Table Of ContentMadrono, VoL 61, No. 1, pp. 126-136, 2014
CHOLLA MORTALITY AND EXTREME DROUGHT IN THE SONORAN DESERT
Edward G. Bobich
Biological Sciences Department, California State Polytechnic University, Pomona,
CA
91768
[email protected]
Nick L. Wallace and Keely L. Sartori
Department of Biology, Whittier College, Whittier, CA 90608
Abstract
At the beginning of the 21st Century, deserts and woodlands of the southwestern United States
were in the midst of a drought that contributed to massive die-offs for many plant species. In the
northwestern SonoranDesert, thedroughtcontributed toextremedesiccationandmortalityofcholla
(Cylindropuntia) cacti. At low elevations (210-290 m), over halfofthe Cylindropuntia bigelovii, over
17% ofthe C. echinocarpa, 6% ofthe C ramosissima, andlessthan2% ofthe C. ganderiweredeadby
winter 2004/2005. At a higher elevation (—820 m), 26% of C. bigelovii and 14% of C ganderi were
dead by winter 2005/2006. The lower mortality for C. bigelovii at the higher elevation site was likely
due to milder temperatures and greater precipitation; the greatermortality for C. ganderiat the same
site may be the result of freezing or frost damage to tissues during the drought. Differences in
mortality among species at both elevations were attributed to several factors, including: intra- and
interspecific competition, reproductive strategy, and shoot architecture. Based on this study and
previous research, it is believed that C. bigeloviiexperiences periodic extensive die-offs in response to
extremedroughts, whereas populations ofthe otherthree species apparently change littleduringsuch
droughts.
Key Words: Chollas, Cylindropuntia, desert, drought, mortality.
Populations of desert perennials are dynamic, Southwest will likely increase in frequency and be
with plant cover, mortality, and recruitment tied more extreme in the future (Weiss and Overpeck
to several factors, especially total yearly or 2005; Seager et al. 2007).
seasonal rainfall (Martin and Turner 1977; Desert cacti, especially barrel and columnar
Goldberg and Turner 1986). Extreme climate forms, are able to survive long-term drought
events are believed to have a disproportionate because they have voluminous amounts ofwater-
effect on a variety ofprocesses within organisms storage tissues (Gibson and Nobel 1986). They
ofa population (Gutschickand BassiriRad2003). also tolerate some of the highest tissue temper-
For populations of desert perennials to experi- atures of any group of vascular plants and can
ence measurable changes, events such as drought acclimate to higher temperatures than they
must be prolonged or especially severe compared typically experience (Smith et al. 1984). Forcacti,
to the conditions they usually experience the relative tolerance to high temperatures and
(Gutschick and BassiriRad2003). Such a drought drought is linked with morphology. Chollas
occurred throughout much of the southwestern (genus Cylindropuntia [Engelm.] F.M. Knuth of
United States around the turn of the 21st North America) have stems with relatively small
Century, with 2002 being the driest year on volumes ofwater-storage tissues and high surface
record for much of the region (NOAA, NCDC area to volume ratios (Gibson and Nobel 1986),
website, Breshears et al. 2005). Massive die-offs characteristics that can lead to lower relative
ofmany desert perennials occurred as a result of tissue temperatures in the field (Nobel 2009),
this drought (Miriti et al. 2007; McAuliffe and which maybe one reason whythis growth formis
Hamerlynck 2010), as well as Pinus edulis successful in warm deserts of North America.
Engelm. (Breshears et al. 2005). There is evidence However, because chollas likely experience lower
that, in addition to low precipitation, increasing stem tissue temperatures in the field, they have
ambient temperatures (Breshears et al. 2005), lower maximum viable tissue temperatures than
differences in soil composition (McAuliffe and barrel and columnar cacti (Smith et al. 1984).
Hamerlynck 2010), and plant age (Miriti et al. Thus, during extreme long-term drought with
2007) affected mortality during this drought. elevated temperatures, such asthatexperienced in
Measured increases in minimum winter temper- the drought at the turn ofthe century (Breshears
atures, as well as predicted increases in annual et al. 2005) and those predicted for the future
mean temperatures and a predicted drying ofthe (IPCC 2007), chollas may experience greater
entire region, indicate that droughts in the Desert mortality than barrel and columnar cacti not
2014] BOBICH ET AL.: CHOLLA MORTALITY AND EXTREME DROUGHT 127
only because they store less water than these 1965), and to compare the climate at the two sites
growth forms, but because their tissues may not in this study.
be able to tolerate increases in temperature.
The severe drought at the end ofthe 20th and Methods
the beginning of the 21st centuries appeared to
lead to extensive mortality for several cholla Field Observations
species in the northwestern Sonoran Desert. In
early fall 2004, nearly every Cylindropuntia Research was performed in the flood plain
bigelovii (Engelm.) F. M. Keuth, Cylindropuntia (210-290 m; 33°39'N, 116°22'W) and at Agave
echinocarpa (Engelm. & J. M. Bigelow) F. M. Hill (820 m; 33°38'N, 116°24'W) within the
Knuth, Cylindropuntia ganderi (C. B, Wolf) University of California, Riverside Philip L.
