photosynthetic pathways, spatial distribution, isotopic ecology, and implications for pre-hispanic...

International Journal of OsteoarchaeologyInt. J. Osteoarchaeol. 19: 130–143 (2009)Published online in Wiley InterScience

051
(www.interscience.wiley.com) DOI: 10.1002/oa.1
* Correspondence to: MuseoParque Mariano Moreno s/ntina 5600.e-mail: carinallano@arqueolo

Copyright # 2009 Joh

Photosynthetic Pathways, SpatialDistribution, Isotopic Ecology, andImplications for Pre-Hispanic HumanDiets in Central-Western Argentina

C. LLANO*

Departamento de Antropologıa, Museo de Historia Natural de San Rafael, Parque Mariano

Moreno (5600) San Rafael, Mendoza, Argentina

ABSTRACT In a number of areas around the world researchers have begun to use the isotopic values ofsubsistence resources as a means of determining diets of human populations. The objectiveof the present study is to classify the plant species present at distinct altitudes in southernMendoza Province, Argentina, considering photosynthetic pathways in order to determinetheir d13C isotopic signature. This will help to understand the relationships between diets andthe isotopic values observed in archaeological human remains. Data compiled from varioussources are used to establish the photosynthetic pathways andmean d13C values. The resultsindicate that C3 species are dominant at high-altitude settings, and that the few identified C4

species were found primarily at lower altitudes. These results are intended to serve as afoundation for future isotopic studies designed to address relationships among species atdifferent trophic levels. Copyright � 2009 John Wiley & Sons, Ltd.

Key words: C3 and C4 plants; stable isotopes; human diets; photosynthetic distribution; Argentina

Introduction

Recently, researchers from different disciplineshave begun to use the isotopic values ofsubsistence resources as a means of determiningthe composition of human diets in the past. Theresults of these analyses indicate cultural patterns,such as the presence of agriculture, dependenceupon marine versus terrestrial resources, manage-ment of domesticated animals, transport, andexchange of materials with neighbouring regions(Ambrose, 1993; Tieszen & Fagre, 1993; Gil,1997–98, 2003; Novellino & Guichon, 1997–98;Coltrain & Leavitt, 2002; Novellino et al., 2004;Gil et al., 2006). Proportions of the stable isotopes

de Historia Natural de San Rafael,Isla Rio Diamante, San Rafael, Argen-

giamendoza.com

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13C/12C and 15N/14N provide information aboutthe origins of consumed resources, metabolicprocesses of consumers, migration of animals, anddifferences between trophic levels and biogeo-chemistry cycles, among other things (Dawsonet al., 2002). Variations in the range of isotopicvalues of biological materials can be used torecognise elements that move through biogeo-chemistry cycles, as with plants in the diets ofhumans and their prey animals (Louis et al., 2005).

In southern Mendoza, stable isotope studieshave been performed on samples of human tissueto determine the composition of the diets of thehuman populations inhabiting the region duringthe middle and late Holocene (Novellino &Guichon, 1997–98; Gil, 2003; Novellino et al.,2004; Gil et al., 2006). This region is consideredthe southern limit of pre-Hispanic agriculturalexpansion (Gil, 1997–1998) and it was associatedwith a range of different subsistence strategies at

Received 3 October 2008Accepted 28 October 2008

Isotopic Ecology and Subsistence 131

the boundary between agriculture to the northand hunting and gathering to the south (Gil,1997–1998; Lagiglia, 2001, 2002; Novellino et al.,2004). One of the main difficulties that research-ers in southern Mendoza have encountered is theexistence of large variations in the isotopicecology across the landscape. Assessing isotopicvalues on prehistoric human remains permitsdiscussion of the resources that these groupsincorporated into their diets on a systematicbasis. These isotopic values may reflect theconsumption of plants with distinct photosyn-thetic pathways and/or the animal consumers ofplants with these pathways (Ambrose, 1993;Barberena, 2004). The results of the analysescarried out in southern Mendoza show that thereare differences in isotopic values between thehighland piedmont region and the lowlands,apparent at all trophic levels. Among the samplesdrawn from human remains, the d13C values aremore enriched in lowland samples than inhighland piedmont samples (Gil et al., 2006).This has been interpreted as a diet composedprimarily of C3 resources in the highlandpiedmont, while in the lowland the moreenriched d13C values are likely to be the resultof a greater incorporation of C4 plants into theirdiet. The aim of this study is to outline theisotopic ecology of southern Mendoza in order tointerpret isotopic ratios observed among pre-historic human remains. Toward this end, Iexplore the altitudinal and topographic frequen-cies of taxa with different photosynthetic path-ways. The distributions of C3, C4 and CAM speciesare then compared with the diets of choique(Pterocnemia pennata) and guanaco (Lama guanicoe) –the most frequently occurring animal taxa in theregion’s archaeological record – and with theisotopic values derived from human remains.

