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Phenological Patterns of Current Season Shoots of Prosopis glandulosa var. torreyana in the Sonoran Desert of Southern California
Flora (1983) 173: 265 - 277
Phenological Patterns of Current Season Shoots of Prosopis glandulosa var. torreyana in the Sonoran Desert of Southern California 1\11. R . SHARIFI, E. T. NILSEN, R . VIRGINIA, P. W. RUNDEL and W. M. JARRELL D e partment of Ecology and Evolutionary Bio logy, Uni vc l'sity of Califomia ; Dep a l'tm ent of Soil and Environme nt a l Sc ie nce, Univc l'sity of Califomi lt
Summary P he nological studies concerning d ese r t pllmts h ave b een fe w especially In the case of phreato· phytic taxa. H e r e we r e port on a investiga tion of t h e season"l pl'ogress ion of phenologi cal cbarac· teristics on c urrent season shoots of ProsoJJi8 gtancltdo8o , a phreatophytic taxon found in t he sou thern Californi a d eserts. Growth ch a racteri sti cs a re divided into "Leaf pools" and "Flux Hates" a nd they are correlated with seasmml climatic conditions. R a t e of growth functions we l'e r a pid and of sh o l·t dumtion. T wo gl'Owth per'iods occurred with sf'veral different structur'al and phe nological ch " l'acte ri sti cs based on the clim atic conditions in which the shoots of each gl"Owth p e riod w e re produced . Maximum leaf a t'elt was maintained on the Prosopis trees throughout the most str essful p e riod o f t h e ye,u'. L ea r ab sc ission was a bmpt OCCUI " ring just b efore leaves of th e n e xt year 's g ro wth w ere pl'Oriu CE'd. Pro8opis phe nology was b est co r· r elated w ith water ava ilability a nd moisture stress. Pro8opis giancluto8a in Routhe m Califol'l1ia h its an unus ua l phen ological system in r ela tion to other d ese l't taxa which may re f! ct the ge neral phenolog y of p hl'eato phyti c taxa. Research is cont inuing on Prosopis in a compamtive m a nn er with oth er ph,'eatophytic sp ecies.
Introduction Desert environments have a diversity of life forms (SHREVE 1942), many of which have different seasonal progr essions of growth and development (TURNER 1963 ; BEATLEY 1974 ; GULMON & MOONEY 1977) . The phenological development of these taxa i s critical to their survival in the harsh desert clima tes. Although co nsiderable resear ch has been conducted on the phenology of desert annuals (BEATLEY 1974 ; MULROY & R UNDEL 1977) and shrubby perennials (MOONEY et al. 1974; HODGKINSON et al. 1978 ; SMI'£H & NOBEL 1978) , v irtually no information is available on the pheno logy of d esert trees (TURNER 1963) . This is surprising because desert trees, particularly legumes, a r e a dominant life, form in m any of t h e world's desert. P!"Osopis itself, for example, occupies 30 million hectares of the south western United States alone (PAR. KER & MARTIN 1952). The unusual ability of these d esert leguminous trees to grow rapidly is particularly interesting. The study of d esert legume growth is also interestin g in light of their potential for food , fodder; and biomass fuel production in marginal agriculture lands (FELKER 1979) . Prosopis is the most wide· spread of the desert tree legumes in North America. Or the several Prosopis sp ecies in North America P . glandulosa is the most a bund a nt.
M. R. SHAHIFI e t a l.
266
In California P . glancl'ulosa TORR. var. torreyana (L. BENS ON) McJoHN grows in dune, wa h woodland, a nd playa outwash communities as a phreatophytic ta:x,a (NILSE~ et al. 198]). The California P. glancl~tlosa was chosen for extensive research because of it!'; phreatophytic nature, its predominantly summer growth, and its potentially high productivity in natuve or agricultural st ands. This initial study of P. glanclulosa phe. nology j;o a segm ent of a r esearch proj ect concerned with Prosopis phenology, produ ctivity, wat~r relations, nitrogen fixation , and nutrient cycling. Si 1,0 De;ocription Th e resear ch site chosen for this study is Harper's Well, which is located 8 kill west of the Salton Sea at the base of the Fish Creek Mountains. The site is located on an out ll'ak h pla in at - 30 m elevation with a soil high in silt components. Average precipita tion is 70 mm/y-l typieally occurring from August to March. Summer rains are infrequent at best. Mean maximum temperature are highest, 47 °C, in July, the driest month of the year . P. glanclulosa accounts for more than 90 % of the vegetation cover, with a biomass of 14,000 k g ha - 1 and a productivity of 3,700 kg ha-1 y - l (SHARIF! ot al. 1!l81) . Only three other shrub sp ecies are present, all with less than 1 % cover, Eph emerals a re infrequent at Harper's Well.
Materials and Methods Five e. ytcmdutosa t,'ees we "e se lec t ed in H a rper 's \'Vell to r e present the diversity of g"owth fo rm s a nd indi v idu al s izes found within the stand. Three individua ls wer e of the tree gl'Owth forl11 and two indi v idu als r eprese nted the shrub gl'Owth form (SHAmFJ et a l. 1981). In early March 1980 25 to 30 n wly initi a ted bmllch es w e re c ho sen on each tree a nd p e rmanently tagged . These branches we ,,€, th e il, monito ,'ed th roug hout the yea ,' for geowth (basal di a m e t er, shoot elongation) and the follo wing ph(' no logie a l ch a .'acte ri stics. 1. 2. 3. 4.
The The The ThE'
nUllIbe ,' nun ,be,' numb(' " nlln,be ,'
o f jnveni le Leaves (lea fl e ts not full y expand ed). of mature leaves (l eafle ts full y expand ed). o f sen esce nt Leaves (le afl e ts c hlorotic, 0" a b sc issed ). o f a b sc issedl eaves.
5. ThE' Jltr11 ,b€' ,' o f C'fltE'n I('aves (25 % or m o ,'e leaf a l'ea con sum ed by insects). The nUlllbC'" o f inflo" es('e l1ces. 7. The numbs ,' o f I,'uits.
(j.
The a bove phenologi ca l ch a "tlcte ,:istics a re cins id e l'ed pools of leaves or f'e p "oductive structures. HlltC's of pLant function (flu x rates ) w e r e calc ulated by the following formuL a b ecau se the re was only on€' I('"f p e ,' n ode. Leaf produc tion = [TOT 2
+ ABS2]
-
[TOT1
+ ABS1] / T2
_ T1
Wc r€' 'I'OT1 = No. of lea vcH p" esent a,t Tim e 1 '1'0'1'2 = No. o f leaves pl'Csent at Tim e 2 ABR 1 = No , of €' mpty n od es £It Tim e 1 ABH2 = No. of e mpty nodes at Time 2 'I' 2 = Tim e 2 '1'1 = Time 1
O the r nlte fun ctions s uch as lea f a b sc ission ""te , lea f h e ,'b ivo "y rate , shoot elongation r a te, fl nd ropl'Oduet i vo 'p rod u ,tion l'ate we 'e I ' 'L' t d I h ' " "om t e Incr e m ent In a gI ven co mponent over the • Ca c u a e
Phenological Pattel'n s
267
time inter va l b e tween m easw 'eme nts. Following the initi a l Ma l'ch g l'owth flu sh a seco nd gl'owlh period occurr ed during .July a nd Augu st of 1980, DUL'ing thi s tim o fifteen newly initi ated s hoots were chosen a nd perm an e ntly t agged on each t ree bringing t h e total numbcl' of h,bc-l ed bl'an ('hes to 200. The previou sly m ention ed ph enological ch al'>tcte l'isti('s we l'e a lso monitol'cel on t hese Rumm el' produced shoots. L eaf a rea a nd specifi c leaf weight chtLl'ftct e l'i sti ('s wer-e also fo ll owed on these fi ve individu>ds. On each phenology sampling date a ll t h e leaves we l'e t ak e n :fl'om twenty shoots, pl'esRed ,in th o fi eld, and dried in a forced a ir oven at 70 °C fo '" 48 h. L efl f HI'ea m('aRUI'om('n t f< W (, ,' l1l ac\(' with th€' L T OIt leaf area m e ter (model # 1(00) a nd sp ecifi c leaf we ight was calculat(,d as mg ('m - 2 • Climati c ch a r acte l' istics of t empe l'atu T'e a nd p,'e cipitation a l'(' ,'edol'd ('d at lh e Bmw l('y LJ,R. D.A , weather st a tion, 40 km south of Harper ' s W ell. Reh\ti ve humidity and lCl11pertul'P we l'(' monito,'pel during p h enology sa m p ling at H a rper' s W ell to de t e rminc vapor' p,'e8S1]1'0 d('fi cits. Thp o ns it(' t('m· peratlll'e values w em con sistentl y 3 - 5 ° C highe. than t hosE' J'('eo l'd ed in Brawley, So il m o istw'e determinat ions w ere m a d e at - 25 c m a nd - 4.0 m b y th p u se of tho ]l<'utl'On acti vflt ion teehni q u ('. Neutron probe a ccess tubes w ere inse rte d und e rnea th eflc h o f the :fivc tl'e S Hnd betw('e 'l th e t ,'p(,., Reported soil moi sture val ves a r e a m ean o f data take n in all the a('('ess tubes. As anoth er r e lati ve indication o f ecosyst e m wa t er ava il ability to P. glandulosa p,'e· dawn xyle m PJ'Pss ul'e pote nti al (XPP) was m eascu'ed with a presslll'e ch a mber. Midday XPP was a lso monito,'('(l to ndi cat e the relative magnitude of season a l plant w a t e r s tress. A ll XPP measure m e n ts a l'e repo ,'ted as a n1('a n for five trees (N = 3 per tree).