Rebman & Pinkava, and Cylindropuntia ramo- Boyd Deep Canyon Desert Research Center
sissima (Engelm,) F. M, Knuth at low elevations (Deep Canyon) in Palm Desert, California. The
were extremely desiccated or dead and most following cholla species were studied in the flood
living plants had not flowered or produced new plain: Cylindropuntia bigelovii, C. echinocarpa, C.
stems for two years (M. Fisher personal com- ganderi, and C ramosissima. Only C bigelovii
munication), In the 1960’s, C bigelovii experi- and C ganderi occurred at Agave Hill. In the
enced a die-off at the same location (McDo- flood plain, 10 plants occurring approximately
nough 1965). 238-250 m in elevation were not included in the
For the recent drought, C bigelovii clearly study because they could not be positively
experiencedextensivemortality. Mortalityforthe identified to species.
other species was difficult to assess initially At both sites, chollas were sampled in 10 m X
because cacti can experience extreme desiccation 10 m quadrats. In the flood plain, four quadrats
and survive (Gibson and Nobel 1986), Thus, the were placed roughly west to east every 0.2 km
purpose of the study was to determine how the along a total distance of 2.8 km south from the
morphology of each species and the apparent fence at the north boundary of the Research
competition they experience were related to their Center. At Agave Hill, three quadrats were
relative mortality as a result of the drought. positioned roughly west to east on two north-
Because ofthelength and severity ofthe drought, and two south-facing slopes, for a total of 12
it was hypothesized that species survival should quadrats. Only chollas whose bases were in the
depend on the ability to store water, which is quadrat boundaries were sampled. Dead chollas
related to stem volume and the amount ofwater were included in the study if they possessed an
storagetissueinthestems (Nobel2009). Based on intact epidermis over approximately 75% oftheir
these criteria and previous research on the four shoots, which would indicate that they died
species in Deep Canyon (Bobich and Nobel during the drought. Chollas in the flood plain
2001), C. ramosissima should have experienced were determined to be living or dead during the
the greatest percent mortality, because its stems winter and early spring of2004/2005 because the
had the smallest volume and smallest amount of site received 269 mm of rain from October 2004
C
water storage tissue, follov/ed in order by through February 2005 (average precipitation
C
echinocarpa, C. bigelovii, and ganderi. It was from July 1-Jurie 30 for the site was 140 mm),
also hypothesized that shorter species with more allowing living plants to rehydrate and produce
basal branches should have experienced lower both new shoots and flowers. Chollas were
mortality because they would experience lower studied at Agave Hill during winter 2005/2006
water stress dueto gravity and be able to sacrifice when all living plants possessed turgid shoots.
some oftheircanopy and survive, comparedwith The following morphological measurements
taller species with fewer basal branches. In were recorded for individual plants: height,
addition, species that experience the greatest lengths of the major and minor axes of the
competition for resources should experience the canopy, and number of basal branches, which
highest mortality. The effects of elevation on were defined as major branches originating
m
plant mortality were also assessed by observing within 0.2 of the plant base. Height measure-
C bigelovii and C ganderi at a higher elevation ments for some of the dead C bigelovii were
where they were hypothesized to have experi- approximated by measuring the height of the
enced lower mortality, because temperature upright portion ofthe shoot and the length ofthe
decreases and rainfall increases as elevation nodding or detached upper portion ofthe shoot
increases. To test these hypotheses, morpholog- lying near the base of the plant. Canopy spread
ical measurements, distances to nearest neigh- was calculated by taking the square root of the
bors, and descriptions ofpatterns ofshoot death product of the major and minor axes. Canopy
were recorded. In addition, climate data were axes were not measured for dead C. bigelovii
analyzed to compare the conditions prior to this because the majority of the lateral branches had
study and those leading up to the previously detached; the dead individuals ofthe other three
reported die-off at the same site (McDonough species appeared to have retained most of their
MADRONO
128 [Vol„ 61
stems, allowing for canopy measurements. Ob- distances to the nearest cholla and nearest shrub
servations of shoot death, including detached among the species in the flood plain were
dead shoots, retained dead shoots, and the performed using Kruskal-Wallis one way AN-
apparent direction of the death of the shoot OVA. Comparisons between C bigelovii and C
(acropetal orbasipetal), weremadein an effort to ganderi at Agave Hill were performed using
relate morphology to mortality. Distance to the Mann-Whitney U tests. Comparisons for C.
nearest cholla was recorded because chollas bigelovii and C ganderi between the flood plain
demonstrate a high-level of intraspecific and and Agave Hill and between living and dead
interspecific competition (Cody 1986a, b). Dis- plants for each species within each site were also
tance to the nearest shrub was also recorded performed using Mann-Whitney U tests. For C
because most of the shrubs at each site, ganderi in the flood plain, living and dead
represented primarily by Ambrosia dumosa (A. individuals could not be compared because only
Gray) W.W. Payne, Enceiiafarinosa A. Gray ex onehad died. ClimatedataforPalm Springswere
Torr., and Larrea tridentata (Sesse & Moc. ex compared between the 1954/1955-1963/1964 and
DC.) Coville in the flood plain and Ambrosia 1994/1995-2003/2004 seasons using Student’s t-
&
dumosa, Bahiopsisparishii(Greene) E.E. Schill. test. Precipitation and temperature were com-
Panero, Bebbia juncea (Benth.) Greene, Enceiia pared between the flood plain and Agave Hill
farinosa, Eriogonum fascicuiatum Benth., and using paired t-tests, with data grouped by year.
