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Abstract-Ocotillo is a drought-deciduous desert shrub capable of orchestrating rapid morphological and physiological adjustments to changes in environmental conditions. Lengths of over 2.500 stem segments from two populations of ocotillo growing in the Chihuahuan
Desert were measured to explore the possibility that episodes of stem growth could be used to infer past environmental change. Stem growth was so intermittent and complex that historical projections of environmental conditions were not possible without first establishing benchmark stem segments. Once established though, benchmark stem segments and subsequent stem growth may be used as easily measurable integrators of ongoing environmental change in desert ecosystems.
Reconstructing past environmental changes with dendrochronological techniques has been highly successful in forest ecosystems (Fritts 1976; Fritts and Swetnam 1989), yet arid ecosystems typically lack an abundance of perennial species replete with measurable growth rings. Notable exceptions include
(Ferguson 1964),
(Flinn and others 1994), and several species of chaparral shrubs (Keeley 1993), but few true desert endemics produce growth rings that are both measurable and interpretable. Anomalies such as "false rings" and "missing rings" (Fritts and Setnam 1989; Keeley 1993) that can obliterate attempts at correlating growth rings with climatic change are especially problematic for plant species growing in the highly variable climatic regimes common to most deserts.
Ocotillo
Engelm.), a drought-deciduous shrub endemic to the Chihuahuan and Sonoran
Deserts of North America, produces terminal segments on its stems that clearly demarcate pulses of growth
(Hendrickson 1977). Segments are separated from one another on the same stem by obvious nodal "seams" that remain intact for the life of the stem. Thus, a separate chronosequence of growth episodes is available for measurement on every stem of an ocotillo plant.
Such a record of growth could be invaluable as a nondestructive phytometric means of tracking environmental change in the Chihuahuan and Sonoran Deserts. However, several prerequisites must be met before ocotillo stem growth can serve in this capacity.
First ocotillo must be capable of making physiological and
adjustments to interyear changes in environmental conditions. The capacity for significant interyear change was demonstrated in 1989 when resorption ?f ~tro­ gen from senescing ocotillo leaves was more than sIX tImes higher than that measured in the same plants three years before (72% versus 11% resorption, respectively; Killingbeck
1992 1993). Additionally, interyear changes in stem growth have 'been documented in a population of ocotillo growing in the
Desert (Darrow 1943).
Second, the years in which stem segments are produced must be ascertainable. Evidence from the Sonoran Desert near Tucson, Arizona, suggests that the ages of extant segments may not be associated with a specific age be~a~se of "missing segments" (Darrow 1943) analogous to "missmg growth rings." Further, because temperatures are relatively warm throughout the year and precipitation is distinctly bimodal in the eastern portion of the Sonoran Desert encompassing the Tucson area (Shreve 1951), ocotillo stems may even produce "false segments." On the contrary, the
Chihuahuan Desert in New Mexico has but a single period of significant precipitation each year during the summer, thus increasing the possibility that ocotillo stems would produce only one segment each year. The consistent production of one segment per stem per year by ocotillos growing in
New Mexico would enable the dating of stem segments, thus meeting the second prerequisite.
The primary goal of this contribution is to explore the efficacy of utilizing stem segment growth patterns in ocotillo to infer past environmental change, and to monitor ongoing environmental change in the Chihuahuan Desert. The specific questions I will attempt to answer include: (1) What are the relationships in length among the six uppermost segments of ocotillo stems between populations and within individual plants? (2) Is the presence or absence of new stem segments in a given year uniform among stems of the same plant, or among individuals in the same population? (3) Is it possible to determine the year in which unmarked, extant ocotillo stem segments were produced? (4) Do the number and length of newly produced stem segments in ocotillo differ between years or populations? (5) Are differences in stem segment production between years and between populations large enough to be useful in tracking environmental change?
In: Barrow, Jerry R.; McArthur, E. Durant; Sosebee, Ronald E.; Tausch,
Robin J., comps. 1996. Proceedings: shrubland ecosystem dynamics in a changing environment; 1995 May 23-25; Las Cruces, NM. Gen. Tech. ~p.