The effects of environmental variableson the distribution of plants withdifferent photosynthetic pathways

Carbon enters the biosphere in the form ofatmospheric carbon dioxide, which is taken up byplants during photosynthesis. The organic matterproduced during photosynthesis has a d13C value

Copyright # 2009 John Wiley & Sons, Ltd.

indicative of the photosynthetic pathway of theplant (Farquhar et al., 1989). Differences ind13C values among plants make it possible todistinguish their photosynthetic pathways bymeasuring carbon isotope ratios. Plants with a C3

photosynthetic pathway have d13C valuesbetween �20 and �35%, plants with a C4

pathway have d13C values between �9 and�17%, and plants with Crassulacean AcidMetabolism (CAM) have d13C values between�10 and �22%, overlapping the ranges ofboth C3 and C4 plants (Bender, 1971; Smith &Epstein, 1971). The d13C values among CAMplants are determined by the environmentalstressors they experience (Farquhar et al., 1989).Species with C3 and C4 photosynthetic pathwaysare easily distinguished because their d13C rangesdo not overlap (Cerling et al., 1999).

It is of special ecological interest that thesegroups possess different physiological, bio-chemical and structural features that result indifferent rates of photosynthesis and differentrelationships with their environments (Tieszen,1970; Williams & Markley, 1973; Williams, 1974;Fischer et al., 2007), especially temperature andmoisture (Teeri & Stowe, 1976). Many C4 plantshave higher temperature optima (30–458C) fornet CO2 exchange than C3 plants (10–258C). C4

plants require higher irradiance for photosyn-thetic saturation, and their maximum rates ofnet CO2 uptake are often substantially greaterthan those of C3 plants (Tieszen et al., 1979).

There are several examples of C3, C4 and CAMplants partitioning along altitudinal gradients inparticular geographical regions (Tieszen, 1970;Tieszen et al., 1979, 1997; Cavagnaro, 1988;Paruelo & Laurenroth, 1996; Ehleringer et al.,1997). These distributions are affected byenvironmental factors such as temperature, lightintensity and water availability (Teeri & Stowe,1976; Tiezsen et al., 1979; Rundel, 1980).

Cavagnaro (1988) examined the distribution ofphotosynthetic pathways in North MendozaProvince, considering the effect of altitude onthe atmospheric discrimination of CO2 (Figure 1).He found that pathways are strongly correlatedwith evapotranspiration and temperature, butonly weakly with precipitation. The relationshipobserved between the distribution of plants withdifferent photosynthetic pathways and climatic

Int. J. Osteoarchaeol. 19: 130–143 (2009)DOI: 10.1002/oa

Figure 1. Location of the study area inMendoza Province,Argentina.

132 C. Llano

parameters implies that the C4 species aredominant at lower elevations, while the C3

species are dominant at higher elevations.Between 1100 and 1600 metres above sea-level(m.a.s.l.), the relative abundance of the two typesis fairly even (Cavagnaro, 1988). Similar results ofphotosynthetic pathways were found in Kenya,where C4 grasses dominate in the warmer, aridlowland areas and C3 grasses dominate at cooler,higher altitudes where more moisture is available(Tieszen et al., 1979). Regarding C3/C4 plantdistributions relative to temperature, Ehleringeret al. (1997) confirmed Cavagnaro’s (1988) findingof a strong relationship between temperature andaltitude, showing that C4 species dominate athigher temperatures. The temperature range fortransition of the dominance/abundance of onemetabolic type to the other is 208–288C in the


northern hemisphere (Ehleringer et al., 1997),and 238–288C in the southern hemisphere(Cavagnaro, 1988).

Paruelo and Laurenroth (1996) accepted thattemperature is the principal determinant of thedistribution of C3 and C4 species, but theirinvestigations showed that precipitation and itsseasonal distribution also influences the relativeabundance of plants with different photosyn-thetic pathways (Paruelo & Laurenroth, 1996).The objective of their study was to analyse thegeographical distribution of photosynthetic path-ways in temperate grasslands and shrublands ofcentral North America. The climatic variablesthey considered were mean annual temperature,mean annual precipitation, thermal amplitude,and the proportion of precipitation that fallsbetween December and February and betweenJune and August. Their results showed that theregional distribution of C4 species increases withtemperature, precipitation and thermal ampli-tude. The abundance of C3 species decreases withmean annual temperature, and increases with theamount of precipitation falling in winter (Paruelo& Laurenroth, 1996). Indeed, on a global scale,the grasslands of the North American GreatPlains are a special case because they aredominated by C3/C4 mixtures. To clarify theeffects of regional climate on the percentagesof C3 and C4 plants in the Great Plains, a studycarried out by Tieszen and colleagues showedthat the region is characterised by wide variationsin C3 and C4 composition, with high proportionsof C4 species in the south and low proportions inthe north (Tieszen et al., 1997).