Larrea tridentata at Agave Hill, likely had a Data are presented as means ±1SE.
significant portion of their roots within the
rooting zone ofthe chollas (Cody 1986b; Rundel
Results
and Nobel 1991; Nobel 1997; E. Bobich personal
observations).
Distribution, Die-back, and Mortality ofChollas
Climate Data Each cholla species in the flood plain had a
different elevational distribution. The only spe-
Precipitation and mean yearly temperature in cies that occurred throughout the entire flood
Palm Springs were determined for the 10 seasons plain was Cylindropuntia ramosissima. Cylindro-
(July 1-June 30; 1954/1955-1963/1964) prior to puntia echinocarpa had the lowest elevational
the publication ofthe die-offofC. bigeloviiin the range and was not sampled in quadrats above
early 1960’s (McDonough 1965) and for the 10 244 m. The lowest elevation at which C bigelovii
seasons (1994/1995-2003/2004) leading up to this and C ganderi were sampled in the flood plain
study. Climate data for Palm Springs were was 250 m, with C ganderi apparently replacing
downloaded from the Desert Research Institute’s C. echinocarpa; C. bigelovii was especially com-
Western Regional Climate Center website mon on rockier soil. At Agave Hill (—820 m), C
(wrcc.dri.edu). Because climate data for Agave bigelovii was sampled only on south-facing
Hill was not recorded until 1973, precipitation slopes, which is where they primarily occurred,
and mean yearly temperature for seasons 1973/ whereas C ganderi occurred in quadrats on both
1974-2003/2004 and the 10 seasons leading up to north- and south-facing slopes.
the drought (1994/1995-2003/2004) were com- In late fall 2004, chollas in the Deep Canyon
pared between the flood plain and Agave Hill. In flood plain were extremely dehydrated and most
addition, the number of days with low temper- had experienced substantial die-back, although
atures <0°C and days with low temperatures 0- the patterns of shoot die-back differed among
2°C, which can lead to radiation frost or frost species (Fig. 1). Most ofthe dead C bigeloviihad
pockets and freezing damage to cacti, were blackened shoots with black spines; living stems
recorded for the 10 seasons leading up to the were usually bright green with yellow spines
drought for both the flood plain and Agave Hill. (Figs. lA and 2). The shoots of C. bigelovii
appeared to have died acropetally, the evidence
Data Analysis being that living plants, as well as some ofthose
that had collapsed, retained living stems on
There were typically few individuals of each approximately the top or distal third of their
species in each quadrat, so the data for each shoots (Fig. 2). The shoots of many dead or
species was pooled for both the flood plain and dying C bigelovii failed near the base and fell
Agave Hill. Percent mortality was calculated for over or appeared to have collapsed (Fig. 2), but
each species at both sites. Morphological data most plants that died had eithera nodding shoot,
and distances to the nearest cholla and nearest with approximately the top third of the shoot
shrub were not distributed normally for any of bent downward, orthe top third orquarter ofthe
the species and the variances among species were shoot had completely detached from the rest of
C
rarely equal. Because most ofthe data could not the plant (Fig. lA), For echinocarpa (Fig. IB),
be transformed to allow for parametric compar- dead stems occurred throughout the shoot
isons, comparisons of morphological data and canopy; in some cases, entire major branches
2014] BOBICH ET AL.: CHOLLA MORTALITY AND EXTREME DROUGHT 129
Fig. 1. Representatives ofA) Cylindropuntia bigelovii, B) C. echinocarpa, C) C. ganderi, and D) C. ramosissima
duringthefallof2004inthefloodplainofthePhilip L. Boyd DeepCanyonDesertResearchCenter, PalmDesert,
CA. Arrows indicate nodding shoots in A) and dead branches in B), C), and D).
had died. There were almost always dead small over 10% mortality (Table 1). For C. ganderi in
C
stems near the base of each echinocarpa. the flood plain, only one sampled individual had
Cylindropuntiaganderiand C. ramosissimaclearly died, whereas 14% died at Agave Hill (Table 1).
experienced basipetal dieback, which often re- Almost 6% of the sampled C ramosissima were
sulted in the death of entire major branches dead in the flood plain by the spring of 2005
(Fig. 1C, D); however, whereas the dead terminal (Table 1).
