Oecologia (1988) 76:273-277 Oecologia Springer-Verlag 1988

Distribution of C3 and C4 grasses at different altitudes in a temperate arid region of

J.B. Cavagnaro Ecofisiologia Vegetal, IADIZA (Instituto Argentino de Invest. de Zonas Aridas), C.C. 507, 5500 Mendoza, Argentina

Summary. The distribution of native C3 and C4 grasses seems to be linked to certain environmental factors such in a temperate arid region of Mendoza, Argentina, was as temperature and water availability (Teeri and Stowes studied in six areas at different altitudes. C4 species predom- 1976; Tiezsen et al. 1979; Rundel 1980; Barnes and Harr- inate at low elevations in both relative species abundance ison 1982; Barnes et al. 1983; Hattersley 1983). In addition, and cover. At high elevations C3 species are dominant in this family most of the species have been clearly deter- in cover and composition. At medium altitudes mined as C3 or C~ on the ground of their anatomical and (1100-t600 m) grass species composition is balanced but physiological characteristics (Smith and Brown 1973; plant cover of Cs species is greater. Of 31 genera in the Downton 1975; Hattersley and Watson 1975). whole area, 19 were C4. Only the genera Stipa (C3) and The aim of this paper is to report the relative distribu- Aristida (C4) were present in all the six areas surveyed. tion and coverage of C3 and C4 grasses in areas located The pattern of grass distribution shows high correlation at different altitudes in a temperate arid region of Mendoza, with evapotranspiration and temperature parameters, but Argentina. The relation between these aspects and some low correlation with rainfall. The relation between grass meteorological parameters from these areas is discussed. distribution and different climatic parameters is discussed.

Key words: Grasses - Photosynthetic type - Distribution Material and methods - Climate - Altitude - Argentina The C4 type was established by the presence of Kranz anat- omy in cross-sections of leaf blades or from the data com- piled by other authors (Smith and Epstein 1971 ; Smith and Brown 1973 ; Downton 1975 ; Hattersley and Watson 1975). The most important characteristics of with different Leaf blades were obtained from field plants or from herbar- CO2 fixation pathways (C3, C4, CAM) have been summa- ium material. rized by Black (1973). Plants belonging to these groups The region surveyed is located between 32~ , and show different anatomical, biochemical, physiological, and 34~ and 69007 , and 68~ (Fig. 1). The study areas ecological characteristics. Thus, C, species have a higher are located at different elevations ranging from 570 to optimum temperature for photosynthesis, higher light in- 2400 m (Fig. 2): tensity for saturation, higher water use efficiency and lack detectable photorespiration. In contrast, C3 plants achieve Area I: plain, 560-580 m, shrubland their maximum photosynthetic rates at lower temperatures Area II: piedmont, 750-1100 m, shrubland and lower light intensities, and they show photorespiration. On the basis of previous statements, it has been postu- Area III: piedmont, 940-1400 m, shrubland lated that the photosynthetic type confers adaptive advan- Area IV: piedmont, 1200-1600 m, shrubland tages under certain environmental conditions. C4 plants should be favoured by high temperature, high irradiance, Area V: piedmont, 1300-1800 m, shrubland and limited water supply. C3 species should be favoured by Area VI: highland plain, 2200-2600 m, grassland cool, shade, and humid conditions (Ehleringer and Bj6rk- man 1977; Ehleringer 1978). Despite these generalizations, According to the phytogeographical classification of Ca- some exceptions have been reported where C4 species can brera (1976) areas I, II, and III correspond to the "Monte" succesfully compete in cool or shaded habitats (Caldwell province. Areas IV and V would be transitional between etal. 1977; Pearcy and Troughton 1975). Besides, other "Monte" and "Prepuna", and finally area VI belongs to plant features, apart from the photosynthetic pathway, can "Prepuna" province. Those areas related to the "Monte" play a major role in the competitive ability of plants (Baskin are characterized by the dominance of Zygophyllaceae, spe- and Baskin 1978; Pearcy and Ehleringer 1984). Moreover, cially of the Larrea (Morello 1958). Syvertsen et al. (1976) have reported that in some desert The species list for area I was compiled by the author. communities C3 species surpass C4 ones in presence and The rest of the distribution data was taken from: Roig biomass. (1976) (areas II and IV); Martinez Carretero (1982, 1985) In the family Poacea, C3 and C4 species show a well (areas III and V) and Passera et al. (1983) (area VI). Species defined pattern of geographical distribution. This pattern list in these papers are based on extensive and detailed phy- 274

