Analysis of interspecific variation in plant growth responses to nitrogen

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  • Analysis of interspecific variation in plant growthresponses to nitrogen

    Daniel R. Taub

    Abstract: Plant species differ greatly in their growth responses to nutrients, but little is known about the physiologicaland morphological factors that are responsible for this variation. To address this question, I measured the responses toadded nitrogen of relative growth rate and three of its components (specific leaf area, unit leaf rate, and leaf weight ra-tio) for 17 C3 grass species. Plants were grown in sand culture in a greenhouse and were fertilized daily with either 5or 0.05 mM NH4NO3. For most species, growth response to nitrogen was primarily associated with an increased massallocation to leaves at high versus low nitrogen. Across all species, the average response at high versus low nitrogenwas a 37% increase in leaf weight ratio, a 12% increase in unit leaf rate, and a 4% decrease in specific leaf area.Interspecific differences in growth response to nitrogen, however, were associated primarily with species differences inthe response of unit leaf area to nitrogen supply. I determined the nitrogen response ratio of each parameter as thevalue of the parameter at high nitrogen divided by the value at low nitrogen. The rank-order correlation between theunit leaf area response ratio and the relative growth rate response ratio was 0.88. Reanalysis of previous experimentson plant nutrient response showed a similar pattern. In all studies, interspecific variation in the response of relativegrowth rate to nutrients was associated primarily with interspecific differences in the plastic response of unit leaf area.

    Key words: leaf weight ratio, net assimilation rate, plant growth analysis, relative growth rate, specific leaf area, unitleaf rate.

    Rsum: Les espces vgtales ragissent trs diffremment aux nutriments, mais on sait peu de choses sur les fac-teurs morphologiques et physiologiques responsables de ces variations. Pour aborder cette question, lauteur mesurles ractions laddition dazote, au niveau du taux relatif de croissance et de trois de ses composantes (surface fo-liaire spcifique, taux foliaire unitaire et rapport du poids foliaire) chez 17 espces de gramines en C3. Il a cultiv cesplantes en serre dans du sable avec fertilisation quotidienne, en utilisant du NH4NO3 5 mM ou 0,05 mM. Chez la plu-part des espces, la raction de croissance lazote est surtout associe avec une augmentation de lallocation demasse dans les feuilles, avec lazote lev vs lazote faible. Chez toutes les espces, la raction moyenne envers lazotelev versus lazote faible se traduit par une augmentation de 37% dans le rapport du poids foliaire, de 12% dans letaux foliaire unitaire et par une diminution de 4% de la surface foliaire spcifique. Cependant, les diffrences intersp-cifiques dans la raction de croissance lazote sont associes surtout avec des diffrences spcifiques dans la ractionau niveau de la surface foliaire unitaire par rapport lapport en azote. Lauteur a dtermin le rapport de la raction lazote pour chaque paramtre comme la valeur du paramtre avec lazote lev divis par la valeur avec lazote faible.La corrlation par ordination entre le rapport de la raction de la surface foliaire unitaire et la raction du taux decroissance relative est de 0,88. Un rexamen dexprience prcdentes sur les ractions nutritionnelles montre un patronsimilaire. Dans toutes les tudes, la variation interspcifique en raction au taux relatif de croissance envers les nutri-ments est associe surtout avec les diffrences interspcifiques dans la raction plastique de la surface foliaire unitaire.

    Mots cls: rapport de poids foliaire, taux net dassimilation, analyse de la croissance foliaire, taux relatif de croissance,surface foliaire spcifique, taux dunit foliaire.

    [Traduit par la Rdaction] 41TaubIntroduction

    Plant species differ greatly in their growth responses to nu-trients, particularly nitrogen. In one well-known study, Shipleyand Keddy (1988) examined the growth of 28 species of plants

    fertilized with full-strength and 1/10 strength Hoaglands solu-tion. Growth response to nutrient supply varied greatly amongspecies. Relative growth rate (RGR) (change in plant weightper plant weight per time) increased in the high-nutrient treat-ment by 11% for the least and 850% for the most responsivespecies. Many other studies have also shown substantialinterspecific differences in the degree to which growth is stim-ulated by nutrients (e.g., Bradshaw et al. 1964; Fichtner andSchulze 1992; Meziane and Shipley 1999).