Results Climate conditions for the region n ear Harper 's Well during 1980- 1981 are shown in figure one. T emperature increased from a minimum in January to a maximum, 43 °C, in July, The man maximum temperature stayed above 40 °C for 5 months (May to September). The lowest m ean temperature was 5 °C, and the t emperature n ever went below 0 °C, The maximum recorded temper ature at Harper's Well was 49,5 °C in July a nd the usual diurnal temperature fluctuation was about 17,5 °C. Vapor pressure d eficit has a simila r seasonal variation to that of temperature with the greatest vapor pressure d eficit (VPD) from May through August, Th e mean maximum YPD was 5,25 kPa (52,5 mbars ) which occurred in July, Also, in Jul y the diurnal VPD fluctuation was 3,5 kPa (NILSEN et al. 1981) , while in Januar y is waR only 2,0 kPa, Soil moisture was recorded at 25 cm depth incrementR from - 25 cm to - 600 cm, Here we report the average valves at - 25 cm and - 4-00 cm because theRe are th e zones of maximum root proliferation (SHARIFI et al. 1982). At a depth of 400 cm there is a constant water availability throughout the season, Th e soil moist ure at 400 cm depth (near field capacity) was much greater than a t 25 cm d epth , th erefore , there wa a constant background of available soil moisture. Surface soil moisture (- 25 cm) was below 9 % throughout the season, but maximum water availability in this rooting zone occurred from January through April during and directly after the period of maximum precipitation, Precipitation only occurred during the winter a nd spring months of 1980 and 1981. Water availability to the plants was m easured by d etermining the pre-dawn XPP, The pre· dawn XPP remained constant at about 2,5 MPa between June a nd December indicating the constant background water availability at d epth, During February
M. R.
268
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MAMJJAS O ND J FMAMJ 1980 1981
Fig. 1. Clim at iC' co ndition s during 1980 - 1981 a t HaJ'pe l" s W ell, Califo1'llia n ear the Sou t hern tip of th o Sal t on i'ka. Pl'e· d >1w n >1nd midday xylem pressure potentials are means (n = 5 trees) for J'ro801Ji8 ytnnduto8a.
through April the pre.dawn XPP inereased (- 1.5 to 1.0 MPa) indicating the plants l'e8pOllRe to increased moisture availability at the surface following precipitation. During March t he midday XPP is similar to the pre·dawn XPP indicating only minor diurnal fluctua t ion in XPP. As the growing season progressed the midday X P P became prog l'c""ivcly lower until June indicating progressively greater plant water stress. The midday X P P r emained con, tant at - 4 .5 MPa from June through late December even t hough there were :-;ignifi cant changes in temperature, day l enght, and evaporative dema nd (V JI I)). Th e HeaHon ality of growth and development of these Prosopis trees is depicted in :Fig. 2. J~ach p h enological component is represented as a mean percentage of the seasonal maximum for the five individuals. The n umber of leaves in developmental catagOl'ies are represented as " Leaf Pools". The total number of leaves pel' branch rapidly increased during early March reaching a maximum value in late March . There was a slight decrease in total leaves from April through June as a result of herbivory (discussed later). The second growth period occUl'red ft'om J'uly through August, when leaves were rapidly produced on new ter-
Phenological Pa,tterns
100
LEAF POOLS Toto I No. of Leaves e" .P-_~ __
269 FLUX RATES
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100 50 E ~ 100 E .;;; c :::!:
.
100
50
50
'0
Leof Abscission
/y\ _-d
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No. of Senescent Leaves /e-e_______..
i
50
100
)<\ ,
No. of Abscissed Leoves .-It
50
/'
1~ Growth Period
.
0--02 QQ Growth Period
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I
100 50
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• / / / . p"P
tt-- _
F M A M J J A SON D J F M 1980 1981
100 50 F M A M J J A SON D J F M 1980 1981
Fig. 2. Seasonal prog"ession of phenological events on current pL'Odu ced shoots of Prosopis giandulosc, at Harper's "VeIl Californi a, near the southern tip of the Salton Sea.
minal shoots. Leaves were also replaced on March produced shoots. Total leaf number then remained constant through January for both sets of shoots. Total leaf number decreased rapidly in January -February for first growth period leaves and in Fe bruaryMarch for the second growth period leaves. The first cohort of leaves had an eleven month life span while the July produced leaves only lasted seven months. Juvenile leaves were present in large numbers on the new shootR only for a short period of time (less than one month). The brief presence of juvenile leaves was true for both growth periods. The first growth period shoots had a secondary occurrence of juvenile leaves just before the second set of new shoots were produced. The number of mature leaves on first growth period branches rapidly reached a maximum in March, remaining constant until late August. As the secondary growth period leaves matured the leaves on first growth period shoots became senescent. The remaining mature leaves on first growth period shoots in September were those produced in JUly. The senescent first growth period leavefl remained on the branches for more than six months (August-January). On the other hand , senescent second growth period leaves were on the branches for only 3-4 months . The senescent leaves began
M. R..
270
SUARIF]
et a l.
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80
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~
(0) Shoot Length (e ) Shoot Basal Diam eter
20
F
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1980 Icig. 3. HpllHo n a l pI'ogl'cHsiol1 o f shoot length a nd b asal diameter in crement for current p"oduced shools o f I'rosopis ylandtt!osCi at Harper's W ell CRliforni a , neal' the southe rn tip of the SaLton Sea. Value'S ,"'(' >t l11 ('a 'l fo,' fi ve t r'ees.
to abscise in July-Augu st but the number of abscised leaves did not significantly incrcasc until January- March. The seaso.n ality of pl ant activity is r epresented as five " Flux Rate" panels in Fig, 2. Lcaf production rates were maximum for very short periods of time which indicate that distinct cohorts of leaves are produced on these individuals p , glandulosa. Shoots produ ced in Mar ch h ad a seconda ry cohort of leaves in August equaling the first coh ort in numbcr . JUly produced branches had only one cohort ofleaves. Shoot elon. O'ation rates were also rapid for short periods of time and there was no secondary elongation period on first growth period shoots. The lack of a secondary shoot elonga· tion period indi cates that the second growth period leaves on the first growth period shootH were located in old nodes, resulting in several nodes with more than one leaf. The leaf abscission rate was maximum in January and February for the first and second growth period leaves respectively. Leaf a bscission seemed to be synchronous within a bran ch similar to that of leaf production. The rate of leaf herbivory was maximum during periods of high leaf production, which coincided with the maximum number of juvenile leave. , Flower and pod production the first cohort in numbers . July pro. duced branches had only one cohort of leaves. Shoot elongation rates were also rapid for short period" of ti me a nd there was no secondary elongation period on first growth period Ahoots. The lack of a secondar y shoot elongation period indicates that the Hecond growt h period leaves on the first growth p eriod shoots were located in old nodes, r esulting .in several nodes with more than one leaf. The leaf abscission rate was maximum in J'a nuary and F ebruar y for the first and second growth period leaves respectively. Lcaf absciss ion seemed to b e synchronous within a branch similar to that of leaf production. The rate of leaf h erbivory was maximum during periods of high leaf production, which coincided with the m a ximum number of juvenile leaves. Flower and pod production rates occurred in a bimodal fa shion, April- May and again in June to
271
Phe nologi ca l P"lto l'n s
Table 1. Seasonal maximum valu es of ph e n ological cl ll:tI'acrorist ics for fiv o P l'Osopis glwullllo (I trees on shoots produced during two growt h p e riod s of 1980- 198 1. (X = moan, SX standa['d dov iation) '1'[,00
#
1
2
3
4
5
X
HX
12.4 16.7 0.5 1.7 0.9 0.7 1.5
11. 6 22.9 0.5 1.5 0.4 1.0 2.3
11 .7 2 1. 0 0.7 1. 8 0.5 1.1 1.:'1
1:3.7 20.3 0.1 1. 9 0. 8 1.0 0.9
11.0 35.9 O. 1. 8 0.6 1.0 3.4
12.9 23.4 0.5 1.8 0.6 1.0 1.8
1.5 7.4
7. 2 21.4 0.0 2.6 0.5 1.2 3.9
8.4 18.0 0.0 1. 4 0.4 0.5 0.7
lO. 2 33.5 0.0 1.9 0.5 0.9 2.7
12.7 26. 9 0.0 2.:3 0.4 0.5 1.7
8.0 29.4 0.0 1.8 0.3 0.5 9.5
9.3 25.8 0.0 2.0 0.4 0.7 3.7
2.2 6.2 0 .0 0.6 0.1 0.3 3.4
1st Growth P oriod (Februa ry - November) No . of leaves pel' s hoot Shoot le ngth (cm) No. of Pods per shoo t L eaf produotion (No. wk - 1 ) L eaf abscission (No . ",k - 1 ) L eaf herbivory (No. wk - 1 ) Shoot elongation (cm wk - 1 )
O . :~
0.3 0.2 0.1 1.0
2nd Growth P eriod (.July-D ece mber) No . of leaves per sh oot Shoot length (cm) No. of Pods p e r sh oot L eaf production (No. wk - 1 ) L eaf abscission (No. wk - 1 ) L eaf herbi vor y (No. ",1;: - 1 ) Shoot elongat ion (om wk - 1 )
August. Both pulses of reproductive activity occurred during the interim period be· tween the two p eriods of rapid leaf production a nd shoot elongation. No flowers or pods were produced on the second growth p eriod shoots. The two shoot growth functions, that of shoot elongation and diameter increment, 4ad varying season al progressions. Shoot elongation during the first growth period occurred within 4- 6 weeks (Fig. 3) , in contrast to cambial activity (diameter increment) which continued from March through November. Therefore these curre nt shoots elongate and produce leaves rapidly and later increase in diameter a nd weight. The actual mean values representing the m aximum values in Fig. 2 are reported in Table 1 for each individual. The highest variability found between trees for an y ph eno. logical component was that of shoot elongation in which the standard deviation was 55 % and 92 % of the rates occurred in a bimodal fashion, April- May and aga in in June-August. Both pulses ofreproductive activity occurred during the interim p eriod between the two periods of rapid leaf production and s hoot elongation. No f1 0werR or pods were produced on the seco nd growth p eriod shoots. The two shoot growth function s, that of shoot elongation and diameter increme nt, had varying seasonal progressions. Shoot elongation during the first growth p eriod occurred within 4- 6 week s (Fig . ~) , in contrast to cambial acitvity (diameter incre· ment) which continued from March through November . Therefore these currcnt sh oots elongate and produce leaves rapidly and later increase in diameter and weight . The actual m ean values representing the maximum values in Fig. 2 arc reported in Table 1 for each individual. The high est varia bility found betwecn trees for a n y phe.