Table l. C4 grasses and plant cover in the study areas

Species Areas I II III IV V VI

* Aristida adscencionis + + + + + -- Aristida aft. humilia ..... + - * Aristida mendocina 2 - + - + - * Aristida spegazzini -- -- + -- + + Bothriochloa springfieldii - - 1 - + + * aristidoide + ..... Bouteloua barbata + + .... Bouteloua curtipendula - - + - + - * Bouteloua lophostachya - + - + - - * Chloris castilloniana + ..... * Cottea pappophoroides + + - + - - * Dig#aria californica 1 -- + + + - * Diplachne dubia + + + + + - * Eragrostis eilianensis + + - + -- -- Eragrostis lugens .... + + * Eragrostis pilosa + + - + -- -- * Erioneurum pilosum -- -- + -- + -- Muehlenbergia asperifolia - - + - - - Muehlenbergia torreyi ..... + * Munroa mendocina + 1 - + - - * Neobouteloua lophostachya + -- + ------N. * Panicum urvilleanum + ..... * Pappophorum caespitosum 2 + + + + - * Pappophorum philippianurn + + + + + - * Scleropogon brevifolius + ..... * Setaria leucopila + + + + + -- Fig. 1. The location of the study area in Mendoza, west Argentina * Setaria mendocina + ..... Setaria pampeana - - + - - - * Sporobolus cryptandrus 1 - + 1 + - * Tragus berteronianus + ..... * Trichloris crinita 1 + + + - -

I00. Total species present 21 12 16 13 14 4 C4 gr=~asse"~ C 3 grasses -, species absent; +, less than 0.1% of plant coverage; 1, 0-5% 80. cover; 2, 5%-25% cover; 3, 25%-50% cover. * Kranz anatomy; e.. inspected by the author o 8 60. E tosociological work and the species mentioned are included 0 r 40. t"-.../",,.. in the IADIZA Herbarium (MERL). ill -1 The region has a temperate-arid climate. Rainfall occurs mainly in summer and originates in convective storms. 20 / -.... Snow is important only in area VI, where 100-120 mm per ! year have been measured. The climatic data were obtained from meteorological 0 s6o 660 e6o ,ioo ,. oo ,goo aioo z,ioo stations located in the study areas (Estrella, unpublished data; Vich 1987). Values for temperature and rainfall are altitude [meters) averaged over 15 and 11 years respectively. Potential evapo- transpiration and water deficits were estimated according to Burgos and Vidal (1951). Grass cover values in Table 1 E W follow the abundance-dominance criterium of Braun-Blan- quet's phytosociological method (Roig 1973). 5000 oE 2000 Results "O

.m A clear pattern of grass distribution as a function of altitude is observed in Fig. 2. C4 species are dominant at lower a I000 elevations. Between 1100 and 1600m the relative abun- dance of both types is quite similar. At the highest eleva- tions C3 species are dominant. 6 // 9o ,oo Out of 31 genera found, 12 were C3 and 19 were CA, Fig. 2. Relative grass species abundance and altitudes of the study though the latter includes the genus Panicum which has areas both C3 and C4 species. In this case only Panicum urviI- 275

Table 2. C3 grasses and plant cover in the study areas Table 3. Altitude and climatic parameters of the study areas