    Such interspecific differences in growth response to nutri-ents are likely to be an important determinant of species dis-tribution across natural fertility gradients. An ability torespond to added nutrients with increased growth is often the-orized to be an important component of success in fertile en-

    Can. J. Bot.80: 3441 (2002) DOI: 10.1139/B01-134 2002 NRC Canada

    34

    Received 13 July 2001. Published on the NRC ResearchPress Web site at http://canjbot.nrc.ca on 30 January 2002.

    D.R. Taub.1 Department of Ecology and Evolution, StateUniversity of New York, Stony Brook, NY 11794, U.S.A.

    1Present address: Department of Biology, SouthwesternUniversity, P.O. Box 770, Georgetown, TX 78627, U.S.A.(email: taubd@southwestern.edu).

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  • vironments. Species that occur naturally in highly fertileenvironments typically have a larger growth response to nutri-ents than species found in less fertile habitats (Chapin 1980;Fichtner and Schulze 1992; Schulze and Chapin 1987). Inspite of the potential ecological importance of interspecificvariation in growth responses to nutrients, relatively few stud-ies have explored the morphological or physiological differ-ences among species that underlie this variation. Mostinterspecific analyses of the morphological or physiologicalcorrelates of growth rate have compared a group of species atonly one level of nutrient supply, typically at levels intendedto maximize plant growth (Grime and Hunt 1975; Hunt et al.1993; Lambers and Poorter 1992). These previous studieshave generated insights into species differences in growthrates in nutrient-rich conditions, often through use of the tech-niques of plant growth analysis (Hunt 1990). The most com-mon method decomposes RGR into three factors: unit leafrate (ULR) (synonymous with net assimilation rate, rate ofdry weight increase per leaf area), specific leaf area (SLA)(leaf area per leaf mass), and leaf weight ratio (LWR) (leafweight per total weight):

    [1] RGR = ULR SLA LWR

    Under conditions that allow near-maximum growth rates,interspecific differences in RGR among herbaceous plantspecies are usually associated with differences in SLA, withinterspecific variation in LWR and ULR playing a much lessimportant role (Lambers and Dijkstra 1987; Poorter 1990;Poorter and van der Werf 1998). For woody species,interspecific variation in RGR is also usually associated withSLA and is additionally correlated with LWR in some stud-ies (e.g., Cornelissen et al. 1998) but not in others (e.g.,Huante et al. 1995a).

    While these studies have generated insight into speciesdifferences in growth under nutrient-rich conditions, theyhave not examined interspecific differences in the degree towhich growth is stimulated by nutrients. Insight into suchplastic responses to nutrients may be gained by a simple ex-tension of the standard growth analysis techniques. There-sponse of growth to an environmental variable such asnutrient supply can be decomposed into several components:

    [2]RGRRGR

    ULRULR

    SLASLA

    LWRLWR

    1

    2

    1

    2

    1

    2

    1

    2

    =

    where the subscripts represent different environmental con-ditions (in the present case, nutrient supply). Equation 2states that the response of growth to a change in nutrientsupply (or other environmental variation) is the product ofthe responses of ULR, SLA, and LWR to the changed nutri-ent supply. This approach allows us to consider the relativeimportance of plastic response in these factors in determin-ing growth response to nutrients. This approach does not ap-pear to have been used previously, although Bunce (1997)used a very similar analysis to examine plant growth re-sponses to atmospheric CO2.

    To apply this approach to the examination of growth re-sponses to nitrogen, I measured RGR, ULR, SLA, and LWRfor 17 C3 grass species grown in a greenhouse at two levelsof nitrogen supply. These species included some that aretypically found in nutrient-poor sites (Deschampsia flexuosa,

    Festuca ovina, Poa compressa) and others that occur typi-cally on fertile soils (Elymus riparius, Glyceria grandis,Phalaris arundinacea, Phleum pratense) as well as addi-tional species that occur in habitats of intermediate fertilityor are found in sites over a wide range of fertility. In addi-tion, I applied the analysis shown in eq. 2 to previously pub-lished results by other authors to examine the generality ofthe findings of this study.