M. R .
272
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Fig . 4. Season a l prog l'esHion of l eaf a l'e a p er leaf, leaf a r ea p el' shoot and specific leaf weight for CtH ,'c nt pl'oduced s hoots of Pro.sop is glandttlosa a t HarpeJ." s 'N e ll California n eal' the southern tip of th o Salton Flea. V alu es ,'cpor:te d a ,'e " m ean for five tl'ees du:[,ing two growth periods.
nological component was that of shoot elongation in which the standard deviation was 55 and 92 % of thc mean for the first and second growth periods respectively. The standard deviations of all other phenology component means combined averaged only 2 % of the mean. Th erefore , except for shoot elongation, there was only moderate v ariability betwee n trees for any phenological component in our samples (n = 5). Th ere were, ignificant differences between phenological charaeter maxima of the tw g t'Owth p eriods. Maximum pla nt activity rates (flux rates) of the second growth pe riod wer e hi gbcr than that of the first growth period (Table 1) except for leaf abscisNioll. Shoot lenO'ti1 s of both growth p eriods were similar although the number of leaves pel' shoot wai-llarger for the first growth period. Therefore , the internodal length of the second growth period (2.77 cm) was larger than that of the first growth period (1.82 cm). Very few reproductive Rtructures were produced during the first growing season and none of these on second growth p eriod shoots. Most fruits are produced on branches which arc two y ears old or older . Maximum leaf herbivory rates were high in relation to maximum leaf production rate" indicating that a large proportion ofleaves were conKumed by herbivorcK. Diffcren ces of climatic conditions and phenological maxima between the two growth period ;; have signifi cant influences on leaf area characteristics. F ig. 4 represents the
273
Phenological Pa ttel' ns
'fable 2. Correla tion between climatic conditions (1980- 1981) a nd phenological ch aractcristics of P.rosop~s glandulosa at H arper 's Well, in southern California Temperature Max
Min
V apor
X i lc m Press ure Potential Pressure Soil Moisturo D efi cit - 25 cm - 400 c m I're-dawll Midday
PhoLopcriod
Total number of leaves
.10
.05
.02
.20
.02
.05
.09
.03
Number of juvenile leav es
.03
.02
.01
.00
.30**
.25
.19
.00
Number of m a tlll'e leav es
.25
.24
Al **
.46**
.27
.00
.19
.55* *
Number of senescent leaves
.01
.00
.08
.07
.71**
.23
.13
.14
Number of abscissed leav es
.26
.16
.27
.30**
.00
.12
.23
.25
R ate of shoot elongation
.17
.15
. 14
.33**
.42**
.57**
.62**
.03
R at e of leaf production
.01
.00
.08
.00
.01
.07
.17
.01
R ate of leaf abscission
.06
.07
.13
.25
.46**
.07
.03
.24
R at e of leaf h erbivory
.00
.01
.01
.03
.06
.06
.12
.01
R at e of reproductive prod uction
.19
.19
.32**
.11
.06
.01
.04
.34**
(**p
~
.01)
leaf area characteristics for both growth periods. Specific leaf weight increased rapidly to a maximum in late March in close association with leaf maturation. The Rpccifi c leaf weight of leaves produced during the second growth period was lowcr than that of the first growth period. The increase in leaf area per leaf was also closely associated with leaf maturation but second growth period leaves were much smaller than firHt growth period leaves. The suddden decrease in leaf area per leaf and per shoot during August is the result of new leaves produced during August (with second growth period area characteristics) on first growth period shoots. The leaf area per shoot is a product of leaf number per shoot and leaf area per leaf. As a result the sccond growth period shoots had a proportionally smaller leaf area per shoot in relation to the first growth period than a similar comparison made for leaf area per leaf. Both leaf area value and specific leaf weight reflect senescence by their decline during November through February. Leaf area decreases as a result of leaflet abscission and leaf abscission on a leaf basis and a shoot basis respectively. Specific leaf weight decreases during senescence as a result of mobile solute re-translocation into the stems. Correlations were made between the climatic parameters and the phenological components (Table 2). The only significant correlations were found between water relations components and phenological events. Shoot elongaton rates and leaf abscission rates
27+
M. R .
S HAIUF [
e t " I.
Ree m to be well associated with surface soil moisture although shoot elongation rates Ree rn bm;t l1HRoc iated with p lant water stress relationships. Senescent leaves also seem be~t assoc iatod with surface :'io.il moisture. The mature leaf pool seems to be well associated with V I'D, soil moisture at d epth, and photoperiod. Associations with VPD and ph otoperiod are hard to Heparate since they are highly intercorrelated (R2 = .90). All ther Heaso nal progressions of phenological characteristics are poorly correlated with the proO" r'osH ion of climati c conditions at Harper 's Well . Discu ssion Th o 'Jimatic co nditions at Harper 's W ell suggest several strong environmental streKRes to which the Prosopis trees are exposed. First , there was a high heat load stress during the s ummel" monthA. Secondly, in accordance with the high temperatures, the V P D waf) hig h particularly during the summer. Thirdly, soil moisture in the upper soil levels was always low (below 9 %) again, particularly during the summer. The low surface Hoil moi f)ture was cleady associated with the v ery low annual rainfall. Therefore, water. tresH in surface soils and heat stress conditions were extreme during the summer month s. These summer temperatures are considerably higher than the temperature optima for photosynthesis in many desert plants (BJORKMAN 1980). The midday XPP ex perienccd by the -e Prosopis trees was lower than the experienced by other desert phrcatop hytes (STRAIN 1970 ; SZAREK & WOODHOUSE 1978). The ai'-nual rainfall for t hi s I:> ite during 1980- 1981 and on a 30 year average basis (65 mm) is in the lower range for most warm desert sites in North America (EHLERINGER & MOONEY 1981). Th eHe Hevore environmental stresses should be strong selective pressure for water f:)tresH a nd heat stress ada ptation in Prosopis as is found in other desert plants. Ma ny desert plants have evolved a daptive phenologies in response to the extreme deHert cli ma teo Some of these a daptive phenologies are manifest ed in short lived winter a nnual;; (M L1WY & R UNDEL 1977) , perennial summer deciduous shrubs (MOONEY 19 0) or p el.'renial evergreen s hrubs with seasonal variability in leaf characteristics (MOON.EY et al. 1974- ; SMl'.r.H & NOBEL 1978). The phenology of Prosopis is quite different tha t t hat of other desert sp ecies. Prosopis maintains maximum leaf area througho ut t he ITI Oflt stressful period of the year. Also, there is a pulse of growth during the h ottest a nd dryest month of the year. Both of these growth characteristics would seem to be maladaptive for sp ecies growing in this summer dry climate. The phonology of current season s hoots in Prosopis is also characterized by rapid growth characteristics over s hort duration. This is true for leaf production, shoot elongation and leaf abscission but not for eambial growth. This occurred during both growth periods. The short duration of leaf production and the rapid leaf maturation result in s hort periods when juvenile l eaves are present on the branches. This may be a n adaptation against herbivores since leaf herbivory was highly associated with the presence of juvenile leaves. Durino- 1980- 1981 there were two growth periods for Prosopis at Harper's Well eac h of which occurred during very different climatic conditions. The first growth
P h enol ogica l P 'tttems
275
period in Marc h occurred during low tempera tures (max = 20 °0) , low VPD (2 kPa) a nd high surface soil moixture (9 % ). The second growth period occurred during high temperatures (max = 45 °C) , high VPD (5 .3 kPa) and low surface soil moisture (5 %). As result of the high July water stress conditions the second growth period leaves were smaller, each branch had fewer leaves, and each branch had a sma ller leaf area. Also, it seemed that the higher t emperatures during the second growth period caused more rapid elongation rates over a shorter duration. Although the second growth period leaves were produced four monthf! after the first growth period leaves, abscission occurred almost simultaneously for leaves of both growth periods. Abscission events were abrupt, just as were leaf production events, a nd abscission seemed to be stimulated by increased surface soil moisture in February. This is suggested by the first growth period senescent leaves, which remained on the trees until late January when they began rapidly abscising a t a , imilar time as the abscission of the second growth period leaves. Associations between climatie conditions and phenological events were minimal. The phenology of current shoots seems best associated with various water relations characteristics particularly shoot elongation and leaf abscission. T~eaf production and leaf herbivory were not correlated with any climatic factor but they were well correlated with each other. The poor associations between climatic events and leaf production is the result of the short duration of leaf production following a stimulus . Also there is often a lag between the climatic stimulus and the phenological response (NILSEN & M ULLER 1980) . Therefore correlations b etween climate and phenology can only be used to suggest relationships and such correlations are prone to missing actual stimulusr esponse associations. There were several phenological events which seemed to b e well associated with each other. Two of these. leaf production and reproductive production, su ggest that there is an endogenou s sequence of growth. That is, leaves are produced, following which all energy is placed into flower and pod production. Following pod drop leaf production is once again initiated even though climatic stress is severe during the second p eriod of leaf production. The initial season al growth in F ebruary a nd March seems to be stimulated b y a climatic factor following which an endogenous growth sequence prevails. There are other suggestion of endogenous system controlling growth in tropical plants (BORCHERT 1978) . Prosopis may be used as an example elucidating the gen eral phenological system of a phreatophytic species. Growth occurs in rapid spurts of s hort duration initially in response to some climatic parameter , which is likely water relations. Following the initiation of growth an internal endogenous sequen ce seem s to directgrowth. Pt'osopis phenology also suggest that phrea tophyties are able to maintain large leaf areas throughout the stressful desert summers, in contrast to other desert taxa with small leaf area or short duration leaves (SMITH & NOBEL 1978). This unusual phreatophytic phenology can only be maintained by ample water resources at d epth. The rapid a nd short duration of growth may be an adaptation against strong herbivory pressure on n ewly produced leaves.