Another study of the distribution of plants withdifferent photosynthetic pathways was outlinedby Ehleringer and colleagues, who assessed theecological, geographical and palaeoecologicalfactors that affect the distribution of plants witha C4 pathway (Ehleringer et al., 1997). Thevariables they used to evaluate the metabolicdistribution were temperature, efficiency in theuse of light intensity, and atmospheric CO2. Tounderstand the distribution of the C3/C4 plantsfrom an ecological perspective, it is useful notonly to evaluate the impact on primary pro-ductivity, but also the distribution, evolution andmigration of invertebrates and vertebrates thatconsume these plants (Ehleringer et al., 1997).



Tieszen et al. (1979) measured the dietarypreferences of vertebrates that inhabit easternAfrica, showing via carbon isotopes that animalsdiffer in their preference for C3 or C4 plants.Central to understanding these preferences aredifferences in the nutritional quality of C3 and C4

plants. In C4 plants, for example, much of theprotein contained in leaves is enclosed in thethicker cell walls of the bundle sheath cells (BSC),which leads to lower digestibility of some specieswith this photosynthetic pathway (Wilson &Hattersley, 1983). However, in the majority ofcases, plant selection on the part of consumers isdue to the relative availability of plants withdifferent photosynthetic pathways.

Isotopic ecology and thearchaeological record

Analyses of carbon and nitrogen isotopes inanimal remains are commonly used to aidreconstruction of the diets of prehistoric humanpopulations (Novellino & Guichon, 1997-98;Coltrain & Leavitt, 2002; Gil, 2003; Novellinoet al., 2004; Codron et al., 2005; Gil et al., 2006).The proportion of stable isotopes in faunalmaterial is dependent on the isotopic compo-sition of the plants that form the base of the foodchain. Accordingly, our capacity to reconstructthe diet is limited by our knowledge of theabundance and distribution of C3 and C4 photo-synthetic pathway plants and of the faunaassociated with them. Isotopic values in bonecollagen have also been used to assess theintroduction of maize (Zea mays) agriculture, orto determine the quantity of C4-derived carbon(i.e. maize) that has entered the diet (Coltrain &Leavitt, 2002; Gil, 2003; Gil et al., 2006; Gil et al.,2009; Calo & Cortes, 2009).

Archaeological investigations in southernMendoza have focused primarily on topicsrelated to subsistence among prehistoric humanpopulations and the introduction of maize.Isotopic trends observed in Mendoza indicatedifferences between the lowland and the high-land piedmont regions, although C4 resources didnot constitute a significant portion of the humandiet in either area. In the lowlands, the human


diet appears to have been highly variable, withisotopic signatures ranging from �17% to�13.9%, while in the highlands the diet wasessentially composed of C3 resources, reflected ind13C values between �18.8% to �25.4% (Gilet al., 2006). These variations in the results ofd13C analyses suggest the need to better under-stand the isotopic ecology of the region, whichwill allow us to define more precisely the variablesthat may influence the results obtained.

Materials and methods

Mendoza Province lies between 328 and 378S,and 668 and 708250W (Capitanelli, 2005;Figure 1), and is characterised by environmentalheterogeneity mainly conditioned by longitudi-nal topographic changes: the Andes Cordillera inthe western portion of the province, plains anddepressions in the central and eastern portions,and the volcanic relief of La Payunia toward thesoutheast, each associated with different types ofsediments (Abraham, 2000). The region is arid tosemi-arid, with an average annual precipitation of250 mm (Capitanelli, 2005), although there isconsiderable variation in annual precipitationbetween the cordillera and the plains. In thecordillera, precipitation falls chiefly as wintersnows while summers are dry, with annual valuesranging from 300 to 1000 mm. On the easternplains, on the other hand, annual precipitation isbelow 250 mm (Abraham, 2000). The combi-nation of geomorphology and distance to theoceans has established different ecologicalcharacteristics in these environments, which arereflected in the distribution of vegetation.

Regarding phytogeography, the vegetationbetween 358 and 378S is composed of shrub-likesteppes, dominated by Patagonian and Monteelements that extend to the eastern plain andvolcanic mesas (Paez et al., 2004). The Andesand La Payunia areas are both subject to theinfluence of the Pacific anticyclonic weatherpatterns, and correspond to the Alto-andina andPatagonica phytogeographical provinces, respec-tively. The central and eastern plains are con-ditioned by the Atlantic anticyclonic patterns and,from a phytogeographical perspective, correspondto the Monte province (Abraham, 2000).