    Materials and methods

    Seeds of Agrostis gigantea, Anthoxanthum odoratum,Bromus inermis, Dactylis glomerata, Deschampsia flexuosa,Elymus virginicus, Festuca ovina, Phalaris arundinacea,Phleum pratense, and Poa compressawere collected frompopulations on Long Island, New York (specific nomencla-ture follows Gleason and Cronquist (1991)). Caryopses ofBromus kalmii, Elymus canadensis, Elymus hystrix, Elymusriparius, Elymus trachycaulus, and Glyceria grandiswereobtained commercially from Prairie Moon Nursery (Winona,Minn.) and originated from populations in Iowa, Minnesota,and Wisconsin. Seeds ofFestuca elatiorwere obtained fromthe U.S. Department of Agriculture Western Regional PlantIntroduction Station (accession No. 304844) and originatedfrom a population in New Hampshire.

    Plants were grown in the Life Sciences greenhouse at theState University of New York at Stony Brook. Seeds weregerminated in flats of sand watered with deionized water.In order to synchronize germination, planting dates foreach species varied based on prior germination tests. Seed-lings were transplanted at emergence into plastic pots con-taining 600 mL of washed sand (one plant per pot). Plantswere grown during the period 20 March 19 April 1996under natural light, with an estimated maximumphotosynthetically active photon flux density of 1150mmolphotonsm2s1. Mean daily minimum and maximum tem-peratures were 18 and 28C, respectively. Pots were wa-tered to excess daily with a modified Johnson solution(Fichtner and Schulze 1992) containing 2 mM K2PO4,1 mM CaSO4, 2 mM MgSO4, 40mM FeNa EDTA, 50mMKCl, 33 mM H3BO4, 2 mM MnSO4, 2 mM ZnSO4, 0.5mMCuSO4, and 0.5mM MoO3. The pH was adjusted to 5.8with H3PO4. Nitrogen was varied as NH4NO3 at concentra-tions of 0.05 and 5 mM. Nutrient solution was delivered viaa drip-irrigation system arranged so that lines delivering 5and 0.05 mM nitrogen solution alternated on the green-house bench (12 irrigation lines in all). Pots receiving 5and 0.05 mM nitrogen were therefore arranged in alternat-ing rows as well.

    Plants were assigned at random to nitrogen treatment, har-vest date (see below), and position on the greenhouse bench.Harvests were scheduled for days 7, 10, 13, 16, 19, and 22 af-ter emergence, although for logistical reasons, a small numberof plants were harvested at other ages (all between 7 and22 days postemergence). The original design called for fourplants per species per treatment per harvest date for a total of24 plants per species and treatment. As it became clear thatsome species would not germinate sufficiently to be includedin the experiment, their bench space was assigned to otherspecies according to the availability of emerging seedlings.

    2002 NRC Canada

    Taub 35

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  • Due to this and to mortality among plants, the number ofplants per species in a given treatment varied from 11 to 29,with a mean of 22.8. Two species (Glyceria grandisandPoacompressa) had sample sizes of less than 17 plants for at leastone of the nutrient treatments. Exclusion of these speciesfrom the analysis had little effect on the overall results, andreported data include these two species.

    At harvest, leaf blade areas were measured with anLI-3000A leaf area meter (LI-COR, Lincoln, Nebr.) andplants were dried at 70C. Dry plants were weighed in threeportions: leaf blades, roots, and other (principally the leafsheaths). Mean RGR, ULR, LWR, and SLA were derivedbetween days 7 and 22 after emergence as described byHunt (1990) and Hunt et al. (1993).

    2002 NRC Canada

    36 Can. J. Bot. Vol. 80, 2002

    0.10 0.15 0.20 0.25 0.300.05

    0.05

    0.10

    0.15

    0.20

    0.25

    0.30

    RG

    Rat

    hig

    h ni

    trog

    en (

    gg -1

    day

    -1)

    RGR at low nitrogen (g g -1day-1)

    a)

    0.15

    0.20

    0.25

    0.30

    0.35

    0.40

    0.45

    0.50

    0.55

    0.60

    0.15

    0.20

    0.25

    0.30

    0.35

    0.40

    0.45

    0.50

    0.55

    0.60

    SLA

    at h

    igh

    nitr

    ogen

    (m

    2k

    g-1 )

