| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
0 Department of Ecology and Evolution, State University of New York, Stony Brook, New York 11794 USA
Received for publication January 4, 2000. Accepted for publication April 18, 2000.
ABSTRACT
I compared the C4 grass flora and climatic records for 32 sites in the United States. Consistent with previous studies, I found that the proportion of the grass flora that uses the NADP malic enzyme (NADP-ME) variant of C4 photosynthesis greatly increases with increasing annual precipitation, while the proportion using the NAD malic enzyme (NAD-ME) variant (and also the less common phosphoenolpyruvate carboxykinase [PCK] variant) decreases. However the association of grass subfamilies with annual precipitation was even stronger than for the C4 decarboxylation variants. Analysis of the patterns of distribution by partial correlation analysis showed that the correlations between the frequency of various C4 types and rainfall were solely due to the association of the C4 types with particular grass subfamilies. In contrast, there was a strong correlation of the frequency of the different subfamilies with annual precipitation that was independent of the influence of the different C4 variants. It therefore appears that other, as yet unidentified, characteristics that differ among grass subfamilies may be responsible for their differences in distribution across natural precipitation gradients.
Key Words: climate • C4 photosynthesis • grasses • NAD-ME photosynthesis • NADP-ME photosynthesis • PCK photosynthesis • Poaceae • precipitation
Differences among major taxonomic groups of grasses in distribution across continental scale gradients of temperature and precipitation have been noted at least since the 1950s (Hartley, 1958a, b
; Hartley and Slater, 1960
). At the time these observations were first made, there was little knowledge that could suggest possible physiological bases for the observed distributional differences among the grass subfamilies. Following the discovery of the C4 photosynthetic pathway in the 1960s (Hatch and Slack, 1966
), it became clear that different photosynthetic pathways were associated with different grass subfamilies (Hattersley, 1987
). Teeri and Stowe (1976)
for North America, Hattersley (1983)
for Australia, and Vogel, Fuls, and Ellis (1978)
for South Africa demonstrated that C4 grass species were relatively most abundant in areas of high temperature. Along with an understanding of mechanistic reasons for a higher temperature optimum for photosynthesis of C4 vs. C3 species (Ehleringer, 1978
) this has provided a convincing explanation for some of the differences in distribution among grass clades that were first noticed by Hartley (1958a, b, 1973
; Hartley and Slater, 1960
).
Some of the patterns noted by Hartley cannot be explained by the C3 vs. C4 distinction. Hartley found that the subfamily Eragrostoideae (= Chloridoideae) is distributed in drier areas than the tribe Andropogoneae (of the subfamily Panicoideae), although both taxa are exclusively C4 (Hartley, 1958a
; Hartley and Slater, 1960
). One potential explanation lies in the variation that is present within C4 photosynthesis. There are three distinct biochemical variants of C4 photosynthesis, with different C4 species using any one variant nearly exclusively. The three varieties of C4 photosynthesis are termed NAD malic enzyme (NAD-ME), NADP malic enzyme (NADP-ME), and phosphoenolpyruvate carboxykinase (PCK) after the bundle sheath decarboxylation enzyme used in each pathway (Hatch, Kagawa, and Craig, 1975
). There is a strong association of C4 variants with particular grass subfamilies. In the subfamily Chloridoideae, virtually all C4 species are of either the NAD-ME or PCK type (Table 1). In the subfamilies Arundinoideae and Panicoideae, the great majority of C4 species are NADP-ME (Table 1).
|
in Australia and Ellis, Vogel, and Fuls (1980)
in Namibia have found strong correlations between precipitation and the percentage of the C4 grass flora in an area with a particular C4 variant. Species with the NAD-ME variety of decarboxylation are predominantly found in the driest habitats, and the percentage of the C4 grass flora using the NADP-ME variety of decarboxylation increases with annual rainfall. As neither study distinguished the role of C4 pathway variation from that of subfamily membership, these observed patterns of distribution suggest two different hypotheses. One possibility is that the variants of C4 photosynthesis differ functionally, so that the NAD-ME pathway itself is more adaptive than the NADP-ME pathway to life in arid environments. The differences in the distributions of panicoid and chloridoid grasses noted by Hartley would result from the different C4 pathways that they use. Alternatively, the NAD-ME and NADP-ME C4 pathways may be functionally equivalent, and other characteristics of the grass subfamilies may be responsible for their differences in distribution across precipitation gradients. The differences in the distributions of the NAD-ME and NADP-ME pathways would then result from the chance evolutionary association of the pathways with these other, adaptively important characteristics of the grass subfamilies in which they occur.