134 C. Llano

The study area

One transect was analysed with the goal ofdetecting altitudinal variations in the distributionof plants with different photosynthetic pathways(Navarro, 2004; Figure 1). This transect is locatedbetween 348420 and 358040S, 688340 and 698520W, and from <1100 to 2000 m.a.s.l. in theAndes (Navarro, 2004) along the Atuel riverbasin, which is one of the main water courses insouthern Mendoza.

At 358S there is a west to east progression ofthe vegetal communities classifiable at the scale ofprovinces: Patagonia, Patagonia-Monte andMonte, the Patagonia-Monte transition occurringat 1500 m.a.s.l. (Navarro, 2004; Figure 1). Themore northerly transect shows that, from west toeast, the units of vegetation co-vary with theenvironmental zones, illustating the co-domi-nance of Monte and Patagonia elements. Towardthe east there are semi-arid steppes of the LaPayunia District, whose volcanic substrate pro-duces attributes that can be characterised as adistinct phytogeographical province within theDominio Andino-Patagonico (Quintana, 2000;Martınez Carretero, 2006).

In the transect survey, the sampling strategyconsisted of a systematic collection at each 100m.a.s.l., and elaboration of a floristic list. Lists ofspecies presence/absence along each transectwere used as a base to establish differences in thedistributions of C3 and C4 photosynthetic path-ways. Classification into C3 and C4 groups wasbased on data compiled by various authors(Bender, 1971; Smith & Epstein, 1971; Downton,1975; Raghavendra & Das, 1978; Boutton et al.,1980; Hnatiuk, 1980; Cavagnaro, 1988; Ehler-inger et al., 1997; Gil et al., 2006) that areappropriate for determining the distribution ofspecies with different photosynthetic pathways.Plants whose pathways are not known wereexcluded from the sample. The list of plantspecies was compared with the diet of thechoique flightless bird – Pterocnemia pennata –(Paoletti & Puig, 2007), guanaco – Lama guanicoe –(Candia & Dalmasso, 1995; Puig et al., 1996) andisotopic values derived from prehistoric humanremains (Gil et al., 2006, 2009) from the lowlandsand the highland piedmont regions. Thiscomparison indicates the consistency between


the isotopic values of human samples and thephotosynthetic pathway in plants.

Results

An analysis of the flora of southern MendozaProvince (Roig, 1960, 1972; Bocher et al., 1963,1968, 1972; Ruiz Leal, 1972) indicates that theregion is home to well over 500 species of variousfamilies. Although exhaustive lists of flora havenot been compiled for most areas in Mendoza,there is some information to verify the trendsobserved in photosynthetic pathway distributions(Table 1). In the study area, 52.3% of speciesfollow a C3 photosynthetic pathway, while46.1% follow a C4 photosynthetic pathway.

The families representing C3 plants areAnacardiaceae, Euphorbiceae, Fabaceae, Junca-ceae, Plantaginaceae, Rhamnaceae, Solanaceaeand Typhaceae; the families representingC4 plants are Boraginaceae, Bromeliaceae andPortulacaceae. The families Asteraceae, Cheno-podiaceae and Poaceae possess both C3 andC4 species.

Survey transect data compiled by Navarro(2004) are used to establish the altitudinaldistribution of these pathway types (Figure 1).The floristic list of presence/absence of plantspecies is summarised in Table 2 and Figure 3.The results of the analysis show that C3 speciespredominate at higher elevations, with a strongcorrelation between altitude and photosyntheticpathways (r¼ 0.64). None the less, this photo-synthetic pathway is present at all altitudes. C4

species are primarily restricted to low altitudesand show lower correlation than C3 plants(r¼�0.36). Figure 2 illustrates the data derivedfrom this transect, indicating which plantsfix CO2 by C3 or C4 photosynthesis. At 1300m.a.s.l. the relative abundance of both photo-synthetic pathways is similar.

Paoletti & Puig (2007) described the diet ofPterocnemia pennata in a high arid pampa (3000m.a.s.l.) of the Andean Precordillera at ParamillosUspallata (328290S, 698080W), Mendoza, Argen-tina. Fieldwork was conducted in three seasons –late spring, late summer and late autumn – and thedietary assessment was based on faecal sampling(Table 3; Paoletti & Puig, 2007). The analysis of


Table 1. Plant species from southern Mendoza Province, examined for C3 and C4 photosynthetic pathways

Family Species Photosyntheticpathway

d13C% References

Amaranthaceae Amaranthus caudatus C4 �15.4 Ehleringer et al. (1997)Smith & Epstein (1971)

Gompherena mendocina (Phil.) R.E. Fr. C4 Ehleringer et al. (1997)Anacardiaceae Schinus fasciculata (Griseb.) I.M. Johnst. C3 Basinger (2002)

Schinus polygamus (Cav.) Cabrera C3 �24.4 Gil et al. (2006)Aizoaceae Mesembryanthemum chilense Mol. C3 �23.6 Smith & Epstein (1971)Asteraceae Artemisia mendozana Dc. C3 �28.8 Bender (1971)

Flaveria bidentis (L.) B.L. Rob.,comb. superfl.