INT-GTR-338. Ogden, UT: U.S. Department of Agriculture, Forest SeJ'Vlce,
Intermountain Research Station.
Keith T. Killingbeck is Professor of Botany, Department of Biological
Sciences, University of Rhode Island, Kingston, RI 02881.
224

Methods
Stem segment production was measured in 1993 and 1994 in two populations of ocotillo, one growing in the foothills of the Organ Mountains and another in the Jornada Long
Term Ecological Research (LTER) Area. Both sites are located in the northern reaches of the Chihuahuan Desert in southern New Mexico and are less than 30 km apart. The
Organ Mountains site (32°19' N, 106°38' W) lies approximately 11 km east of Las Cruces, New Mexico, and is characterized by rocky soils and moderate slopes. The Jornada LTER site (32°30' N, 106°48' W) lies within the New
Mexico State University Jornada Experiment Range 20 km north of Las Cruces and is also characterized by rocky soils and moderate slopes.
In June 1993, the lengths of the terminal six growth segments (fig. 1) were measured on the stems of 12 plants in the Organ Mountains, and 23 plants in the Jornada LTER site. Stems less than 150 cm long were excluded from analysis as were stems that were branched in their terminal meter of length or that had obvious morphological defects.
Each segment was measured separately and segregated according to its relative position within the sequence of six terminal segments. In the Organ Mountains, all stems fitting the above criteria were measured (193 stems, 1,158 segments) whereas in the Jornada LTER site, sampling was limited to ten stems per plant (228 stems, 1,368 segments; two plants had only nine stems each that met the above criteria). Because stem segments are not produced in these populations until July-August, measurement of the terminal segments in June reflected stem growth through 1992.
The most recently produced stem segment on each stem of
11 of the 12 study plants at the Organ Mountains site was marked with red nail polish in June 1993 so as to be able to identify future stem growth. In late May 1994, all new stem segments produced after June 1993 were located, tagged with color-coded pipe cleaners, and measured (length). The most recently produced stem segment on each stem of the previously unmarked plant was also tagged with a pipe cleaner. In early September 1994, all new stem segments produced on all 12 study plants after May 1994 were located, tagged with color-coded pipe cleaners, and measured (length).
All stem segments produced during 1994 on the 23 study plants at the Jornada LTER site were located, tagged with color-coded pipe cleaners, and measured (length) in early
September 1994. None of the segments on these plants had been marked previously, yet new segments bore leaves that clearly identified the segments as newly produced. Because primary leaves only occur on newly produced stem segments and differ significantly in appearance from secondary leaves, segments holding primary leaves are easily identified as newly produced segments. However, because primary leaves can be dropped from a segment in the same growing season in which they were produced (petiole tissue is retained and develops into the stem spines characteristic of this species) and replaced by secondary leaves, the absence of primary leaves on a stem segment does not necessarily indicate that the segment was produced in years past (personal observation).
The number of stems on each plant of both populations was measured in April 1995.
All 35 plants used in this study are also part of another study begun in 1989 to test the effects of trace metal fertilization on the resorption of nitrogen from senescing ocotillo leaves. Because fertilization treatment effects did not affect the outcome ofthe stem segment analyses, data for treatments and controls were not segregated in this paper.
To estimate the percentage of stems on each plant that produced new stem segments in a given year, I divided total number of stems per plant by total new segments produced in a specific year. Given the fact that a small number of stems produced terminal and lateral segments in a given year (i.e. more than one new segment per stem per year), the values presented (table 1) slightly overestimate the percentage of stems producing new segments in 1993 or 1994.
All statistical analyses were completed with SYSTAT software (Wilkinson 1992) on Macintosh computers. Normality of data distribution was determined with the Lilliefors test. When the assumption of normality was not met, the
Kruskal-Wallis test was used to establish probabilities of difference among three or more means, and the Mann-
Whitney U-test was used to determine whether pairs of means were statistically different. When the assumption of normality was met, Student's t-test was used to determine whether pairs of means were statistically different. Correlation analyses were all performed with the Pearson correlation statistic.