M. H,. SHARIF! et a!.
276
Continued invQf;tigations of the ph enologieal patterns of legumes are of critical importance in understanding the adaptions of these taxa to desert environments. Such invoRtigati.onfl aro a lso important to interface with studies of legume physiological eco logy a nd population biology. Sympatric phreatophytie taxa may have a differing phenological patterns (TUl~NE1~ 1963) with a different adaptive significance. For this rea on we are continuing research on the phenology of several phreatophytic taxa in a n atural eommon garden. Also, the temporally separated production of P1'osopisleaf co hortR iR being tudied through life table population biology analysis (HARPER & W IIIT.m '1974) . In addition, a comprehensive study of older Prosopis branch phenology haR b een initiated .
Acknowledgements 'l"hiH "C'Hl1>L.'ch
WllS
s UPPol'ted by t h e National Science Founda tion grant number DEB 79-21971.
References ,I. C. (1974): Ph enolog ical event s and their en vironmenta l triggers in Mojave Desert ('C'OSYHtP III K. 'I ~co i ogy 55: 85fl - 8 C13. BOltCII"It'I', H. (197R): F t>E'dbfl(;k control and flge r elated ch anges of shoot growth in seasonal and non'KPHHonH i c'iin mtes. In: TOMLINSON, P. B., & ZJMMERMANN, M. H. (eds.), Tropical Trees as Living HYKtel11s. Cambl·jdge U ni ve l'sity Press, Cambridge, M assachusetts, pp. 497 - 515. BJOltl(MAN, 0., BADGE R, M. H,., & AHMOND, P. A. (1980): H,esponse and adaptation of photosynthcHiH to high t empe .'atlu'e. In: T UHNllH, N. C., & KUAMER, P. J. (eds.), Ada ptation of Plants to W"tc' .' "nd Hig h Te mpe.l'atul.'e Stress. WiLey-Interscien ce, N e w York, pp. 233 - 249. IBIiLICltl NG" It, ,I ., & MOON" ' -, H. A. (1983): Photosynthesis and productivity of desert and mediterl'lll1l'llll-e iim flto pla nts. Encye iopedia of Plant Physiology 120 . Springer, N ew York-Heidelberg· BC' riin. F.I'LK ICIt, 1'. (1979) : Mesquite : an an purpose leguminous arid la nd tree_ In: Rrl.'CHIE, G. A. (ed.), NC'w Ag ,'ieultuL'll1 C,·o ps. AAAS, W estview PJ'ess. Boulder, Colorado. GULMO N, H. L., & MOONJ~Y, H. A. (1977): Spatial and t e mpo.'a lrelationships between two desert s hl.' ubs, A t1'ip lex hyrnenelytm Hnd TJ.'idest1·ornia oblongifolia in D ea th V alley, California. J. E ra!. 65: 831 - 8 38 . .H.A lt l'mt, ,I. L. , & WHI 'I'Il, .1 . (1974): The d e l'llogmphy of plants . Ann_ R ev. of E col. and System 5: 419 - 4(;3.
B'M'I'LIW,
HODOK' NSON, K. C.. JOII NSON, P. S., & NOltTON, B. E. (1978): Influen ce on summer rainfall on I'oot and "hoot g l'ow th of a eold winter d esert 8hmb Atriplex conjertijolia. Oecologia 34: 353 - 3(;2. MOONE ", I-l. A. (1980): SeflsonaJity and gradients in the study of stress a d a ptation. In: TultNlm, N. C. , & KItAMEH, P. J. (eds.), Ad a pta tions of Plants to W a t e r find High T emperature Stress. Wii cy- lnte l'sden ce, N ew York. BJO ltKMAN, 0 ., & 'J'.ltO UGllTON, .J. (1974): Seasonal changes in the leaf ch aracteristics of the clesPl't shl'ub At1'iplex hymenelytm. Carnegie Ins t. Yr. Book 73: 84C1-852. MULltO'{, '1'_ W., & H,UNDEL, P. \-V. (1977): Annual pla nts: adaptions to desert environments. Bioscie .wC' 27: 109 - 114. N ILSEN, E. '1'_, & MULLJm,W. H. (1980): An evalu a tion of summ er d eciduousness inLotu88copariu8 NUTT. in T . & G. ArneI'. Mid. N a t. 103: 88 - 95. RIJND IU", P. W., & flHAltlFJ, M. R. (19 81): Summer wa ter r el a tions of the d esert phreatophytie Prospis alandulosa in the Sononlll D esert of southern California . Oecologia 50: 217 - 224.
Phe nological Patte m s
277
PARKJ<~R, IC "V., & MARTIN, S. C_ (1952): The m esquite pl'Obl e m on soutl1el'll Al'izona range. USDA
Circular 968: 70. SHAnn'], M . R., NlLSEN, E. '1'., & gUNDEL, P. 'vV. (1982): Biom ass a nd ne t prim ary production of Prosopis glcmdulose, (Fabaceae) in the SOIlOI'un d esert of Califomi a. Am er. J. Bot. 69 (5): 760 - 767. SHREVE, F. (1942): The d ese rt vegetat ion of North Am eri ca. Bota ni cal R evie w 8: 195 - 246. SMITH, vV. IC, & NOBEL, P. S . (1978): Influ e nce of il'l'>ldiation, soil wa te l' potenti al, and leaf temperatur'e on lea f morphology of a d ese r t bl'oadle"f Encelia farinosa GUAY (Compositae). Am er. J. Bot. 65: 429 - 432. STR,II N, B. R_ (1970): Fi eld measure m e nts of ti s~u e wate l' pote ntia l ,tnd ca l'bon dioxid e xchange in the d esert shrubs P1'080pis jUliflom and Lrt1'1'6(f, divCI1'icata. Photosyn thetic" 4: 11 8 - 122. SZARl~K, S. P., & WOODHOUSE , R. M. (1978): E co phys iological ~ tudi es of SonOl'an d esel't pla nts. III. Daily course of photosynthes is for Acacia gr'eggi'i " nd Gercidium micfophyllum. Oecologi a 35 : 285 - 294. TURNER, g . M. (1963 ): Growth in fOU l' s p ecies of Sonol'ttn deser·t trees. E cology 44: 760 - 765. Received April 20, 1982 Authors' a ddresses : M. R. SHAR[FI, E . T. NILSEN, a nd P. W. R UNDEL, De partm ent of E cology and Evolutionary Biology, University of California, Ir'vin CA 92717; l~. VIRGINJA a nd W. M. J.umELL, D e pal·tm ent of Soil a nd Environm ental Science, Unive r'sity o f California, Rive r sid e CA 92521.