Species Areas I II III IV V IV Parameters Areas I II III IV V VI

* Bromus araucanus ..... + Altitude (m) 570 920 1170 1450 ~1600 2400 * Bromus brevis - - - + + 1 Mean annual 15.7 16.3 13.6 14.2 10.5 7.8 * Bromus sp. ------+ + temperature (~ Cortaderia rudiuscula - - + - - - Elymus erianthus _ _ + + + _ January 24.4 24.2 21.5 21.0 17.1 13.5 Elytrigia atternuatta ..... + mean temperature (~ * Elytrigia mendocina ..... + July mean temperature 6.9 8.1 6.1 7.4 5.0 2.4 * Festuca rubra ..... + (~ * Koeleria mendocinensis ..... + January mean maximum 32.5 30.0 28.3 25.0 22.7 18.7 Melica andina .... + + temperature (~ * Piptochaetium napostaense - - + + + + * Poa lanuginosa .... + + January mean minimum 16.4 18.5 14.0 13.3 12.9 8.4 * Poa resinulosa .... + 2 temperature (~ Poa ligularis - - + - + + Annual rainfall (mm) 344 255 164 200 194 421 * Polypogon monspeliensis - - + - + + October-March 264 192 135 157 153 344 Sehismus barbatus .... + - rainfall (mm) Stipa debilis - - + - + - Annual 829 828 726 727 630 558 * Stipa ichu + - 2 + 2 + Stipa paramilloensis .... + + evapotranspiration * Stipa plumosa _ + + + + _ (ram) Stipa psittacorum - - + - + - October-March 642 645 558 554 466 411 Stipa sanluisensis - - 1 + 2 - evapotranspiration Stipa scirpea - - + - 1 + (mm) * Stipa tenuis - - + 1 + - Water deficit from 378 454 423 397 313 67 * Stipa tenuissima - - + - 1 3 October to March (ram) * Stipa vaginata - - 1 1 1 + C4 grass percentage 95.5 92.3 53.3 61.9 41.1 18.2 Total species present 1 1 14 8 20 18 Ca grass percentage 4.5 7.7 46.7 38.1 58.9 81.8 -, species absent; +, less than 0.1% of plant cover; 1, 0-5% cover; 2, 5%-25% cover; 3, 25%-50% cover. * Lack of Kranz anatomy; inspected by the author Table 4. Linear regression analysis of C4 grass distribution and environmental variables (Y= a + bX) leanum, which is C4, was present. Only Aristida (C4) and Variables R a b Stipa (C3) were present in all the six areas surveyed. Consid- ering the number of species, 26 were C3 and 31 C4. Among Annual average temperature (~ 0.96 b - 50.4 8.48 Ca grasses, the genus Stipa was the largest with 10 species, January average temperature (~ 0.968 - 71.4 6.46 while Aristida and Bouteloua (C4) had 4 species each. July average temperature (~ 0.90" - 14.9 12.47 Tables 1 and 2 show the presence of C3 and C4 species January maximum temperature (~ 0.93 b - 78.3 5.27 in each area, as well as the species cover-according to the January minimum temperature (~ 0.95 b -- 50.8 7.95 Annual rainfall (mm/yr) -- 0.17 ns 72.2 -- 0.05 criterion used in Braun Blanquet's censuses (Roig 1973). October-March rainfall (ram) --0.24 ns 78.2 -0.09 Area I, at the lowest elevation, has 21 C4 species and Annual evapotranspiration (mm/yr) 0.98 b - 128.1 0.26 only i C3 species. The most important species in terms of October-March evapotranspiration 0.98 b - 104.3 0.30 cover are Aristida mendocina, Pappophorum caespitosum, (ram) Sporobolus cryptandrus, and Trichloris crinita. The only C3 Annual water deficit (mm/yr) 0.75 ns - 0.4 0.13 species in this area, Stipa ichu, is always found in shady October-March water deficit (mm) 0.79 ns 5.1 0.16 places beneath trees. Area II has the lowest richness with only 13 species, 12 of them C4 and only 1 C3. Again, the R = linear correlation coefficient; "significant at P < ,0.05; b = sig- C3 species belongs to the genus Stipa and is found in more nificant at P < 0.01 ; ns = non-significant shaded and humid places. Although the species composition of areas III, IV, and are shown in Table 4. The highest correlation coefficients V is quite balanced between C3 and C4 species (Fig. 2), were with evapotranspiration and temperature (R=0.98 C3 species are more important in terms of plant cover. and R=0.96 respectively). Evapotranspiration was calcu- The most important species are those of the genus Stipa lated according to Thornthwaite's formula, which is based such as S. iehu, S. sanluisensis, S. tenuissima, S. tenuis, and on temperature. Correlation with rainfall was very low. The S. vaginata. R values for water deficit, which were calculated as the The highest elevation (area VI) shows a complete domi- difference between evapotranspiration and rainfall, are in- nance of C3 grasses in both relative abundance and plant termediate but still not significant. cover. Stipa tenuissirna, Poa resinulosa, and Bromus brevis are outstanding in this respect. Discussion Table 3 shows the altitude and climatic parameters of the areas studied. The linear correlation coefficients for per- The results of this paper clearly show differences in the centage of C4 species and the climatic factors in those areas distribution of C3 and C4 grasses. The grass species compo- 276