TERMINAL SIX STEM
SEGMENTS,
NUMBERS 1-6
Figure 1-Diagram of terminal ocotillo stem segments
(numbers 1-6) measured in this study.
225
Mean segment length in the terminal six ocotillo stem segments varied from 14.0-16.6 cm in the Organ Mountains and 12.0-17.0 cm at the Jornada site (table 1). Segments 3,
4, and 5 of both populations were the shortest segments, and segments 1 and 2 were the longest. Ranges of stem segment lengths were remarkably large. Lengths of stem segment 5 varied from 1-41 em in the Organ Mountains and lengths of stem segment 1 varied from 1-44 cm at the Jornada site.
Even for the segment with the smallest range in lengths
(segment 4, Organ Mountains) there was more than a

Table 1-Length of the terminal six stem segments growing on 193 ocotillo stems in the foothills of the Organ Mountains, and 228 stems in the Jornada
L TER site (mean and range, cm). Segment number '1' was the uppermost segment on each stem in spring 1993, and segments '2-6' followed in sequence down each stem. SE = standard error of the mean.
Organ Mountains
Segment Length SE Range
1
2
3
4
5
6
16.6
15.8
14.0
14.6
15.4
15.7
0.5
0.5
0.4
0.4
0.5
0.5
1.3-35.6
1.3-38.1
1.3-38.1
2.5-35.6
1.3-40.6
2.5-40.6
Jornada L TER site
Length
16.3
17.0
12.0
13.3
12.7
14.0
SE
0.5
0.6
0.4
0.5
0.4
0.4
Range
1.3-44.5
1.3-41.9
1.3-35.6
1.3-43.2
1.3-30.5
1.3-35.6
14-fold difference between the shortest and longest individual segments.
Variability in segment lengths was also extremely high in different stems growing on the same plant. Data from plant
#19 at the Jornada site are representative of this high variability (fig. 2). The uppermost segment on stem 5 (33.0 cm) was 8.7 times longer than the uppermost segment on stem 10 (3.8 cm). Lengths of segment 5 were the most uniform, but even the longest (on stem 4) and shortest (on stem 1) number 5 segments differed by a factor of 2.5.
Patterns of segment growth were also dissimilar among
120
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W
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SEGMENT ON END =
OFSTEM
1 2 3 4 5 6 7 8 9 10
Figure 2-Lengths (cm) of the terminal six segments of
10 stems growing on one ocotillo (#19) at the Jornada
LTER site. The uppermost, cross-hatched sector of each bar represents the most terminal segment on each stem, and the remaining sectors follow in sequence down the stems. Data for this plant were representative of the variability in stem segment growth displayed by all plants. stems. For example, segment rankings in descending order by length were 3 > 6 > 1 > 4 = 5 > 2 for stem 7, and 6 > 2 > 1
=
5> 4 > 3 for stem 9. Segment 3 was both the longest and shortest of the terminal six segments on different stems.
Differences in growth among stems were also appreciable when considered for periods of time greater than one growing season. Because the number of terminal stem segments produced by any stem of the 40 study plants in a given year was either one or none (i.e. never two or more, unpublished data), the combined lengths of the six terminal segments on each stem in figure 2 represent a minimum of six years of growth. Over this period of time, terminal growth of the fastest growing stem (stem 7, 95.3 cm) was twice that of the slowest growing stem (stem 10, 43.2 cm).
New stem segments produced in 1993 and 1994 suggest the presence of yet another tier of complexity inherent in ocotillo growth (fig. 3). Individuals in both populations of
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50
0
10%
81%
1993
ORGAN MOUNTAINS
1994
JORNADA L TER
Figure 3-Percentage of stems on ocotillo plants that produced new stem segments at the Organ Mountains site (1993 and 1994) and the Jornada L TER site (1994).