If there were a perfect association of grass subfamilies with particular C4 variants, it would be impossible to distinguish between these two alternatives on the basis of geographic surveys of C4 grass distribution. However, ~26% of the worldwide C4 grass flora consists of species that are neither NAD-ME chloridoids nor NADP-ME panicoids (Table 1). It is therefore possible to consider the relationships of climatic variables with subfamily membership and C4 pathway variants separately, in an attempt to distinguish the roles of C4 pathway variation from that of subfamily membership in determining the geographic distributions of C4 grasses.
To address this question, I surveyed the C4 grass flora and climate of 32 sites from across the United States, using data assembled from a variety of sources (listed in the Appendix). The United States was chosen for this study because it provides a test of the relationships observed in Australia and Namibia on an additional continent, and because the extensive network of weather stations across the United States makes it possible to find weather data from locations near the floristic survey sites. Unlike previous studies, I statistically tested relationships with climate both on a C4 variant basis and on a grass subfamily basis.
MATERIALS AND METHODS
Sources for grass floras and climatic data are given in the Appendix. All flora sites in the databases used for this study were included in the analyses if they had at least 18 C4 grass species and were <600 km2 in area. A minimum number of C4 grass species was desired so that percentages of the flora at a site (for example, the percentage of C4 grass species which use the NAD-ME pathway) would not be excessively influenced by the recorded presence or absence of a single species. A maximum area for sites was desired to minimize the amount of climate variation likely to be present within a site.
Because the areas surveyed for flora lists varied greatly (1–593 km2), comparisons among sites in absolute numbers of species would depend largely on the size of the areas, rather than on the botanical characteristics of the sites. Data are therefore presented on the basis of percentages of the C4 flora rather than on absolute numbers of species.
Weather stations were located at an average distance of 23 km (maximum = 55 km) from the geographic center of their corresponding flora site. The average difference in altitude between weather stations and the average altitude for their corresponding flora site was 83 m (maximum = 357 m).
The variety of C4 photosynthesis used by each species was determined from several sources (primarily Table 2.2 in Hattersley and Watson, 1992
), using the established associations of leaf anatomy with C4 variants. Genera with Hattersley and Watson's type 1 or 6 leaf anatomy were identified as NADP-ME, and genera with type 2 or 7 leaf anatomy were identified as NAD-ME. Species of Panicum were identified to C4 variant based on leaf anatomy using Table 6 of Brown (1977)
, and by reference to Zuloaga (1987)
. The only leaf anatomy type found in this survey for which pathway cannot be confidently identified is Hattersley and Watson's leaf anatomy type 3; species with this type of leaf anatomy can be either PCK or NAD-ME. Some of these genera have been biochemically typed; these were identified from Hattersley (1987)
. Species which could not be resolved as to whether they were of the PCK or NAD-ME variants (e.g., a number of species in the genera Bouteloua and Sporobolus) were included in analyses based on grass subfamilies, but excluded from those which compared C4 variants.
Ten climatic variables were included in this study, including normal annual precipitation and nine temperature variables (Table 2). These climatic variables were chosen because previous studies have found both annual precipitation and mid-summer temperatures to be correlated with the proportion of NAD-ME and NADP-ME species in local and regional floras (Ellis, Vogel and Fuls, 1980
; Hattersley, 1992
).
|
The strongest relationships of grass subfamily and C4 variant frequency with climatic factors were with normal annual precipitation. The distributions of the Panicoideae and Chloridoideae subfamilies along precipitation gradients were diametrically opposed, with the Panicoideae positively (r = 0.89) and the Chloridoideae negatively (r = -0.90) correlated with normal annual precipitation (Fig. 1, Table 2). All three C4 variants were also highly significantly correlated with normal annual precipitation, the NADP-ME pathway positively (r = 0.83), and the PCK and NAD-ME pathways negatively (r = -0.75 and r = -0.68, respectively; Fig. 2, Table 2).
|
|
). This method allows consideration of the correlation that is found between two variables when the value of a third variable is mathematically held constant. In the present case, for example, partial correlation analysis allows us to consider the correlation between the percentage of the local C4 flora that uses the NADP-ME pathway and annual precipitation, free of the influence of the third variable, the percentage of the C4 flora that is in the Panicoideae. When partial correlation analysis is performed to remove the influence of the frequency of C4 pathway types, the correlations between the frequency of the Panicoideae and Chloridoideae subfamilies in local floras and normal annual precipitation remain large and highly significant (Table 3), with partial correlations of the frequency of the Panicoideae with annual precipitation of 0.61, and of the Chloridoideae subfamily with annual precipitation of -0.79 and -0.75 (with the frequency of the NAD-ME and PCK C4 variants held constant, respectively). This suggests that the relationships between the frequencies of these grass subfamilies and precipitation are independent of the frequency of the C4 decarboxylation variants.