stems of C. ganderi were almost always attached
to the plant, copious numbers of dead stems Morphology and Proximity to Other Chollas
occurred at the base of all but the smallest C. and Shrubs
ramosissima. The shoots ofmany ofthe largest C
ramosissima apparently split at the base, appear- In the flood plain, C ganderi was on average
ing initially as separate plants, especially those 75% as tall as the other three cholla species, but
individuals whose bases were buried in mounds at Agave Hill it was statistically the same height
ofsandy alluvium. After the rainfall in the winter as C bigelovii (Table 2). Cylindropuntia bigelovii
of2004/2005, many plants that initially appeared had the smallest canopy spread of the four
to have been dead, especially certain C. ramo- species, with a canopy 40% as broad as those of
sissima, rehydrated and developed new stems. C echinocarpaand C ganderi, and 24% ofthat of
The cholla species that experienced the highest C. ramosissima in the flood plain. At Agave Hill,
mortality at both sites in the Boyd Reserve was the spread of C bigelovii was less than 50% of
C
C. bigelovii(Table 1). Overhalfofthe sampled that of C. ganderi (Table 2). Cylindropuntia
bigeiovii were dead in the floodplain, whereas bigelovii also had the fewest basal branches, with
just over one-fourth were dead at Agave Hill almost all plants having a single trunk at both
(Table 1). Ofthe otherthree speciesthatoccurred sites. In the flood plain, C ramosissima had the
C
inthefloodplain,only C. echinocarpaexperienced most basal branches, followed in order by
i
MADRONO
130 [Vol. 61
Fig. 2. A) Two healthy and two collapsed dying individuals of Cylindropuntia bigelovii and B) a view of the
collapseddyingindividualsshowingdeadbases,leadingtothecollapse, andlivingstemsontheapicesoftheshoots.
The plants were located in the flood plain of the Philip L. Boyd Deep Canyon Desert Research Center, Palm
Desert, CA.
gander and C. echinocarpa (Table 2). At Agave morphology (height, spread, and number ofbasal
Hill, C ganderi had three times as many basal branches), orproximityto otherchollas orshrubs
branches as did C. bigelovii (Table 2). (Table 2). At Agave Hill, dead C. ganderi nearly
In general, chollas were smaller at Agave Hill differed in height from living individuals; how-
than in the flood plain. The heights ofC. bigelovii ever, no other comparisons yielded P < 0.12
and C. ganderi at Agave Hill averaged 71% of (Table 2).
those in the flood plain (Table 2). Canopy spread
and the number of basal branches did not differ Climate
between C. bigelovii in the flood plain and those
at Agave Hill. For C. ganderi at Agave Hill, ForPalm Springs, the average precipitation for
canopy spread was 75% smaller and individuals the 10 seasons (July 1-June 30) prior to the
averaged one less basal branch than did those in publication of McDonough (1965) was statisti-
the flood plain (Table 2). cally the same as it was for the 10 seasons leading
In the flood plain, C bigeloviiindividuals were up to this study (Table 3), whereas the average
m
nearly 1.0 closer to other chollas, usually other yearly temperature for the 10 seasons leading up
C bigelovii, than were plants of the other three to this study was almost two degrees higher than
species, all of which were similar distances from it was from 1954/55-1963/64 (Table 3). From
other chollas (Table 2). At Agave Hill, C 1973/74 to 2003/04, the climate in the flood plain
m
bigelovii was 0.7 closer to other chollas than was warmer and drier than that of Agave Hill
was C ganderi (Table 2). Cylindropuntia bigelovii (Table 4). In fact, for every season, except 1986/
individuals were also 1.0 m closer to shrubs than 87 and 1989/90, Agave Hill received more
were the other three species in the flood plain, precipitation than did the flood plain, with the
whereas at Agave Hill C. bigeloviiand C. ganderi average seasonal precipitation in the flood plain
were similar distances from the nearest shrubs 80% of that at Agave Hill. During that same
(Table 2). Overall, chollas at Agave Hill were period, the average daily temperature in the flood
much closer to their nearest neighboring chollas plain was over 3°C greater than that at Agave
and shrubs than were similar species in the flood Hill (Table 4). Over the ten seasons leading up to
plain (Table 2). this study, the flood plain again received approx-
Dead individuals did not differ significantly imately 80% of the precipitation at Agave Hill.
from living individuals for any of the species in During the same period, both the flood plain and
the flood plain or at Agave Hill in terms of Agave Hill received an average of 69% of the
Table 1. Percent Mortality for Cylindropuntia Bigelovii, C. echinocarpa, C. ganderi, and C.
RAMOSISSIMA IN THE FLOOD PLAIN AND AT AGAVE HILL IN THE PHILIP L. BOYD DEEP CANYON DESERT
Research Center, Palm Desert, CA. Valuesinparenthesesindicatethe totalnumberofindividualssampledat
each location.