C4 Raghavendra &Das (1978)

Tagetes argentina Cabrera C3 �28.9 Bender (1971)Tagetes mendocina Phil. C3 Bender (1971)Tagetes minuta L. C3 Bender (1971)

Boraginaceae Heliotropium mendocinum Phil. C4 Ehleringer et al. (1997)Bromeliaceae Tillandsia bryoides Griseb. ex Baker C4 Smith & Epstein (1971)Cactaceae Maihuenia patagonica CAMCyperaceae Cyperus rotundus L. C4 �15.9 Downton (1975) Smith &

Epstein (1971)Carex sp. C4 �11.5 Smith & Epstein (1971)

Chenopodiaceae Atriplex lampa(Moq.) D. Dietr. C4 Ehleringer et al. (1997)Atriplex patagonica(Moq.) D. Dietr. C4 Ehleringer et al. (1997)Chenopodium albumL. C3 �28.1 Bender (1971)Chenopodium sp. C3 �27.6 Gil et al. (2006)Bassia scoparia (L.) A.J. Scott C4 Ehleringer et al. (1997)Kochia scoparia (L.) Schrader C4 �14.0 Smith & Epstein (1971)Suaeda argentinensis A. Soriano C4 Fisher et al. (1997)Suaeda divaricata Moq. C4 Fisher et al. (1997)Suaeda patagonica Speg. C3 Fisher et al. (1997)

Euphorbiaceae Euphorbia serpens Kunth C4 Downton (1975)Fabaceae Astragalus pehuenches C3 Hnatiuk (1980)

Geoffroea decorticans C3 �20.2 Gil et al. (2006)Prosopis sp. C3 �23.9 Gil et al. (2006)Senna arnottiana C3 �25.4 Gil et al. (2006)

Frankeniaceae Frankenia juniperoides (Hieron.)M.N. Correa

C3 Smith & Epstein (1971)

Juncaceae Juncus balticus Willd C3 Hnatiuk (1980)Plantaginaceae Plantago patagonica C3 Hnatiuk (1980)Poaceae Aristida mendocina Phil. C4 Cavagnaro (1988)

Aristida subulata Henrard C4 Cavagnaro (1988)Aristida spegazzinii Arechav C4 Cavagnaro (1988)Bouteloua curtipendula auct. non(Michx.) Torr.

C4 Cavagnaro (1988)

Bothriochloa springfieldii (Gould) Parodi C4 Cavagnaro (1988)Bromus catharticus Vahl C3 Cavagnaro (1988)Cortaderia ridiuscula Stapf C3 Cavagnaro (1988)Cortederia selloana (Schult. & Schult. f.)Asch. & Graebn.

C3 Cavagnaro (1988)

Digitaria californica (Benth.) Henrard C4 Cavagnaro (1988)Distichlis scoparia (Kunth) Arechav. C4 �15.0 Bender (1971)Eragrostis cilianensis (All.) Vignolo ex Janch. C4 Cavagnaro (1988)Eragrostis lugens Nees C4 Cavagnaro (1988)Festuca rubra L. C3 Cavagnaro (1988)Hordeum comosum J. Presl C3 Cavagnaro (1988)Leymus erianthus (Phil.) Dubcovsky C3 Cavagnaro (1988)Melica andina J. Presl C3 Cavagnaro (1988)Muhlenbergia torreyii (Kunth) Hitchc. ex Bush C4 Cavagnaro (1988)Panicum urvilleanum Kunth C4 Cavagnaro (1988)Phragmites australis (Cav.) Trin. ex Steud. C3 �26.6 Bender (1971)Poa lanuginosa Poir. C3 Cavagnaro (1988)

(Continues)

Copyright # 2009 John Wiley & Sons, Ltd. Int. J. Osteoarchaeol. 19: 130–143 (2009)DOI: 10.1002/oa


Table 1. (Continued)


d13C% References

Setaria leucopila (Scribn. & Merr.) K. Schum. C4 Cavagnaro (1988)Sporobolus rigens (Trin.) E. Desv. C4 Cavagnaro (1988)Stipa sp. C3 Cavagnaro (1988)Trichloris crinita (Lag.) Parodi C4 Cavagnaro (1988)

Portulacaceae Portulaca grandiflora Hook. C4 �11.4 Bender (1971)Portulaca oleraceae L. C4 �12.1 Bender (1971)

Rhamnaceae Condalia microphylla Cav. C3 �25.3 Gil et al. (2006)Scrophulariaceae Mimulus sp. C3 �34.1 Smith & Epstein

(1971)Solanaceae Lycium sp. C3

Physalis viscosa L. C3 �27.2 Bender (1971)Solanum sp. C3 Hnatiuk (1980)

Typhaceae Typha domingensis Pers. C3 �31.0 Bender (1971)Verbenaceae Nesparthon aphyllum C3

Sources: Bender (1971); Smith & Epstein (1971); Downton (1975); Raghavendra & Das (1978); Boutton et al. (1980);Hnatiuk (1980); Cavagnaro (1988); Ehleringer et al. (1997); Gil et al. (2006).