H :FJora, Ed. 173
Phenological Patterns of Current Season Shoots of Prosopis glandulosa var. torreyana in the Sonoran Desert of Southern California 1\11. R . SHARIFI, E. T. NILSEN, R . VIRGINIA, P. W. RUNDEL and W. M. JARRELL D e partment of Ecology and Evolutionary Bio logy, Uni vc l'sity of Califomia ; Dep a l'tm ent of Soil and Environme nt a l Sc ie nce, Univc l'sity of Califomi lt
Summary P he nological studies concerning d ese r t pllmts h ave b een fe w especially In the case of phreato· phytic taxa. H e r e we r e port on a investiga tion of t h e season"l pl'ogress ion of phenologi cal cbarac· teristics on c urrent season shoots of ProsoJJi8 gtancltdo8o , a phreatophytic taxon found in t he sou thern Californi a d eserts. Growth ch a racteri sti cs a re divided into "Leaf pools" and "Flux Hates" a nd they are correlated with seasmml climatic conditions. R a t e of growth functions we l'e r a pid and of sh o l·t dumtion. T wo gl'Owth per'iods occurred with sf'veral different structur'al and phe nological ch " l'acte ri sti cs based on the clim atic conditions in which the shoots of each gl"Owth p e riod w e re produced . Maximum leaf a t'elt was maintained on the Prosopis trees throughout the most str essful p e riod o f t h e ye,u'. L ea r ab sc ission was a bmpt OCCUI " ring just b efore leaves of th e n e xt year 's g ro wth w ere pl'Oriu CE'd. Pro8opis phe nology was b est co r· r elated w ith water ava ilability a nd moisture stress. Pro8opis giancluto8a in Routhe m Califol'l1ia h its an unus ua l phen ological system in r ela tion to other d ese l't taxa which may re f! ct the ge neral phenolog y of p hl'eato phyti c taxa. Research is cont inuing on Prosopis in a compamtive m a nn er with oth er ph,'eatophytic sp ecies.
Introduction Desert environments have a diversity of life forms (SHREVE 1942), many of which have different seasonal progr essions of growth and development (TURNER 1963 ; BEATLEY 1974 ; GULMON & MOONEY 1977) . The phenological development of these taxa i s critical to their survival in the harsh desert clima tes. Although co nsiderable resear ch has been conducted on the phenology of desert annuals (BEATLEY 1974 ; MULROY & R UNDEL 1977) and shrubby perennials (MOONEY et al. 1974; HODGKINSON et al. 1978 ; SMI'£H & NOBEL 1978) , v irtually no information is available on the pheno logy of d esert trees (TURNER 1963) . This is surprising because desert trees, particularly legumes, a r e a dominant life, form in m any of t h e world's desert. P!"Osopis itself, for example, occupies 30 million hectares of the south western United States alone (PAR. KER & MARTIN 1952). The unusual ability of these d esert leguminous trees to grow rapidly is particularly interesting. The study of d esert legume growth is also interestin g in light of their potential for food , fodder; and biomass fuel production in marginal agriculture lands (FELKER 1979) . Prosopis is the most wide· spread of the desert tree legumes in North America. Or the several Prosopis sp ecies in North America P . glandulosa is the most a bund a nt.
M. R. SHAHIFI e t a l.
266
In California P . glancl'ulosa TORR. var. torreyana (L. BENS ON) McJoHN grows in dune, wa h woodland, a nd playa outwash communities as a phreatophytic ta:x,a (NILSE~ et al. 198]). The California P. glancl~tlosa was chosen for extensive research because of it!'; phreatophytic nature, its predominantly summer growth, and its potentially high productivity in natuve or agricultural st ands. This initial study of P. glanclulosa phe. nology j;o a segm ent of a r esearch proj ect concerned with Prosopis phenology, produ ctivity, wat~r relations, nitrogen fixation , and nutrient cycling. Si 1,0 De;ocription Th e resear ch site chosen for this study is Harper's Well, which is located 8 kill west of the Salton Sea at the base of the Fish Creek Mountains. The site is located on an out ll'ak h pla in at - 30 m elevation with a soil high in silt components. Average precipita tion is 70 mm/y-l typieally occurring from August to March. Summer rains are infrequent at best. Mean maximum temperature are highest, 47 °C, in July, the driest month of the year . P. glanclulosa accounts for more than 90 % of the vegetation cover, with a biomass of 14,000 k g ha - 1 and a productivity of 3,700 kg ha-1 y - l (SHARIF! ot al. 1!l81) . Only three other shrub sp ecies are present, all with less than 1 % cover, Eph emerals a re infrequent at Harper's Well.
Materials and Methods Five e. ytcmdutosa t,'ees we "e se lec t ed in H a rper 's \'Vell to r e present the diversity of g"owth fo rm s a nd indi v idu al s izes found within the stand. Three individua ls wer e of the tree gl'Owth forl11 and two indi v idu als r eprese nted the shrub gl'Owth form (SHAmFJ et a l. 1981). In early March 1980 25 to 30 n wly initi a ted bmllch es w e re c ho sen on each tree a nd p e rmanently tagged . These branches we ,,€, th e il, monito ,'ed th roug hout the yea ,' for geowth (basal di a m e t er, shoot elongation) and the follo wing ph(' no logie a l ch a .'acte ri stics. 1. 2. 3. 4.
The The The ThE'
nUllIbe ,' nun ,be,' numb(' " nlln,be ,'
o f jnveni le Leaves (lea fl e ts not full y expand ed). of mature leaves (l eafle ts full y expand ed). o f sen esce nt Leaves (le afl e ts c hlorotic, 0" a b sc issed ). o f a b sc issedl eaves.
5. ThE' Jltr11 ,b€' ,' o f C'fltE'n I('aves (25 % or m o ,'e leaf a l'ea con sum ed by insects). The nUlllbC'" o f inflo" es('e l1ces. 7. The numbs ,' o f I,'uits.
(j.
The a bove phenologi ca l ch a "tlcte ,:istics a re cins id e l'ed pools of leaves or f'e p "oductive structures. HlltC's of pLant function (flu x rates ) w e r e calc ulated by the following formuL a b ecau se the re was only on€' I('"f p e ,' n ode. Leaf produc tion = [TOT 2
+ ABS2]
-
[TOT1
+ ABS1] / T2
_ T1
Wc r€' 'I'OT1 = No. of lea vcH p" esent a,t Tim e 1 '1'0'1'2 = No. o f leaves pl'Csent at Tim e 2 ABR 1 = No , of €' mpty n od es £It Tim e 1 ABH2 = No. of e mpty nodes at Time 2 'I' 2 = Tim e 2 '1'1 = Time 1
O the r nlte fun ctions s uch as lea f a b sc ission ""te , lea f h e ,'b ivo "y rate , shoot elongation r a te, fl nd ropl'Oduet i vo 'p rod u ,tion l'ate we 'e I ' 'L' t d I h ' " "om t e Incr e m ent In a gI ven co mponent over the • Ca c u a e
Phenological Pattel'n s
267
time inter va l b e tween m easw 'eme nts. Following the initi a l Ma l'ch g l'owth flu sh a seco nd gl'owlh period occurr ed during .July a nd Augu st of 1980, DUL'ing thi s tim o fifteen newly initi ated s hoots were chosen a nd perm an e ntly t agged on each t ree bringing t h e total numbcl' of h,bc-l ed bl'an ('hes to 200. The previou sly m ention ed ph enological ch al'>tcte l'isti('s we l'e a lso monitol'cel on t hese Rumm el' produced shoots. L eaf a rea a nd specifi c leaf weight chtLl'ftct e l'i sti ('s wer-e also fo ll owed on these fi ve individu>ds. On each phenology sampling date a ll t h e leaves we l'e t ak e n :fl'om twenty shoots, pl'esRed ,in th o fi eld, and dried in a forced a ir oven at 70 °C fo '" 48 h. L efl f HI'ea m('aRUI'om('n t f< W (, ,' l1l ac\(' with th€' L T OIt leaf area m e ter (model # 1(00) a nd sp ecifi c leaf we ight was calculat(,d as mg ('m - 2 • Climati c ch a r acte l' istics of t empe l'atu T'e a nd p,'e cipitation a l'(' ,'edol'd ('d at lh e Bmw l('y LJ,R. D.A , weather st a tion, 40 km south of Harper ' s W ell. Reh\ti ve humidity and lCl11pertul'P we l'(' monito,'pel during p h enology sa m p ling at H a rper' s W ell to de t e rminc vapor' p,'e8S1]1'0 d('fi cits. Thp o ns it(' t('m· peratlll'e values w em con sistentl y 3 - 5 ° C highe. than t hosE' J'('eo l'd ed in Brawley, So il m o istw'e determinat ions w ere m a d e at - 25 c m a nd - 4.0 m b y th p u se of tho ]l<'utl'On acti vflt ion teehni q u ('. Neutron probe a ccess tubes w ere inse rte d und e rnea th eflc h o f the :fivc tl'e S Hnd betw('e 'l th e t ,'p(,., Reported soil moi sture val ves a r e a m ean o f data take n in all the a('('ess tubes. As anoth er r e lati ve indication o f ecosyst e m wa t er ava il ability to P. glandulosa p,'e· dawn xyle m PJ'Pss ul'e pote nti al (XPP) was m eascu'ed with a presslll'e ch a mber. Midday XPP was a lso monito,'('(l to ndi cat e the relative magnitude of season a l plant w a t e r s tress. A ll XPP measure m e n ts a l'e repo ,'ted as a n1('a n for five trees (N = 3 per tree).