C. bigelovii C. echinocarpa C. ganderi C. ramosissima
Flood plain 55.6 (275) 17.5—(63) 1.6 (61) 5.9—(85)
Agave Hill 25.8 (128) 14.0 (57)
2014] BOBICH ET AL.: CHOLLA MORTALITY AND EXTREME DROUGHT 131
Sampled Ftlohoed oatihfle "C£TdS wO T^cwSd TawS.S ^ X) o^o<<o:oxo<o<oxo ^ XOorn<—Or!n^r<CONkioOcmd'oO'<d!oC"<DXrooc’'drOo<'!Ooo<N'
the in For C § “ -O I - i+1o+m1x+1o<+1xH)o+o1^+1oo+1 d +1 +1 +1 +1 +1 fl +1 +1 +1
X m
of CA. rXn L(N rn rinn vrqn OIT) (N mmcnoooooo
S -o SI s,, s
all ramosissima M ^ W czi '‘
Desert,
Shfrourb Cand Palm '(Cou'olUi~U:^o"ss ^^^oo<<.unu. ofc6oid •^CS§a-fl 28d^ ^cOOd ooO+^1s—d'+1^id<^n+1rrdiX-+m1-dc<—+N1<id<rt+!1s-diX'+r1d0N—+i1oI NXfo+d1oN<+Xfd1'N<+E^r1idod+n1o(<do+X1o<)d+*1iX^d>+^1c<d’D+1-N<d^+X1
bO ® o ^ ^ or-r--oxoimnxofooNqoxrr^Nci^ oinoiin>r-^0i'ndi‘ni'n^(cNnrmif.n-xH
Center, o 2 S ^ 'C X X E r4 d ri ri rl cN (N fN d d d -=< L
Nearest ganderi, TO ^ ^
> 6(D ^^ OgUS)
tthoe C. Research Z 2 UCcod« Ja^-l x^<Ju X,ccc)dnd o<Do oddododfNdXcdsdmfdondm ’dod’d<lnd<oNdOdfd<N'<dd'xdf<ndX!'do<o
§:°S O Q
§§ d
echinocarpa,Desert IisS - “ § X 2 +1 il +1 +1 il +1 fl +1 X+1 O+1 +1 X+1 X+1 X+1 X+1 +1 ®+1
Distance ,^(^U ^T2 o ZSd-^ X X X d O O -d" 'd' in in "dL -4 X X d d
ai
and C. Canyon ^iD=( ^«^ ^sQ oo o
E S W. X<<X x<<d X < <
Bigelovii,Deep d o ^ S mOdiOdn'md-ihdnOidOn^dOOd-dhdO Xo Xo o
X d d d
Cholla, 2
Boyd S^ ^2 ^§d -^OSP 2SI U§ gb OXo+N1 VVo+OO1 o’0+-01H o0X+01 o0X+01 d X^+1 r^+-1 om+o1 -0+d41- <m+-11 X(+N1 m+1
Nearest Cylindropuntia L. o2 r^d _Ed L) d<D
'S > ^
tthoe of HPhitiihllnielp ^‘S»^^MM3S<.ccccog™2d«d«-'^cS«g3ggc-iQ^«o8d„S2'I.^Q2da2-d2. 'X?ES XdfdO(+ccNN1dd <dXOdo+N1 X<didOc+nn1 oX0dOm+c0id <oXrdo^+-1- <0dr0do+-001- OXddon+cN1d diodOfHnN d00 dXdo+c1d X<dodo+o1 <drdOo+-N1. XdmdCo+cN1d dmo<d+1 <dXdXo+1 dmXXdCo+N1 d<rcdfo+nN-1 d<(dfO+NN1
Distance
Individuals g “.>D °
Agave
2-sl &|
X d G S X
at g ^ g:d > bgOx bgOx bgDx gbJ)x bgOx bgOx
Dead
Characteristics, ganderi S-^ 2 « id-XS X Q < d Q < d Q < d Q < d Q < d Q
the w 5o do 2 X0
cd cn
and C. b&•^? -d2 a
and S S CCd« bp s
0
Living s;
w .^O .O “ d 1 I SP I
Morphological the bigelovii ^5 E^c(/UD D^d) «cyd -^>^s u u
and C. X§ >. >>.6S '2
|S3S|
of
2. d IS S ^ o
and '5 ^ ^iS3 Sa
Table Individuals,Plain K&I.^ed ^d .X> o^ <(>cbiUd}
MADRONO
132 [VoL 61
Table3. MeanPrecipitationandTemperatureforPalm Springsforthe 1954/1955-1963/1964 Seasons
ANDTHE 1994/1995-2003/2004 Rainfall Seasons. Temperatureswerenot included for 1958/59 and 1963/64 due
to insufficient data. Values with different letters within a row indicate a significant difference (P < 0.05) for
Student's t-test. Data are means ± ISE.