136 C. Llano

the photosynthetic pathways of the plantsconsumed by Pterocnemia pennata revealed a strongtendency towards the consumption of C3 plants(Figure 4).

Candia & Dalmasso (1995) determined the dietof Lama guanicoe using the method of direct visualobservation of guanaco populations in La Payuniareserve, Malargue, Mendoza (368520S, 688300W).Other studies carried out in La Payunia by Puigand colleagues on the dietary preferences of Lamaguanicoe are considered here (Puig et al., 1996).The diet was determined through faecalsampling, and shows a preference for theconsumption of different food items. Grassessuch as Panicum, Poa and Hordeum, as well as lowshrubs such as Hyalis and Ephedra, are importantcomponents of the guanaco diet. Table 3summarises the results for Lama guanicoe diet,revealing the same tendency as observed forPterocnemia pennata, given the predominance ofC3 species. This may be due to the predominanceof C3 species on the landscape relative toC4 species (Figure 4).

There is important information on the localplants potentially utilised by human populationsfor nutritional and medicinal purposes (Table 4;Ragonese & Martınez Crovetto, 1947; Hernan-dez, 2002). This set of plants includes 32 species,of which at least 11 of the edible specieswere found in direct association with culturalremains in archaeological contexts. These include


Phaseolus vulgaris, Zea mays, Cucurbita maxima,Lagenaria sp., Prosopis sp. and Amaranthus caudatus.All of the identified species, except for Amaranthuscaudatus and Zea mays, follow the C3 photosyn-thetic pathway.

Discussion

Studies of species with distinct photosyntheticpathways have been used to assess biogeographi-cal distributions and the relative abundance of C3

and C4 systems, and the manner in whichincorporation of plants with different photosyn-thetic pathways is reflected in isotopic values atdifferent trophic levels (Ehleringer, 1978; Tieszenet al., 1979; Hnatiuk, 1980; Tieszen & Fagre, 1993).

There is a clear difference in the distribution ofplants according to photosynthetic pathways.The present work is consistent with studiesconducted by various authors regarding patternsof species distribution, all showing a predomi-nance of plants with a C3 photosyntheticpathway across the landscape, increasing in thehighlands, while C4 species increase in thelowlands (Ehleringer, 1978; Tieszen et al., 1979;Hnatiuk, 1980; Cavagnaro, 1988).

It is interesting to note that there is acorrelation between species habitat, physiologyand distribution. In general, C3 species areabundant in moist, shady areas with low solar


Table 2. Spatial distribution of species with C3 and C4 photosynthetic pathways at 358S

Family Species Lat. 358S Photosynthetic pathway

I II

Amaranthaceae Gompherena mendocina � � C4

Anacardiaceae Schinus polygamus þ þ C3

Apiaceae Mulinum spinosum � þ C3

Asteraceae Brachyclados lycioides � � C3

Eupathorium buniifolium þ � C3

Grindelia chiloensis þ þ C3

Hyalis argentea þ � C3

Senecio filagenoides � þ C3

Senecio subulatus þ þ C3

Senecio subumbellatus � � C3

Berberidaceae Berberis grevilleana � � C3

Boraginaceae Heliotropium mendocinum � � C4

Phacelia magellanica � � C3

Chenopodiaceae Atriplex lampa þ � C4

Atriplex patagonica � þ C4

Kochia scoparia � � C4

Ephedraceae Ephedra triandra � þ C3

Ephedra ochreata þ � C3

Fabaceae Adesmia aff. glomerula � � C3

Astragalus pehuenches � � C3

Geoffroea decorticans � � C3

Hoffmanseggia glauca � � C3

Prosopis alpataco þ � C3

Prosopis flexuosa � � C3

Senna arnottiana � � C3

Plantaginaceae Plantago patagonica � � C3

Poaceae Aristida subulata þ � C4

Aristida spegazzinii � � C4

Bouteloua curtipendula þ � C4

Bromus brevis � � C3

Distichlis scoparia þ � C4

Elymus erianthus � � C3

Hordeum murinum � þ C3

Panicum urvilleanum þ þ C4

Poa holciformis � � C3

Poa lanuginosa � � C3

Setaria leucopila � � C4

Sporobolus rigens þ � C4

Stipa chrysophylla � þ C3

Stipa humilis � � C3

Stipa ichu � � C3

Stipa neaei � � C3

Stipa speciosa � þ C3

Stipa tenuis þ � C3

Rosaceae Acaena pinnatifida � � C3

Solanaceae Lycium sp. þ � C3

Verbenaceae Nesparthon aphyllum þ þ C3

Zygophyllaceae Larrea divaricata þ � C3

Larrea nitida � þ C3

I: 200–1600 m.a.s.l.; II: 1600–2600 m.a.s.l.�, species absent; þ, species present.