|
DISCUSSION
The tight relationships found here between grass subfamily / C4 variant frequency and annual precipitation are especially striking in light of the relatively coarse nature of the analysis. Neither microsite variation nor the seasonality of precipitation have been taken into account in this analysis (or in that of Ellis, Vogel, and Fuls [1980
] in Namibia). Nonetheless, this study found, as have previous studies (Ellis, Vogel, and Fuls, 1980
; Hattersley, 1992
), a very strong and significant relationship between annual precipitation and the prevalence of the NAD-ME and NADP-ME photosynthetic pathways in local grass floras.
At least for the United States this seems to be due to a shared correlation of these variables with the frequencies of the Panicoideae and Chloridoideae grass subfamilies. This suggests that the correlations between the frequencies of the NAD-ME and NADP-ME C4 variants and annual precipitation found by Hattersley (1987)
and Ellis, Vogel, and Fuls (1980)
might also be due to the tight association between C4 variants and grass subfamilies.
A comparison of the distributions of PCK grasses in Australia and the United States additionally suggests the importance of subfamily-level traits other than C4 variants in structuring their distribution. The prevalence of the PCK pathway is negatively correlated with annual precipitation in the United States and positively correlated with annual precipitation in Australia (Hattersley, 1992
). The explanation for these divergent patterns may lie in the different compositions of the PCK flora of these two areas. In the United States, the great majority of PCK species are from the subfamily Chloridoideae. In the sites in this sample, for example, an average of 97% of the PCK species are from the subfamily Chloridoideae. In Australia, on the other hand, a slim majority (51%) of the PCK species are members of the Panicoideae (Prendergast, 1989
).
The results of the partial correlation analysis do not support the hypothesis that functional differences among the C4 variants are responsible for the differences in distribution between C4 panicoid and chloridoid grasses. This begs the question of what traits are responsible for the relationship between C4 variant composition in local floras and precipitation. It may well prove that no individual trait, but a suite of interrelated traits, including aspects of physiology, anatomy, and life history differ between these subfamilies and is ultimately responsible for the striking differences in distribution along precipitation gradients seen between the C4 members of the Chloridoideae and Panicoideae.
|
1 The author thanks Jessica Gurevitch and Daniel Sims and the anonymous reviewers for comments on drafts of this manuscript and Toby Kellogg and many others for discussion of this work. This is contribution 1069 in Ecology and Evolution, State University of New York, Stony Brook. 
2 Current address: Division of Earth and Ecosystem Sciences, Desert Research Institute, 2215 Raggio Parkway, Reno, Nevada 89512 USA.
LITERATURE CITED
Brown, W. V. 1977 The Kranz syndrome and its subtypes in grass systematics. Memoirs of the Torrey Botanical Club 23: 1–97.
Ehleringer, J. R. 1978 Implications of quantum yield differences on the distributions of C3 and C4 grasses. Oecologia 31: 255–267.[CrossRef][ISI]
Ellis, R. P., J. C. Vogel, and A. Fuls. 1980 Photosynthetic pathways and the geographical distribution of grasses in South West Africa/Namibia. South African Journal of Science 76: 307–314.[ISI]
Furbank, R. T., C. L. D. Jenkins, and M. D. Hatch. 1989 CO2 concentrating mechanism of C4 photosynthesis. Plant Physiology 91: 1364–1371.
Hartley, W. 1958a Studies on the origin, evolution and distribution of the Gramineae. I. The tribe Andropogoneae. Australian Journal of Botany 6: 115–128.
———. 1958b Studies on the origin, evolution and distribution of the Gramineae. II. The tribe Paniceae. Australian Journal of Botany 6: 343–357.[CrossRef]
———. 1973 Studies on the origin, evolution and distribution of the Gramineae. V. The subfamily Festucoideae. Australian Journal of Botany 21: 201–234.[CrossRef][ISI]
———, and C. Slater. 1960 Studies on the origin, evolution and distribution of the Gramineae. III. The tribes of the subfamily Eragrostoideae. Australian Journal of Botany 8: 256–276.[CrossRef]
Hatch, M. D., T. Kagawa, and S. Craig. 1975 Subdivision of C4-pathway species based on differing C4 acid decarboxylating systems and ultrastructural features. Australian Journal of Plant Physiology 2: 111–128.