1954/1955-1963/1964 1994/1995-2003/2004
Precipitation (mm) 95.0 ± 14.6a 85.0 ± 22.4a
Temperature (°C) 22.1 ± 0.2a 24.0 ± 0.3b
average seasonal rainfallthey received from 1973/ repeated die-offs that likely result from extreme
1974 to 2003/2004 (Table 4). The two seasons drought.
with the lowest precipitation at both sites were The greater susceptibility of C. bigelovii to
1998/1999, with 49.3 rnm received in the flood droughtcomparedwith the othercholla species is
mm
plain and 68.8 at Agave Hill, and 2001/2002, related to its morphology, reproductive mode,
with 57.4 mm received in the flood plain and and low genetic diversity. The shoots of C
mm
67.4 atAgave Hill; thecalendaryearwith the bigelovii almost always had one basal branch
lploawienstrecperievciinpgit2a6t.i9onmmwasand20A0g2,avewiHtihllt3h7e.8fmlomo.d n(toruugnkh),1w96h5i;chTuisrnteypriceatl afohr 1t9h9e5)s.pecTiheuss,(MicfDtoh-e
The average temperature for the 10 seasons trunk fails, thatindividual essentiallydies. Unlike
leading up to this study was over 4°C greater in the other three species, all of which depend on
the flood plain than at Agave Hill (Table 4). sexual reproduction to regeneratepopulations, C
The low temperatures in the flood plain were bigelovii rarely produces viable seeds (Pinkava
never <2°C during the 10 seasons prior to the et al. 1985) and almost solely propagates
study. At Agave Hill, there were three freezing vegetativelyviathe successful rootingofdetached
days, occurring in December 1998 (0.0°C), April stems (Benson 1982; Nobel et al. 1986; Bobich
1999 (0.0°C), and January 2002 (-0.5°C). Each and Nobel 2001). Thus, C. bigelovii likely
freezing day was preceded by and/or followed by experiences acropetal shoot death to allow
days with low temperatures 0-2°C. Overall, there individuals to keep their young stems, which are
were 23 d with low temperatures 0-2°C at Agave their propagules, alive to regenerate their popu-
Hill, with all ofthem occurring during the 1997/ lations. For the other three species that depend
98-2001/02 and 2003-2004 seasons. on sexual reproduction, survival of adults is
importantbecause successful seedlingrecruitment
Discussion of cacti in deserts is rare (Gibson and Nobel
C
1986). Finally, bigelovii appears to be sterile
Thecholla species that experienced the greatest and completely dependent on vegetative repro-
mortality in Deep Canyon duringthe most recent duction because it is triploid (Pinkava and Parfltt
drought was C. bigelovii, with populations 1982; Baldwin et al, 2012) throughoutmuch ofits
decreasing over 50% in the flood plain and over range. As a result, the genetic diversity of C.
25% at Agave Hill, McDonough (1965) reported bigelovii is likely very low, which could make
that C bigelovii experienced greater than 50% certain clones especially susceptible to adverse
mortality in Deep Canyon approximately 40 yr conditions like extreme drought, resulting in
earlier, but did not attribute the mortality to relatively high mortality for this species.
any one factor. Populations of C. bigelovii may Because C. bigelovii reproduces vegetatively
be stable for several decades and individual and its propagules are large (Bobich and Nobel
plants can live over 60 yr (Hastings and Turner 2001), its populations tend to be aggregated
1965). Based on the results of this study and (McDonough 1965), which should lead to in-
McDonough (1965), and the climate leading up creased intraspecific competition. Cylindropuntia
to both studies, it can be assumed that, at least in acanthocarpa, C. echinocarpa and C. ramosissima,
the northwestern Sonoran Desert, the popula- tend to be randomly or regularly spaced and
tions of C bigelovii are dynamic and experience avoid neighboring conspecifics and/or congeners
Table 4. Mean Precipitationand Temperature for the 1973/1974-2003/2004 and 1994/1995-2003/2004
Seasons in the Flood Plain and Agave Hill in the Philip L. Boyd Deep Canyon Research Center.
Yearlyrainfall andmeantemperaturewerecomparedbetweensitesusingpairedt-tests;valueswithdifferentletters
within a row indicate a significant difference (P < 0.05) between the sites. Data are means ± ISE.
1973/1974-2003/2004 1994/1995-2003/2004
Flood plain Agave hill Flood plain Agave hill
Precipitation (mm) 156 ± 17a 193 ± 20b 108 ± 24a 134 ± 26b
Temperature (°C) 23.8 ± 0.2a 20.6 ± 0.2b 24.5 ± 0.3a 20.0 ± 0.5b
2014] BOBICH ET AL.: CHOLLA MORTALITY AND EXTREME DROUGHT 133
(Cody 1986a, b). The aggregated distributions of damage for this species also increases with