irradiance, as well as in temperate and highmountain regions. C4 species inhabit drier orxerophytic locations, with greater solar irradiance(Rugolo de Agrassar et al., 2005). The results of


the present study show that, in spite of thegeneral predominance of the C3 photosyntheticpathway, at the family level as well as the level ofgenus and species, this pathway type becomes


Figure 2. Presence/absence of plant types by altitude along the survey transect with their photosynthetic pathways.

138 C. Llano

less prevalent in the lowlands, while at the sametime C4 species increase in frequency. Although adetailed study of the correlation betweenprecipitation and temperature and proportionsof C3 and C4 plants has not yet been conducted insouthern Mendoza, the pattern is probablysimilar to that in the north. Cavagnaro (1988)showed a clear correspondence between precipi-tation and temperature in northern Mendoza. Inthe cordillera, where mean annual precipitation ishigher, between 300 and 1000 mm, and meantemperature is between 108 and 208C, there is ahigher proportion of C3 species. In the lowlandplains, where temperatures are higher and mean

Figure 3. The spatial distribution of photosynthetic pathwayr¼�0.36 (C4).


annual precipitation is lower (250 mm), C4

species increase in frequency.Regarding the dietary composition of the

animals found most frequently in the archae-ological record of the region, the diet of Lamaguanicoe is composed mainly of gramineous plants(Candia & Dalmasso, 1995). The most frequentlyeaten genera correspond to Panicum (C4), Poa (C3)and Stipa (C3), according to their availability(Puig et al., 1996). Isotopic information obtainedfrom Lama guanicoe in the highlands of southernMendoza Province, from sites such as El Desechoand El Indıgeno, indicates less enriched values(�19.1%), while results for the same species

s: the correlation coefficent with altitude is r¼ 0.64 (C3),


Table 3. Plant species in the diet of Pterocnemia pennata (Paoletti & Puig, 2007) and of Lama guanicoe (Candia &Dalmasso, 1995)


Diet ofPterocnemia pennata

Diet ofLama guanicoe

Amaranthaceae Gompherena pumila C4 x —Anacardiaceae Schinus fasciculatus C3 — xApiaceae Mulinum spinosum C3 — xAsteraceae Artemisia mendozana C3 x —

Brachyclados lycioides C3 — xConyza lorentzi Ind x —Chuquiraga erinacea C3 x —Gutierrezia sphathulata C3 — xGrindelia chiloensis C3 — xHyalis argentea C3 — xNassauvia axillaris Ind x —Senecio filagenoides C3 x xSenecio subulatus C3 x x

Berberidaceae Berberis empetrifolia C3 x —Berberis grevilleana C3 — x

Boraginaceae Heliotropium sp. C4 x —Phacelia sinuata C3 x —Phacelia artemisiodes C3 x —

Cactaceae Maihuenia patagonica CAM — xMaihuenipsis glomerata CAM x —

Capparaceae Capparis atamisquea Ind x —Ephedraceae Ephedra andina C3 x —

Ephedra ochreata C3 — xEuphorbiaceae Euphorbia spp. C4 x —Fabaceae Adesmia horrida C3 x —

Adesmia trijuga C3 — xAstragalus spp. C3 x —Hoffmansegia eremophila C3 x —Medicago spp. C3 x —Prosopis flexuosa C3 — xProsopidastrum globosum C3 — x

Geraniaceae Erodium cicutarium C3 x —Loasaceae Mentzelia parviflora Ind x —Malvaceae Sphaeralcea philippiana C3 x —Nyctaginaceae Bougainvillea spinosa C3 — xOxalidaceae Oxalis muscoides C3 x —Plantaginaceae Monttea aphylla C3 — xPoaceae Aristida sp. C4 — x

Bothriochloa springfieldii C4 — xBromus setifolius C3 x —Melica chilensis C3 x —Panicum urvilleanum C4 — xPoa lanuginosa C3 x xSporobolus rigens C4 — xStippa spp. C3 x —

Polygalaceae Bredemeyera microphyla Ind x —Portulacaceae Montiopsis gilliesii Ind x —Rosaceae Acaena sericea C3 — x

Tetraglochim alatum Ind — xSolanaceae Lycium chilense C3 x x

Solanum spp. C3 x —Verbenaceae Glandularia crithmifolia Ind x x

Junellia spp. Ind x —Neosparton aphyllum C3 — x

Zygophyllaceae Larrea divaricata C3 x x

Copyright # 2009 John Wiley & Sons, Ltd. Int. J. Osteoarchaeol. 19: 130–143 (2009)DOI: 10.1002/oa


Figure 4. Plant species with different photosynthetic pathways in the diets of Pterocnemia pennata (determined throughfaecal sampling) and Lama guanicoe (determined through direct visual observation of guanaco feeding behaviour).