———, and C. R. Slack. 1966 Photosynthesis by sugar cane leaves. A new carboxylation reaction and the pathway of sugar formation. Biochemical Journal 101: 103–111.[ISI][Medline]
Hattersley, P. W. 1983 The distribution of C3 and C4 grasses in Australia in relation to climate. Oecologia 57: 113–128.[CrossRef][ISI]
———. 1987 Variations in photosynthetic pathway. In T. R. Soderstrom, K. W. Hilu, C. S. Campbell, and M. E. Barkworth [eds.], Grass systematics and evolution, 49–64. Smithsonian Institute, Washington, D.C., USA.
———. 1992 C4 photosynthetic pathway variation in grasses (Poaceae): its significance for arid and semi-arid lands. In G. P. Chapman [ed.], Desertified grasslands: their biology and management, 181–212. Academic Press, London, U.K.
———, and L. Watson. 1992 Diversification of photosynthesis. In G. P. Chapman [ed.], Grass evolution and domestication, 38–116. Cambridge University, Cambridge, U.K.
NCDC (National Climatic Data Center). 1993a Local climatological data: annual summary with comparative data, Amarillo Texas. NCDC, Asheville North Carolina, USA.
———. 1993b Local climatological data: annual summary with comparative data, New Orleans Louisiana. NCDC, Asheville North Carolina, USA.
———. 1993c Local climatological data: annual summary with comparative data, Port Arthur Texas. NCDC, Asheville North Carolina, USA.
———. 1993d Local climatological data: annual summary with comparative data, Scottsbluff Nebraska. NCDC, Asheville North Carolina, USA.
———. 1994 U.S. divisional and station climatic data and normals [Compact Disc]. NCDC, Asheville North Carolina, USA.
NPS (National Park Service) (accessed Dec. 1996). NPFlora [database]. National Park Service. ice.ucdavis.edu/nps.
Prendergast, H. D. V. 1989 Geographical distribution of C4 acid decarboxylation types and associated structural variants in native Australian C4 grasses (Poaceae). Australian Journal of Botany 37: 253–273.[CrossRef]
Sage, R. F., M. Li, and R. K. Monson. 1999 The taxonomic distribution of C4 photosynthesis. In R. F. Sage, and R. K. Monson [ed.], C4 plant biology, 551–584. Academic Press, San Diego, California, USA.
Sokal, R. R., and F. J. Rohlf. 1995 Biometry. W. H. Freeman, New York, New York, USA.
Teeri, J. A., and L. G. Stowe. 1976 Climatic patterns and the distribution of C4 grasses in North America. Oecologia 23: 1–12.
Vogel, J. C., A. Fuls, and R. P. Ellis. 1978 The geographical distribution of kranz grasses in South Africa. South African Journal of Science 74: 209–215.[ISI]
Watson, L., and M. J. Dallwitz. 1999 Grass genera of the world: descriptions, illustrations, identification, and information retrieval; including synonyms, morphology, anatomy, physiology, phytochemistry, cytology, classification, pathogens, world and local distribution, and references. biodiversity.uno.edu/delta [accessed Dec. 1999].
WICPSU (Wisconsin Cooperative Park Studies Unit) (accessed Nov. 1996). Floras of midwestern national parks [database]. WICPSU. www.emtc.nbs.gov/wicpsu.html.
Willis, J. C., and H. K. Airy Shaw. 1966 A dictionary of the flowering plants and ferns. Cambridge University, Cambridge, UK.
Zuloaga, F. O. 1987 Systematics of new world species of Panicum (Poaceae: Paniceae). In T. R. Soderstrom, K. W. Hilu, C. S. Campbell, and M. E. Barkworth [eds.], Grass systematics and evolution, 287–306. Smithsonian Institute, Washington, D.C., USA.
This article has been cited by other articles:
|
|
 |
|
  O. Ghannoum C4 Photosynthesis and Water Stress Ann. Bot., June 13, 2008; (2008) mcn093v1. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B. S. Ripley, M. E. Gilbert, D. G. Ibrahim, and C. P. Osborne Drought constraints on C4 photosynthesis: stomatal and metabolic limitations in C3 and C4 subspecies of Alloteropsis semialata J. Exp. Bot., April 1, 2007; 58(6): 1351 - 1363. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