C. bigelovii are likely to exist for long periods increasing elevation (Nobel and Bobich 2002).
between extreme droughts, after which extensive One reason for the increased tissue damage at
mortality drives populations towards a more higher elevations compared with lower elevations
randomdistribution, as hypothesized by McDon- may be because C. ganderi stems are less tolerant
ough (1965). Cylindropuntia bigelovii were also of low than high temperatures, suffering 50%
closer to shrubs than the other cholla species in tissue death at —4.9°C and 69.5°C after temper-
the flood plain, reflecting the fact that the species ature acclimation, respectively (Nobel and Bob-
occurs in areas with relatively high plant ground ich 2002); these values are —7.3°C (Nobel 1982)
cover (E. Bobich, unpublished results). Thus, and 59.0°C (Didden-Zopfy and Nobel 1982) for
interspecific competition may have also contrib- C. bigelovii, respectively (Nobel 1988). Further-
C
uted to therelativelyhighmortality ofthis species more, ganderi has a relatively open canopy
in the flood plain. that results in lower shoot temperatures than
The specieswith thelowestpercentmortalityin other cacti (Nobel et al. 1991) and has an
theflood plain was C gander whichwas also the apparent increased need for nurse plants at high
i,
shortest ofthe cholla species; C. ganderialso had elevations (Nobel and Bobich 2002), likely for
a similar number of basal branches to those of protection from freezing temperatures; nurse
the most prolifically branched species, C ramo- plants would not have supplied much cover
sissima. Like C. ramosissima, C. ganderi experi- during the drought because of dieback and
enced basipetal shoot death, reflecting the ten- relative leaflessness. Considering that there were
dency for adults to persist because they likely three freezing episodes at Agave Hill in the seven
reproduce solely from seed (Bobich and Nobel seasons prior to the study, with one being in
2001). Cylindropuntia ganderi did appear to lose January 2002, the driest year on record, it is
fewer stems during the drought than the other possible that drought combined with susceptibil-
species in the study, which is likely because it has ity to freezing and frost damage led to greater
extremely fibrous wood in its terminal stem mortality of C. ganderi at Agave Hill than in the
junctions, whereas the other three species com- flood plain.
pletely lacked fibers in those regions (Bobich and In this study, C ramosissima had the smallest
Nobel 2001). The resistance of C ganderi to stems in terms ofmass and diameter (Bobich and
mortality in the flood plain may be because it has Nobel 2001), making individual stems more
the greatest stem capacitance based on stem susceptible to dehydration (Nobel 1988) than
volume of the four species studied (Bobich and those ofthe other three species due to the lack of
Nobel 2001), and its stems are very tolerant of stem capacitance. Although there was a consider-
high temperatures (Nobel and Bobich 2002). The able amount ofstanding dead and detached dead
effect of how its relatively short height might stems near individuals, mortality was relatively
have contributed to its high survivorship is low(6%) for C ramosissima, whichmaybedueto
unclear, because the difference in height between several factors, including the relatively high
C. ganderi and the other cholla species would number of basal branches and the large canopy
have a small effect on water potential, yet the spread of the individuals. Different branches
relatively low stature and surface area/volume of emanating from the bases of C ramosissima
its shoots could have resulted in it depleting less appeared to respond to the drought differently,
soil water than the other species in the flood with some branches dying completely, while
plain. others survived and produced new stems and
Elevation affected mortality of C. bigelovii and flowers after the winter of 2004/2005, indicating
C C
ganderi differently. Typically, ganderi that this species experiences branch sacrifice
occurs at higher elevations than does C. bigelovii during drought (Rood et al. 2000). The shoots
(Baldwin et al. 2012), which may be related to oflarger C ramosissima appeared to split at the
their relative abilities to establish in colder base, possibly allowing each resulting section to
microclimates. In fact, at Agave Hill C bigelovii act independently of each other, as occurs for
occurs almost exclusively on south-facing slopes, desert shrubs (Schenk 1999). Thus, individual C.
which experience the highest local temperatures, ramosissima may increase their chances of long-
whereas C. ganderioccurs on slopes ofall aspects. term survival by compartmentalizing their shoots
At Agave Hill, mortality for C bigeloviiwas half andstemredundancy. Ofthefourchollaspeciesin
C
ofwhat it was in the flood plain, supporting the this study, ramosissima was the only one that
hypothesis that the lower daily high temperatures apparently experienced shoot splitting.
