakatos I 1978 Falsification and the methodology of scientific research

programmes Pages 8ndash101 in Worrall J Currie G eds The Methodolo -

gy of Scientific Research Programmes Cambridge (UK) Cambridge

University Press

Lawton JH 1999 Are there general laws in ecology Oikos 84 177ndash192

Loacutepez-Calleja MV 1995 Dieta de Zonotrichia capensis y Diuca diuca Efec-

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Lopez de Casenave J Cueto VR Marone L 1998 Granivory in the Monte

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Mares MA 1993a Desert rodents seed consumption and convergence

BioScience 43 372ndash379

______ 1993b Heteromyids and their ecological counterparts A pan-

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Genoways HH Brown JH eds Biology of the Heteromyidae Ship-

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Mares MA Rosenzweig ML 1978 Granivory in North and South Ameri-

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Mares MA Blair WF Enders FA Greegor D Hulse AC Hunt JH Otte D

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Marone L 1992 Seasonal and year-to-year fluctuations of bird populations

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Marone L Horno ME 1997 Seed reserves in the central Monte Desert

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36 661ndash670

Marone L Rossi BE Horno ME 1998a Timing and spatial patterning of

seed dispersal and redistribution in a South American warm desert

Plant Ecology 137 143ndash150

Marone L Rossi BE Lopez de Casenave J 1998b Granivore impact on soil

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Medel RG 1995 Convergence and historical effects in harvester ant assem-

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Medel RG Vaacutesquez RA 1994 Comparative analysis of harvester ant

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Meserve PL 1981a Trophic relationships among small mammals in a

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304ndash314

______ 1981b Resource partitioning in a Chilean semi-arid small mam-

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Morton SR 1985 Granivory in arid regions Comparison of Australia with

North and South America Ecology 66 1859ndash1866

______ 1993 Determinants of diversity in animal communities of arid

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Morton SR Davidson DW 1988 Comparative structure of harvester ant

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Nowak RM Paradiso JL 1983 Walkerrsquos Mammals of the World 4th ed

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Pulliam HR Parker TA 1979 Population regulation of sparrows

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Schluter D Ricklefs RE 1993 Species diversity An introduction to the

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Vaacutesquez RA 1996 Patch utilization by three species of Chilean rodents dif-

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