sition at different altitudes agrees with the results obtained correlation coefficient between altitude and rainfall is low by Tiezsen et al. (1979) and Rundel (1980). At low eleva- and non-significant (R=0.56). Except for area VI, which tions C4 species are dominant, the relative abundances are has snow every year, the rest of the areas get most of their similar at medium altitudes, and at the highest elevation water in summer, from convective storms of highly variable C3 species predominate. frequency and intensity. However, as altitude increases, The transition range for the dominance of C3 and C4 higher water availability can occur as a consequence of grasses occurs between 1100 and 1600 m. These altitudes lower evapotranspiration and dew. Hence, in these circum- are lower than those mentioned by Tiezsen et al. (1979), stances rainfall is not a good predictor of C4 grass distribu- but quite similar to those of Rundel (1980). These two tion. papers described tropical environments where, despite dif- Moreover, these results show that biomass production ferences in altitudes, the mean maximum and mean mini- in arid regions is possible for species with any of the photo- mum temperature for the warmest month were quite similar synthetic types, depending on the temperature conditions (21~ and 9~ respectively). The results presented here in each area. Thus, except for area VI, which has the lowest show that floristic balance between C3 and C4 grasses oc- water deficits, the rest of the areas had permanent water curs at higher temperatures. Thus, the mean maximum tem- deficits. In areas I and II biomass production, expressed perature for the warmest month is 23~ ~ C, and the mean as plant cover, was dominated by C4 species. In areas III, minimum temperature is 13~ ~ C. These values are closer IV, and V, Ca species surpassed C4 ones in plant cover to those obtained by simulation by Ehleringer (1978), sug- despite a similar number of species. gesting that in temperate climates the transition range oc- Finally, if we assume that the current distribution of curs at higher temperature than in tropical environments. Ca and C4 species in the region is the consequence of the Teeri and Stowes (1976) found the minimum tempera- recently prevailing climate, we can postulate that C3 and ture of the warmest month to be the best predictor of C4 C4 grass distribution along this gradient is correlated with grass distribution. The results of this paper show that what- temperature more than with water availability. ever temperature we consider (mean annual, warmest month, etc), it will be a good predictor of C4 grass percent- Acknowledgements. I wish to thank F. Roig, R. Tizio, O. Trione, age in a given area. These results also agree with their postu- and C. Passera for their critical reading and suggestions concerning late that sites with minimum temperatures below 8~ the manuscript. This work was supported by CONICET. should have few or no C4 species, as is the case in area VI. According to Ehleringer and Bjrrkman (1977), at nor- References mal CO2 concentrations, the quantum yield of C3 species decreases as temperature increases over 30 ~ C. The quan- Barnes PW, Harrison AT (1982) Species distribution and commun- tum yield of C4 species is independent of temperature. ity organization in a Nebraska sandhill mixed prairie as in- fluenced by plant/soil-water relationships. Oecologia (Berlin) Therefore, C4 species would have competitive advantages 52:192-201 at the high temperatures of areas I and II. The advantage Barnes PW, Tiezsen LL, Ode DJ (1983) Distribution, production in net photosynthesis in C3 species at high temperatures and diversity of C3- and C4-dominated communities in a mixed is the result of enhanced concentration of CO/at the fixa- prairie. Can J Bot 61 : 741-751 tion levels, and consequently lower photorespiration. In Baskin JM, Baskin CC (1978) A discussion of the growth and contrast, at low temperatures, quantum yields for C3 species competitive ability of C3 and C4 plants. Castanea 43 : 71-76 are higher than for C4 and the former will be favoured, Black CC (1973) Photosynthetic carbon fixation in relation to net as occurs in area VI. CO2 uptake. Annu Rev Plant Physiol 24:253-286 Hattersley (1983) pointed out the convenience of study- Burgos JJ, Vidal AL (1951) Los climas de la Repnblica Argentina segun la nueva clasificacion de Thornthwaite. Meteoros 1 : 3-32 ing grass distribution not only in a relative form, that is Cabrera A (1976) Regiones fitogeograficas . Enciclope- as percentage of C4 species, but also as C3 and C, species dia Arg. de Agric. y Jardineria, fasciculo I. Ed. ACME, Buenos number in different areas. In this paper, the linear correla- Aires, 85 pp tion coefficients between total grass number and altitude, Caldwell MM, White RS, Moore RT, Camp LB (1977) Carbon mean annual temperature, and mean annual rainfall were balance, productivity and water use of cold winter desert shrub not significant. Only January mean maximum temperature communities dominated by C3 and C4 species. Oecologia (Ber- shows a significant correlation coefficient with C4 number. lin) 29:275-300 When the climatological parameters were regressed against Downton WJS (1975) The occurrence of C4 photosynthesis among C3 grass number, significant negative correlations coeffi- plants. Photosynthetica 9:96-105 Ehleringer JR (1978) Implications of quantum yield differences cients were obtained with evapotranspiration and tempera- on the distribution of C3 and C4 grasses. Oecologia (Berlin) ture parameters (not shown in Table). Despite this, it is 31:255-267 interesting that grass distribution expressed in a relative Ehleringer JR, Bjrrkman O (1977) Quantum yields for COz uptake form (e.g. % C4) can be interpreted as the final result of in C3 and C4 plants: dependence on temperature, CO2 and competition between C3 and C4 species in the same environ- O2 concentrations. Plant Physiol 59:86-90 ment. Hattersley PW (1983) The distribution of C3 and C4 grasses in Although the correlation coefficients are not indicative Australia in relation to climate. Oecologia (Berlin) 57:113-128 of causal relationships, they indicate a stronger association Hattersley PW, Watson L (1975) Anatomical parameters for pre- with temperature than with precipitation. Some papers dicting photosynthetic pathways of grass leaves: The 'maxi- mum lateral cell count' and the 'maximum cell distance count'. about distribution of C3 and C4 grasses along altitudinal Phytomorphology 25 : 32~333 gradients have mentioned that temperature and precipita- Martinez Carretero E (1982) Carta fitosociologica de la hoja Men- tion change inversely and gradually as altitude increases doza 230-21 (C Casa de Piedra-Rio San Isidro). Informe CON- (Tieszen et al. 1979; Rundel 1980). In our case, rainfall ICET 1980-82, 70 pp does not increase simultaneously with elevation. The linear Martinez Carretero E (1985) La vegetation de la reserva natural 277