140 C. Llano

found in sites located in the lowlands (e.g. Aguade Los Caballos-1) show more enriched values(�14.2%; Gil et al., 2006). The more enrichedvalues seen in Lama guanicoe from lowland sites canbe attributed to environmental conditions thatfavour the growth or preference of species withthe C4 photosynthetic pathway.

Table 4. Plant species potentially edible by and/or of poss

Family Species

Amaranthaceae Amaranthus caudatusAnacardiaceae Schinus polygamusAsteraceae Xanthium spinosumBerberidaceae Berberis empetrifolia

Berberis cuneataCactaceae Cereus aethiops

Maihuenia sp.Opuntia sulfureaTrichocereus candica

Cucurbitaceae Cucurbita maximaLagenaria sp.

Ephedraceae Ephedra ochreataEphedra triandra

Ericaceae Pernettya pumilaFabaceae Senna arnottiana

Cercidium australeGeoffroea decorticansLathyrus macropusPhaseolus vulgaris vaProsopis albaProsopis chilensisProsopis flexuosaProsopis nigraProsopis torquata

Hydnoraceae Prosopanche americaOlacaceae Ximenia americanaPoaceae Zea maysRhamnaceae Condalia microphyllaSolanaceae Lycium chilense


The modern diet of Pterocnemia pennata isdominated by species that photosynthesisethrough C3 photosynthetic pathways (Paoletti& Puig, 2007). This is consistent with the resultsof analyses performed on samples of Rheaamericana and Pterocnemia pennata from archaeolo-gical sites located in the piedmont, where

ible medicinal use for humans

Photosynthetic pathway

C4

C3

C3

C3

C3

CAMCAMCAM

ns CAMC3

C3

C3

C3

IndC3

C3

C3

Indr. Oblongus C3

C3

C3

C3

C3

C3

na IndIndC4

C3

C3



d13C values are between �20% and �21% (Gilet al., 2006).

Analysis of prehistoric human remains fromsites in southern Mendoza shows significantd13CCOL variation, from �18.5% to �13.9%(Gil, 2003; Gil et al., 2006), which may reflect aheterogeneous ecological context for theinterpretation of palaeodiets. In order to interpretthe variations in d13C among human samples, it isnecessary to conduct detailed studies in specificgeographical areas.

Conclusions

There are three important points that can bemade on the basis of the analysis developed in thepresent study.

Firstly, the distribution of C3 and C4 plantsalong an altitudinal gradient was recorded inseveral transects conducted in Mendoza Pro-vince. The presence of C3 plants was evaluatedalong the entire altitudinal gradient, suggestingthat they are more abundant in the highlands,while the distribution of C4 plants increased inthe lowlands.

Secondly, analyses of the diet of Lama guanicoeand Pterocnemia pennata, the dominant animal taxafound in archaeological contexts in Mendoza,indicate a large consumption of C3 plants to thedetriment of C4 species. This could be due to twothings: (1) the predominace of C3 species in thelandscape, and/or (2) differences in nutritionalquality between C3 and C4 species and the lowerdigestibility of some C4 plants. On the otherhand, the work by Puig et al. (1996) on Lamaguanicoe dietary preferences indicates dietarychanges in the proportions of grasses and forbsaccording to their availability.

Thirdly, isotopic information derived fromprehistoric human remains indicates a significantvariation in the use of C4 resources anddemonstrates that they were not a quantitativelysignificant part of human diets in the study area.The relationship between isotopic values and thedifferent participants at different trophic levelsneeds to be evaluated.

Sampling procedures may have to be refined inorder to understand the variation not only in thealtitudinal distribution of these plant types, but


also in the differences in the d13C values ofherbivores and human samples. Finally, a betterunderstanding of the isotopic ecology will help usto improve our knowledge of human populationsand animal migrations.

Acknowledgements

I thank Gustavo Neme, Adolfo Gil, Analia For-asiepi and Agustin Martinelli for their commentson an earlier version of this manuscript, andRaven Carper and Juliana Sterli for their helpwith the English translation. I also thank LarryTieszen and Julieta Aranibar for providing usefulsuggestions for improving the manuscript. Thisresearch was funded by the Agencia Nacional dePromocion Cientıfica y Tecnologica (N8 4-14695).

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