and greater rainfall at Agave Hill should lead to The low mortality of C ramosissima in the
reduced mortality; however, mortality of C flood plain of Deep Canyon is in contrast with
ganderi was over seven times greater at Agave the response of the species to the drought in
Hill than in the flood plain. Although produc- Joshua Tree National Park, where over 50% of
tivity appears to increase with increases in the adults died between 1999 and 2004 (Miriti
elevation for C. ganderi, the amount of tissue et al. 2007). The difference in mortality of this
MADRONO
134 [Vol. 61
species between the sites may be related to the the Deep Canyon drainage (Kelly and Goulden
fact that the drought was especially severe in 2008). How these predicted changes in climate
Joshua Tree National Park, resulting in massive will affect cholla populations is unclear because
die-offs ofA. dumosa and other subshrubs aswell mortality was low for the sexually reproducing
as the highestmortality observed forL. tridentata species during this drought, which included the
in the Mojave or Sonoran Deserts after the driest year on record, and because each species
drought (McAuliffe and Hamerlynck 2010). appearsto havedifferent adaptationsto dealwith
Furthermore, the site where C ramosissima was prolonged drought. The sexually reproducing
studied (1006 m) was near the elevational limit of species, C echinocarpa, C. ganderi, and C
the species (1100 m; Baldwin et al. 2012) and, as ramosissima, may experience greater changes
C
such, the individuals at that site could have been than bigelovii in elevational range over time
more susceptible to extreme changes in climate. because seedling recruitment should be lower in
Cylindropuntia echinocarpa was the only spe- the predicted future climates, whereas C. bigelovii
cies other than C bigelovii to experience over stems have a large capacitance and can produce
10% mortality in the flood plain. The stems ofC roots readily when exposed to moist soil (Bobich
echinocarpa have a small capacitance compared and Nobel 2001). Thus, although C bigelovii
to those of C. bigelovii and C. ganderi (Bobich individuals clearly experienced the greatest mor-
and Nobel 2001), explainingwhy there were dead tality due to the most recent major drought
stems at the bases of individuals. Cylindropuntia compared with sexually reproducing species, it is
echinocarpa had an intermediate canopy spread not indicative of their relative future success in
and number of basal branches compared to the the northwestern Sonoran Desert.
other three species, meaning that although they
might be able to compartmentalize their shoot Conclusions
mortality, the loss of one basal branch would
result in a loss of40% oftheir canopy compared Cholla species responses to the recent severe
to less than 25% for C. ganderi and C. droughtin thenorthwestern Sonoran Desertwere
ramosissima. Thus, it is likely that the intermedi- related the primary mode ofreproduction, which
ate mortality of C. echinocarpa during the was related, in part, to their morphological
drought is related to its morphology. characteristics, and proximity to othercompeting
Dead individuals did not differ from living plants. Mortalitywas highest in the flood plain at
individuals in morphology or their proximity to Agave Hill for C. bigelovii, which is the only
other chollas or shrubs for any of the cholla cholla species that relied completely onvegetative
species. Juvenile desert shrubs tend to experience reproduction. Because their youngest stems are
C
greater mortality than adults and their mortality their propagules, bigelovii plants sacrificed
isnotrelated to theirrelativedistributionwithina their single trunk, essentially killing the individ-
population (Wright and Howe 1987). Further, uals, to keep their youngest stems alive. Cylin-
seedlings and young juvenile cacti are extremely dropuntia bigelovii also experiences the greatest
susceptible to desiccation (Gibson and Nobel intraspecific competition of the four species
1986). Miriti et al. (2007), who separated plants because its reproductive mode leads to closer
intojuveniles and adults for perennials in Joshua groupings ofindividuals. Individuals ofthe other
Tree National Park, found that juvenile C. three species appeared to sacrifice different parts
ramosissima experienced greater percent mortal- of their shoots for plant survival. Young stems
ity than did adults between 1999 and 2004. died throughout the canopy for C. echinocarpa,
Because the drought was prolonged and there with plants rarely losing entire basal branches,
waslikelylowrecruitmentduringthatperiod, itis whereas terminal stems and entire major branch-
C C
probable that the cholla populations in Deep es died on ganderiand ramosissima, both of
Canyon had few individuals younger than five- which had several major branches; C. ganderi
years-old at the time ofthis study. Thus, even if retainedits stems and responded as a singleplant,
there was selection against younger individuals in whereas all C. ramosissima shed their youngest
Deep Canyon during the drought, it might not stems and thelargestindividuals respondedto the
have been detectable in this study. drought as several independent units. Mortality
Most climate models for the Sonoran Desert for C. bigeloviiwas lower at Agave Hill, which is
indicate the region will be warmer and drier, with cooler and receives more rain than does the flood
droughts being longer and more severe (Weiss plain, whereas mortality for C. ganderi increased
and Overpeck 2005; Seager et al. 2007), which is with increases in elevation, possibly reflecting a
somewhat supported by the 2°C increase in mean susceptibility to low temperature tissue damage
annual temperature in Palm Springs from the during the extreme drought.
1950’s and 1960’s to the most recent drought.
Acknowledgments
Climate has already been cited as the main factor
in the upward change in elevational ranges of We thank Allan Muth and Mark Fisherfor allowing
some of the most prominent perennial plants in us to perform the research at the Philip L. Boyd Deep
.
2014] BOBICH ET AL.: CHOLLA MORTALITY AND EXTREME DROUGHT 135
Canyon Desert Research Center, for sharing their Martin, S. C. and R. M. Turner. 1977. Vegetation
observations of the drought, and for providing the change in the Sonoran Desert region, Arizona and
climatedataforthefloodplainandAgaveHill.Wealso Sonora. Journal of the Arizona Academy of
thank Gretchen B. North for her insightful comments Science 12:59-69.
in the preparation ofthe manuscript. McAuliffe, j. R. and E. P. Hamerlynck. 2010.
Perennial plant mortality in the Sonoran and
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