Results Climate conditions for the region n ear Harper 's Well during 1980- 1981 are shown in figure one. T emperature increased from a minimum in January to a maximum, 43 °C, in July, The man maximum temperature stayed above 40 °C for 5 months (May to September). The lowest m ean temperature was 5 °C, and the t emperature n ever went below 0 °C, The maximum recorded temper ature at Harper's Well was 49,5 °C in July a nd the usual diurnal temperature fluctuation was about 17,5 °C. Vapor pressure d eficit has a simila r seasonal variation to that of temperature with the greatest vapor pressure d eficit (VPD) from May through August, Th e mean maximum YPD was 5,25 kPa (52,5 mbars ) which occurred in July, Also, in Jul y the diurnal VPD fluctuation was 3,5 kPa (NILSEN et al. 1981) , while in Januar y is waR only 2,0 kPa, Soil moisture was recorded at 25 cm depth incrementR from - 25 cm to - 600 cm, Here we report the average valves at - 25 cm and - 4-00 cm because theRe are th e zones of maximum root proliferation (SHARIFI et al. 1982). At a depth of 400 cm there is a constant water availability throughout the season, Th e soil moist ure at 400 cm depth (near field capacity) was much greater than a t 25 cm d epth , th erefore , there wa a constant background of available soil moisture. Surface soil moisture (- 25 cm) was below 9 % throughout the season, but maximum water availability in this rooting zone occurred from January through April during and directly after the period of maximum precipitation, Precipitation only occurred during the winter a nd spring months of 1980 and 1981. Water availability to the plants was m easured by d etermining the pre-dawn XPP, The pre· dawn XPP remained constant at about 2,5 MPa between June a nd December indicating the constant background water availability at d epth, During February
M. R.
268
SHARIFI
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MAMJJAS O ND J FMAMJ 1980 1981
Fig. 1. Clim at iC' co ndition s during 1980 - 1981 a t HaJ'pe l" s W ell, Califo1'llia n ear the Sou t hern tip of th o Sal t on i'ka. Pl'e· d >1w n >1nd midday xylem pressure potentials are means (n = 5 trees) for J'ro801Ji8 ytnnduto8a.
through April the pre.dawn XPP inereased (- 1.5 to 1.0 MPa) indicating the plants l'e8pOllRe to increased moisture availability at the surface following precipitation. During March t he midday XPP is similar to the pre·dawn XPP indicating only minor diurnal fluctua t ion in XPP. As the growing season progressed the midday X P P became prog l'c""ivcly lower until June indicating progressively greater plant water stress. The midday X P P r emained con, tant at - 4 .5 MPa from June through late December even t hough there were :-;ignifi cant changes in temperature, day l enght, and evaporative dema nd (V JI I)). Th e HeaHon ality of growth and development of these Prosopis trees is depicted in :Fig. 2. J~ach p h enological component is represented as a mean percentage of the seasonal maximum for the five individuals. The n umber of leaves in developmental catagOl'ies are represented as " Leaf Pools". The total number of leaves pel' branch rapidly increased during early March reaching a maximum value in late March . There was a slight decrease in total leaves from April through June as a result of herbivory (discussed later). The second growth period occUl'red ft'om J'uly through August, when leaves were rapidly produced on new ter-
Phenological Pa,tterns
100
LEAF POOLS Toto I No. of Leaves e" .P-_~ __
269 FLUX RATES
e_--,_.~P'e-.-~\-q\
50
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100 50 E ~ 100 E .;;; c :::!:
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No. of Senescent Leaves /e-e_______..
i
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No. of Abscissed Leoves .-It
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/'
1~ Growth Period
.
0--02 QQ Growth Period
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I
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F M A M J J A SON D J F M 1980 1981
100 50 F M A M J J A SON D J F M 1980 1981
Fig. 2. Seasonal prog"ession of phenological events on current pL'Odu ced shoots of Prosopis giandulosc, at Harper's "VeIl Californi a, near the southern tip of the Salton Sea.
minal shoots. Leaves were also replaced on March produced shoots. Total leaf number then remained constant through January for both sets of shoots. Total leaf number decreased rapidly in January -February for first growth period leaves and in Fe bruaryMarch for the second growth period leaves. The first cohort of leaves had an eleven month life span while the July produced leaves only lasted seven months. Juvenile leaves were present in large numbers on the new shootR only for a short period of time (less than one month). The brief presence of juvenile leaves was true for both growth periods. The first growth period shoots had a secondary occurrence of juvenile leaves just before the second set of new shoots were produced. The number of mature leaves on first growth period branches rapidly reached a maximum in March, remaining constant until late August. As the secondary growth period leaves matured the leaves on first growth period shoots became senescent. The remaining mature leaves on first growth period shoots in September were those produced in JUly. The senescent first growth period leavefl remained on the branches for more than six months (August-January). On the other hand , senescent second growth period leaves were on the branches for only 3-4 months . The senescent leaves began
M. R..
270
SUARIF]
et a l.
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(0) Shoot Length (e ) Shoot Basal Diam eter
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A
S
o
D
1980 Icig. 3. HpllHo n a l pI'ogl'cHsiol1 o f shoot length a nd b asal diameter in crement for current p"oduced shools o f I'rosopis ylandtt!osCi at Harper's W ell CRliforni a , neal' the southe rn tip of the SaLton Sea. Value'S ,"'(' >t l11 ('a 'l fo,' fi ve t r'ees.
to abscise in July-Augu st but the number of abscised leaves did not significantly incrcasc until January- March. The seaso.n ality of pl ant activity is r epresented as five " Flux Rate" panels in Fig, 2. Lcaf production rates were maximum for very short periods of time which indicate that distinct cohorts of leaves are produced on these individuals p , glandulosa. Shoots produ ced in Mar ch h ad a seconda ry cohort of leaves in August equaling the first coh ort in numbcr . JUly produced branches had only one cohort ofleaves. Shoot elon. O'ation rates were also rapid for short periods of time and there was no secondary elongation period on first growth period shoots. The lack of a secondary shoot elonga· tion period indi cates that the second growth period leaves on the first growth period shootH were located in old nodes, resulting in several nodes with more than one leaf. The leaf abscission rate was maximum in January and February for the first and second growth period leaves respectively. Leaf a bscission seemed to be synchronous within a bran ch similar to that of leaf production. The rate of leaf herbivory was maximum during periods of high leaf production, which coincided with the maximum number of juvenile leave. , Flower and pod production the first cohort in numbers . July pro. duced branches had only one cohort of leaves. Shoot elongation rates were also rapid for short period" of ti me a nd there was no secondary elongation period on first growth period Ahoots. The lack of a secondar y shoot elongation period indicates that the Hecond growt h period leaves on the first growth p eriod shoots were located in old nodes, r esulting .in several nodes with more than one leaf. The leaf abscission rate was maximum in J'a nuary and F ebruar y for the first and second growth period leaves respectively. Lcaf absciss ion seemed to b e synchronous within a branch similar to that of leaf production. The rate of leaf h erbivory was maximum during periods of high leaf production, which coincided with the m a ximum number of juvenile leaves. Flower and pod production rates occurred in a bimodal fa shion, April- May and again in June to
271
Phe nologi ca l P"lto l'n s
Table 1. Seasonal maximum valu es of ph e n ological cl ll:tI'acrorist ics for fiv o P l'Osopis glwullllo (I trees on shoots produced during two growt h p e riod s of 1980- 198 1. (X = moan, SX standa['d dov iation) '1'[,00
#
1
2
3
4
5
X
HX
12.4 16.7 0.5 1.7 0.9 0.7 1.5
11. 6 22.9 0.5 1.5 0.4 1.0 2.3
11 .7 2 1. 0 0.7 1. 8 0.5 1.1 1.:'1
1:3.7 20.3 0.1 1. 9 0. 8 1.0 0.9
11.0 35.9 O. 1. 8 0.6 1.0 3.4
12.9 23.4 0.5 1.8 0.6 1.0 1.8
1.5 7.4
7. 2 21.4 0.0 2.6 0.5 1.2 3.9
8.4 18.0 0.0 1. 4 0.4 0.5 0.7
lO. 2 33.5 0.0 1.9 0.5 0.9 2.7
12.7 26. 9 0.0 2.:3 0.4 0.5 1.7
8.0 29.4 0.0 1.8 0.3 0.5 9.5
9.3 25.8 0.0 2.0 0.4 0.7 3.7
2.2 6.2 0 .0 0.6 0.1 0.3 3.4
1st Growth P oriod (Februa ry - November) No . of leaves pel' s hoot Shoot le ngth (cm) No. of Pods per shoo t L eaf produotion (No. wk - 1 ) L eaf abscission (No . ",k - 1 ) L eaf herbivory (No. wk - 1 ) Shoot elongation (cm wk - 1 )
O . :~
0.3 0.2 0.1 1.0
2nd Growth P eriod (.July-D ece mber) No . of leaves per sh oot Shoot length (cm) No. of Pods p e r sh oot L eaf production (No. wk - 1 ) L eaf abscission (No. wk - 1 ) L eaf herbi vor y (No. ",1;: - 1 ) Shoot elongat ion (om wk - 1 )
August. Both pulses of reproductive activity occurred during the interim period be· tween the two p eriods of rapid leaf production a nd shoot elongation. No flowers or pods were produced on the second growth p eriod shoots. The two shoot growth functions, that of shoot elongation and diameter increment, 4ad varying season al progressions. Shoot elongation during the first growth period occurred within 4- 6 weeks (Fig. 3) , in contrast to cambial activity (diameter increment) which continued from March through November. Therefore these curre nt shoots elongate and produce leaves rapidly and later increase in diameter a nd weight. The actual mean values representing the m aximum values in Fig. 2 are reported in Table 1 for each individual. The highest variability found between trees for an y ph eno. logical component was that of shoot elongation in which the standard deviation was 55 % and 92 % of the rates occurred in a bimodal fashion, April- May and aga in in June-August. Both pulses ofreproductive activity occurred during the interim p eriod between the two periods of rapid leaf production and s hoot elongation. No f1 0werR or pods were produced on the seco nd growth p eriod shoots. The two shoot growth function s, that of shoot elongation and diameter increme nt, had varying seasonal progressions. Shoot elongation during the first growth p eriod occurred within 4- 6 week s (Fig . ~) , in contrast to cambial acitvity (diameter incre· ment) which continued from March through November . Therefore these currcnt sh oots elongate and produce leaves rapidly and later increase in diameter and weight . The actual m ean values representing the maximum values in Fig. 2 arc reported in Table 1 for each individual. The high est varia bility found betwecn trees for a n y phe.