Divisadero Largo (Mendoza, Argentina). Doc Phytosociol Smith BN, Epstein S (1971) Two categories of 13C/12~Cratios for 9:25 49 higher plants. Plant Physiol 47 : 380-384 Morello J (1958) La provincia fitogeografica del Monte. Opera Syvertsen JP, Nickell GL, Spellenberg RW, Cunningham GL Lilloana 2:1-155 (1976) Carbon reduction pathways and standing crop in three Passera CB, Dalmasso AD, Duffar E (1983) Ambiente fisico y Chihuahuan desert plant communities. Southwest Nat vegetacion de las pampas de los Nangos y Seca, Mendoza, 21 : 311-320 Argentina. Deserta 7 : 108-144 Teeri JA, Stowes LG (1976) Climatic patterns and the distribution Pearcy RW, Troughton JH (1975) C4 photosynthesis in tree form of C4 grasses in North America. Oecologia (Berlin). 23 : 1-12 Euphorbia species from Hawaiian rainforest sites. Plant Physiol Tiezsen LL, Senyimba MM, Imbamba SK, Troughton JH (1979) 55:1055-1056 The distribution of C3 and C4 grasses and isotope discrimina- Pearcy RW, Ehleringer J (1984) Comparative ecophysiology of tion along an altitudinal and moisture gradient in Kenya. Oeco- C3 and C4 plants. Plant, Cell Environ 7:1-13 logia (Berlin) 37 : 337-350 Roig FA (1973) El cuadro fitosociologico en el estudio de la vegeta- Vich AIJ (1987) Estimacion del indice de erosividad R, en el area cion. Deserta 4:45-67 pedemontana del gran Mendoza (Argentina). Rev Geofis (in Roig FA (1976) Las comunidades vegetales del piedemonte de la press) precordillera de Mendoza. Ecosur 3 : 1-45 Rundel PW (1980) The ecological distribution of C, and C3 grasses in the Hawaiian islands. Oecologia (Berlin) 45 : 354-359 Smith BN, Brown WV (1973) The Kranz syndrome in the Gramin- eae as indicated by carbon isotopic ratios. Am J Bot 60: 505-513 Received October 25, 1987