    SLA at low nitrogen (m2 kg-1)

    3

    4

    5

    6

    7

    8

    9

    10

    11

    12

    4 5 6 7 8 9 10 11 123

    ULR at low nitrogen (g m -2 day -1)

    ULR

    at h

    igh

    nitr

    ogen

    (g

    m -2

    day

    -1)

    c)

    0.3 0.4 0.5 0.6 0.7 0.8 0.9

    0.3

    0.4

    0.5

    0.6

    0.7

    0.8

    0.9

    LWR at low nitrogen (g g -1)

    LWR

    at h

    igh

    nitr

    ogen

    (g

    g -1

    )

    d)b)

    Df Bk

    Ev

    ErEh

    Fe Fo Ao

    PcEcEt

    BiPp

    AgGg

    Dg

    Pa

    Er

    AgBkEv

    AoPp

    Pc

    EhEc

    DgPa

    Bi

    Et Fe

    Gg Fo

    Df

    Df

    Fo Pc

    FeAo

    Bk

    Gg

    EvPp

    EtEhEc

    AgBi

    Er

    Dg Pa

    Ev Bk

    Eh ErEcFe

    Et

    DgBiPa Pp

    FoGg

    AoAg

    Pc Df

    Fig. 1. Responses of (a) RGR, (b) SLA, (c) ULR, and (d) LWR to nitrogen supply in 17 C3 grass species. Plants were grown in sand cultureat 5 mM (high) and 0.05 mM (low) nitrogen. Each point represents the mean value for one species. Letters correspond to the initials of thespecies binomials; full names are given in Table 1. The broken line across the diagonal indicates equal values in the two treatments.

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  • 2002 NRC Canada

    Taub 37

    0.10

    0.05

    0.15

    0.20

    0.25

    0.30

    3 4 5 6 7 8 9 10 12

    0.10

    0.05

    0.15

    0.20

    0.25

    0.30

    ULR (g m -2 day -1)

    b)

    Spearman r = 0.13

    11

    0.10

    0.05

    0.15

    0.20

    0.25

    0.30

    3 4 5 6 7 8 9 10 11 12

    ULR (g m -2 day -1)

    e)

    Spearman r = 0.52*

    0.3 0.4 0.5 0.6 0.7 0.8 0.9

    0.10

    0.05

    0.15

    0.20

    0.25

    0.30

    LWR (g g -1)

    Rela

    tive

    gro

    wth

    rate

    (gg

    Rela

    tive

    gro

    wth

    rate

    (gg

    Rela

    tive

    gro

    wth

    rate

    (gg

    -1-1

    -1day

    day

    day

    -1

    -1-1

    ))

    )

    c)

    Spearman r = 0.25

    0.10

    0.05

    0.15

    0.20

    0.25

    0.30

    0.3 0.4 0.5 0.6 0.7 0.8 0.9

    LWR (g g -1)

    f)

    Spearman r = 0.34

    0.10

    0.05

    0.15

    0.20

    0.25

    0.30

    SLA (m2 kg-1)

    15 20 25 30 35 40 50 55 6045

    a)

    Spearman r = 0.66 **

    Df BkEv

    ErEhFo Fe

    Ao

    Pc EcEt

    PpAg

    Bi

    GgDg

    Pa

    15 20 25 30 35 40 50 55 6045

    SLA (m2 kg-1)

    d)

    Spearman r = - 0.21

    DfBk

    EvEr

    FoFe

    EhAoPc

    Ec Et

    Ag Bi Pp

    GgDg

    Pa

    DfBk

    EvEr

    EhFe Fo Ao

    PcEc Et

    Bi

    PpAg

    DgPa

    Gg

    Bi

    Er

    Pa

    Dg

    Df GgEv

    Et

    Ec

    EhFeBk

    Fo PcPp

    Ao

    Ag

    Bi

    DfEr

    GgEv

    Pa EtEc Fe

    Bk

    Fo

    Ao

    Ag

    PpPcDg

    Bi

    DfGg

    Er

    Ev

    FeEc

    Et

    Eh

    Bk

    Eh

    FoPc

    DgAo

    Pp

    Ag

    High nitrogen Low nitrogen

    Fig. 2. Rela...

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