M. R .
272
""'"
;;:
'0 .,
-' U
':'
E u
12
0>
.§
.,
.. ....
/
16
' 0;
•
SHARTFI
-
.
-.-.~
~j
p-~ -- -~, /
8
'0
e t a1.
6
0. (f)
4
5j
12
-'
., ~
0. 0
~
-
N
E
~
'0 .,
8 4
-'
e - e lll Growth Period 0- -o2!Jlj Growth Pe riod
•
<>0
150
.r::
(f)
:;; 0. N 0
~
'0 ., -'
E
~
100
\
... . • .-.
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-
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50
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Fig . 4. Season a l prog l'esHion of l eaf a l'e a p er leaf, leaf a r ea p el' shoot and specific leaf weight for CtH ,'c nt pl'oduced s hoots of Pro.sop is glandttlosa a t HarpeJ." s 'N e ll California n eal' the southern tip of th o Salton Flea. V alu es ,'cpor:te d a ,'e " m ean for five tl'ees du:[,ing two growth periods.
nological component was that of shoot elongation in which the standard deviation was 55 and 92 % of thc mean for the first and second growth periods respectively. The standard deviations of all other phenology component means combined averaged only 2 % of the mean. Th erefore , except for shoot elongation, there was only moderate v ariability betwee n trees for any phenological component in our samples (n = 5). Th ere were, ignificant differences between phenological charaeter maxima of the tw g t'Owth p eriods. Maximum pla nt activity rates (flux rates) of the second growth pe riod wer e hi gbcr than that of the first growth period (Table 1) except for leaf abscisNioll. Shoot lenO'ti1 s of both growth p eriods were similar although the number of leaves pel' shoot wai-llarger for the first growth period. Therefore , the internodal length of the second growth period (2.77 cm) was larger than that of the first growth period (1.82 cm). Very few reproductive Rtructures were produced during the first growing season and none of these on second growth p eriod shoots. Most fruits are produced on branches which arc two y ears old or older . Maximum leaf herbivory rates were high in relation to maximum leaf production rate" indicating that a large proportion ofleaves were conKumed by herbivorcK. Diffcren ces of climatic conditions and phenological maxima between the two growth period ;; have signifi cant influences on leaf area characteristics. F ig. 4 represents the
273
Phenological Pa ttel' ns
'fable 2. Correla tion between climatic conditions (1980- 1981) a nd phenological ch aractcristics of P.rosop~s glandulosa at H arper 's Well, in southern California Temperature Max
Min
V apor
X i lc m Press ure Potential Pressure Soil Moisturo D efi cit - 25 cm - 400 c m I're-dawll Midday
PhoLopcriod
Total number of leaves
.10
.05
.02
.20
.02
.05
.09
.03
Number of juvenile leav es
.03
.02
.01
.00
.30**
.25
.19
.00
Number of m a tlll'e leav es
.25
.24
Al **
.46**
.27
.00
.19
.55* *
Number of senescent leaves
.01
.00
.08
.07
.71**
.23
.13
.14
Number of abscissed leav es
.26
.16
.27
.30**
.00
.12
.23
.25
R ate of shoot elongation
.17
.15
. 14
.33**
.42**
.57**
.62**
.03
R at e of leaf production
.01
.00
.08
.00
.01
.07
.17
.01
R ate of leaf abscission
.06
.07
.13
.25
.46**
.07
.03
.24
R at e of leaf h erbivory
.00
.01
.01
.03
.06
.06
.12
.01
R at e of reproductive prod uction
.19
.19
.32**
.11
.06
.01
.04
.34**
(**p
~
.01)
leaf area characteristics for both growth periods. Specific leaf weight increased rapidly to a maximum in late March in close association with leaf maturation. The Rpccifi c leaf weight of leaves produced during the second growth period was lowcr than that of the first growth period. The increase in leaf area per leaf was also closely associated with leaf maturation but second growth period leaves were much smaller than firHt growth period leaves. The suddden decrease in leaf area per leaf and per shoot during August is the result of new leaves produced during August (with second growth period area characteristics) on first growth period shoots. The leaf area per shoot is a product of leaf number per shoot and leaf area per leaf. As a result the sccond growth period shoots had a proportionally smaller leaf area per shoot in relation to the first growth period than a similar comparison made for leaf area per leaf. Both leaf area value and specific leaf weight reflect senescence by their decline during November through February. Leaf area decreases as a result of leaflet abscission and leaf abscission on a leaf basis and a shoot basis respectively. Specific leaf weight decreases during senescence as a result of mobile solute re-translocation into the stems. Correlations were made between the climatic parameters and the phenological components (Table 2). The only significant correlations were found between water relations components and phenological events. Shoot elongaton rates and leaf abscission rates
27+
M. R .
S HAIUF [
e t " I.
Ree m to be well associated with surface soil moisture although shoot elongation rates Ree rn bm;t l1HRoc iated with p lant water stress relationships. Senescent leaves also seem be~t assoc iatod with surface :'io.il moisture. The mature leaf pool seems to be well associated with V I'D, soil moisture at d epth, and photoperiod. Associations with VPD and ph otoperiod are hard to Heparate since they are highly intercorrelated (R2 = .90). All ther Heaso nal progressions of phenological characteristics are poorly correlated with the proO" r'osH ion of climati c conditions at Harper 's Well . Discu ssion Th o 'Jimatic co nditions at Harper 's W ell suggest several strong environmental streKRes to which the Prosopis trees are exposed. First , there was a high heat load stress during the s ummel" monthA. Secondly, in accordance with the high temperatures, the V P D waf) hig h particularly during the summer. Thirdly, soil moisture in the upper soil levels was always low (below 9 %) again, particularly during the summer. The low surface Hoil moi f)ture was cleady associated with the v ery low annual rainfall. Therefore, water. tresH in surface soils and heat stress conditions were extreme during the summer month s. These summer temperatures are considerably higher than the temperature optima for photosynthesis in many desert plants (BJORKMAN 1980). The midday XPP ex perienccd by the -e Prosopis trees was lower than the experienced by other desert phrcatop hytes (STRAIN 1970 ; SZAREK & WOODHOUSE 1978). The ai'-nual rainfall for t hi s I:> ite during 1980- 1981 and on a 30 year average basis (65 mm) is in the lower range for most warm desert sites in North America (EHLERINGER & MOONEY 1981). Th eHe Hevore environmental stresses should be strong selective pressure for water f:)tresH a nd heat stress ada ptation in Prosopis as is found in other desert plants. Ma ny desert plants have evolved a daptive phenologies in response to the extreme deHert cli ma teo Some of these a daptive phenologies are manifest ed in short lived winter a nnual;; (M L1WY & R UNDEL 1977) , perennial summer deciduous shrubs (MOONEY 19 0) or p el.'renial evergreen s hrubs with seasonal variability in leaf characteristics (MOON.EY et al. 1974- ; SMl'.r.H & NOBEL 1978). The phenology of Prosopis is quite different tha t t hat of other desert sp ecies. Prosopis maintains maximum leaf area througho ut t he ITI Oflt stressful period of the year. Also, there is a pulse of growth during the h ottest a nd dryest month of the year. Both of these growth characteristics would seem to be maladaptive for sp ecies growing in this summer dry climate. The phonology of current season s hoots in Prosopis is also characterized by rapid growth characteristics over s hort duration. This is true for leaf production, shoot elongation and leaf abscission but not for eambial growth. This occurred during both growth periods. The short duration of leaf production and the rapid leaf maturation result in s hort periods when juvenile l eaves are present on the branches. This may be a n adaptation against herbivores since leaf herbivory was highly associated with the presence of juvenile leaves. Durino- 1980- 1981 there were two growth periods for Prosopis at Harper's Well eac h of which occurred during very different climatic conditions. The first growth
P h enol ogica l P 'tttems
275
period in Marc h occurred during low tempera tures (max = 20 °0) , low VPD (2 kPa) a nd high surface soil moixture (9 % ). The second growth period occurred during high temperatures (max = 45 °C) , high VPD (5 .3 kPa) and low surface soil moisture (5 %). As result of the high July water stress conditions the second growth period leaves were smaller, each branch had fewer leaves, and each branch had a sma ller leaf area. Also, it seemed that the higher t emperatures during the second growth period caused more rapid elongation rates over a shorter duration. Although the second growth period leaves were produced four monthf! after the first growth period leaves, abscission occurred almost simultaneously for leaves of both growth periods. Abscission events were abrupt, just as were leaf production events, a nd abscission seemed to be stimulated by increased surface soil moisture in February. This is suggested by the first growth period senescent leaves, which remained on the trees until late January when they began rapidly abscising a t a , imilar time as the abscission of the second growth period leaves. Associations between climatie conditions and phenological events were minimal. The phenology of current shoots seems best associated with various water relations characteristics particularly shoot elongation and leaf abscission. T~eaf production and leaf herbivory were not correlated with any climatic factor but they were well correlated with each other. The poor associations between climatic events and leaf production is the result of the short duration of leaf production following a stimulus . Also there is often a lag between the climatic stimulus and the phenological response (NILSEN & M ULLER 1980) . Therefore correlations b etween climate and phenology can only be used to suggest relationships and such correlations are prone to missing actual stimulusr esponse associations. There were several phenological events which seemed to b e well associated with each other. Two of these. leaf production and reproductive production, su ggest that there is an endogenou s sequence of growth. That is, leaves are produced, following which all energy is placed into flower and pod production. Following pod drop leaf production is once again initiated even though climatic stress is severe during the second p eriod of leaf production. The initial season al growth in F ebruary a nd March seems to be stimulated b y a climatic factor following which an endogenous growth sequence prevails. There are other suggestion of endogenous system controlling growth in tropical plants (BORCHERT 1978) . Prosopis may be used as an example elucidating the gen eral phenological system of a phreatophytic species. Growth occurs in rapid spurts of s hort duration initially in response to some climatic parameter , which is likely water relations. Following the initiation of growth an internal endogenous sequen ce seem s to directgrowth. Pt'osopis phenology also suggest that phrea tophyties are able to maintain large leaf areas throughout the stressful desert summers, in contrast to other desert taxa with small leaf area or short duration leaves (SMITH & NOBEL 1978). This unusual phreatophytic phenology can only be maintained by ample water resources at d epth. The rapid a nd short duration of growth may be an adaptation against strong herbivory pressure on n ewly produced leaves.
M. H,. SHARIF! et a!.
276
Continued invQf;tigations of the ph enologieal patterns of legumes are of critical importance in understanding the adaptions of these taxa to desert environments. Such invoRtigati.onfl aro a lso important to interface with studies of legume physiological eco logy a nd population biology. Sympatric phreatophytie taxa may have a differing phenological patterns (TUl~NE1~ 1963) with a different adaptive significance. For this rea on we are continuing research on the phenology of several phreatophytic taxa in a n atural eommon garden. Also, the temporally separated production of P1'osopisleaf co hortR iR being tudied through life table population biology analysis (HARPER & W IIIT.m '1974) . In addition, a comprehensive study of older Prosopis branch phenology haR b een initiated .
Acknowledgements 'l"hiH "C'Hl1>L.'ch
WllS
s UPPol'ted by t h e National Science Founda tion grant number DEB 79-21971.
References ,I. C. (1974): Ph enolog ical event s and their en vironmenta l triggers in Mojave Desert ('C'OSYHtP III K. 'I ~co i ogy 55: 85fl - 8 C13. BOltCII"It'I', H. (197R): F t>E'dbfl(;k control and flge r elated ch anges of shoot growth in seasonal and non'KPHHonH i c'iin mtes. In: TOMLINSON, P. B., & ZJMMERMANN, M. H. (eds.), Tropical Trees as Living HYKtel11s. Cambl·jdge U ni ve l'sity Press, Cambridge, M assachusetts, pp. 497 - 515. BJOltl(MAN, 0., BADGE R, M. H,., & AHMOND, P. A. (1980): H,esponse and adaptation of photosynthcHiH to high t empe .'atlu'e. In: T UHNllH, N. C., & KUAMER, P. J. (eds.), Ada ptation of Plants to W"tc' .' "nd Hig h Te mpe.l'atul.'e Stress. WiLey-Interscien ce, N e w York, pp. 233 - 249. IBIiLICltl NG" It, ,I ., & MOON" ' -, H. A. (1983): Photosynthesis and productivity of desert and mediterl'lll1l'llll-e iim flto pla nts. Encye iopedia of Plant Physiology 120 . Springer, N ew York-Heidelberg· BC' riin. F.I'LK ICIt, 1'. (1979) : Mesquite : an an purpose leguminous arid la nd tree_ In: Rrl.'CHIE, G. A. (ed.), NC'w Ag ,'ieultuL'll1 C,·o ps. AAAS, W estview PJ'ess. Boulder, Colorado. GULMO N, H. L., & MOONJ~Y, H. A. (1977): Spatial and t e mpo.'a lrelationships between two desert s hl.' ubs, A t1'ip lex hyrnenelytm Hnd TJ.'idest1·ornia oblongifolia in D ea th V alley, California. J. E ra!. 65: 831 - 8 38 . .H.A lt l'mt, ,I. L. , & WHI 'I'Il, .1 . (1974): The d e l'llogmphy of plants . Ann_ R ev. of E col. and System 5: 419 - 4(;3.
B'M'I'LIW,
HODOK' NSON, K. C.. JOII NSON, P. S., & NOltTON, B. E. (1978): Influen ce on summer rainfall on I'oot and "hoot g l'ow th of a eold winter d esert 8hmb Atriplex conjertijolia. Oecologia 34: 353 - 3(;2. MOONE ", I-l. A. (1980): SeflsonaJity and gradients in the study of stress a d a ptation. In: TultNlm, N. C. , & KItAMEH, P. J. (eds.), Ad a pta tions of Plants to W a t e r find High T emperature Stress. Wii cy- lnte l'sden ce, N ew York. BJO ltKMAN, 0 ., & 'J'.ltO UGllTON, .J. (1974): Seasonal changes in the leaf ch aracteristics of the clesPl't shl'ub At1'iplex hymenelytm. Carnegie Ins t. Yr. Book 73: 84C1-852. MULltO'{, '1'_ W., & H,UNDEL, P. \-V. (1977): Annual pla nts: adaptions to desert environments. Bioscie .wC' 27: 109 - 114. N ILSEN, E. '1'_, & MULLJm,W. H. (1980): An evalu a tion of summ er d eciduousness inLotu88copariu8 NUTT. in T . & G. ArneI'. Mid. N a t. 103: 88 - 95. RIJND IU", P. W., & flHAltlFJ, M. R. (19 81): Summer wa ter r el a tions of the d esert phreatophytie Prospis alandulosa in the Sononlll D esert of southern California . Oecologia 50: 217 - 224.
Phe nological Patte m s
277
PARKJ<~R, IC "V., & MARTIN, S. C_ (1952): The m esquite pl'Obl e m on soutl1el'll Al'izona range. USDA
Circular 968: 70. SHAnn'], M . R., NlLSEN, E. '1'., & gUNDEL, P. 'vV. (1982): Biom ass a nd ne t prim ary production of Prosopis glcmdulose, (Fabaceae) in the SOIlOI'un d esert of Califomi a. Am er. J. Bot. 69 (5): 760 - 767. SHREVE, F. (1942): The d ese rt vegetat ion of North Am eri ca. Bota ni cal R evie w 8: 195 - 246. SMITH, vV. IC, & NOBEL, P. S . (1978): Influ e nce of il'l'>ldiation, soil wa te l' potenti al, and leaf temperatur'e on lea f morphology of a d ese r t bl'oadle"f Encelia farinosa GUAY (Compositae). Am er. J. Bot. 65: 429 - 432. STR,II N, B. R_ (1970): Fi eld measure m e nts of ti s~u e wate l' pote ntia l ,tnd ca l'bon dioxid e xchange in the d esert shrubs P1'080pis jUliflom and Lrt1'1'6(f, divCI1'icata. Photosyn thetic" 4: 11 8 - 122. SZARl~K, S. P., & WOODHOUSE , R. M. (1978): E co phys iological ~ tudi es of SonOl'an d esel't pla nts. III. Daily course of photosynthes is for Acacia gr'eggi'i " nd Gercidium micfophyllum. Oecologi a 35 : 285 - 294. TURNER, g . M. (1963 ): Growth in fOU l' s p ecies of Sonol'ttn deser·t trees. E cology 44: 760 - 765. Received April 20, 1982 Authors' a ddresses : M. R. SHAR[FI, E . T. NILSEN, a nd P. W. R UNDEL, De partm ent of E cology and Evolutionary Biology, University of California, Ir'vin CA 92717; l~. VIRGINJA a nd W. M. J.umELL, D e pal·tm ent of Soil a nd Environm ental Science, Unive r'sity o f California, Rive r sid e CA 92521.
H :FJora, Ed. 173