Values are means of individual plant percentages at each site in each year and are displayed within the shaded boxes. Ranges are indicated in the attached, unshaded boxes. The minimum percentage for the
Organ Mountains population in 1994 was 0%. All means are statistically different from one another (P < 0.01;
Mann-Whitney U-test).
226

ocotillo varied widely in the percentage of their stems that produced new segments. In 1993, 10-73% of the stems on individual plants growing in the Organ Mountains produced new growth. The range in percentages declined to 0-22% in
1994, but was 0-81% among individuals at the J ornada site in this same year. Therefore, in some years it is possible to find plants with no new terminal stem growth growing adjacent to plants with new terminal growth on the majority of their stems.
Mean percentages of stems with new growth differed significantly between years and sites (Organ Mountains
1994 < Jornada 1994 < Organ Mountains 1993, P < 0.01,
Mann-Whitney U-test)in spite of the high variability among individual plants (fig. 3).
Both the number of new segments produced per plant and the total length of new segments produced per plant were lower in the Organ Mountains population in 1994 than in the same population one year earlier, or than in the Jornada population during the same year (table 2; P < 0.001, Mann-
Whitney U-test). The total length of terminal stem growth per individual was seven times lower in the Organ Mountains population in 1994 than in the same population one year earlier, or than in the Jornada population during the same year.
To compensate for the fact that plants in the Organ
Mountains had fewer stems (36 stems/plant, SE = 2.9) than plants at the Jomada site (50 stems/plant, SE = 4.6; P <0.05,
Student's t-test), lengths of new segments per plant were divided by the total number of stems per plant to produce a standardized measure of segment production (fig. 4). This analysis revealed that not only was new stem segment length lower in the Organ Mountains in 1994 than in 1993 or than at the Jornada site in 1994, but that plants in the
Organ Mountains produced more new stem tissue in 1993 than did plants at the Jornada site in 1994 (P <0.05, Mann-
Whitney U-test).
Data expressing the number of new stem segments produced as a function of total number of stems per plant (fig. 3; for example, 48 new segments per 100 stems were produced in the Organ Mountains population in 1993) indicate that as with stem segment lengths, numbers of stem segments were lower in the Organ Mountains in 1994 than in 1993 or than at the Jornada site in 1994 on a per stem basis.
Discussion
Tier after tier of complexity characterized stem segment growth patterns in populations of ocotillo growing in the northern reaches of the Chihuahuan Desert. Stem segment i'
5.0 e. w
I-
~ w
:::E fa
2.5
~ z
LL o i!=
...J
0
1993 1994
ORGAN MOUNTAINS
Figure 4-Means of the length (cm) of new stem segmtilnts produced per plant at the Organ Mountains site (1993 and 1994) and the Jornada L TER site (1994) divided by the total number of stems per plant. New growth was divided by total stems per plant to minimize differences in stem segment production that may have been a function of plant size and/or age as estimated by the total number of stems per plant. Error bars represent the standard error of the mean. All means are statistically different from one another (P < 0.05; Mann-Whitney U-test).
1994
JORNADA L TER production varied markedly between years (table 2, figs. 3,
4), between populations growing less than 30 km apart
(table 2, figs. 3,4), among individuals of the same population
(fig. 3), and even among different stems growing on the same plant (fig. 2). While such complexity poses problems for using unmarked, extant stem segments to infer past environmental change, it also offers opportunities for using new growth to track environmental change.
The key to the effective use of ocotillo stem growth in tracking environmental change is the identification of an initial set of benchmark segments. Once a set of uppermost stem segments has been permanently marked, growth can be measured at any time interval deemed appropriate to the questions asked. Uppermost stem segments simply need to be marked at the end of each sampling interval to allow monitoring to continue into the future. Because maximum
Table 2-Mean total length (cm) and number of new stem segments produced per plant in 1993 and 1994 in the foothills of the Organ Mountains and in the Jornada
L TER site. Parentheses contain standard error of the mean. Means with an asterisk are statistically different from all other means in the same row
(P < 0.001; Mann-Whitney U-test).
Length of new stem segments (cm)
Number of new stem segments
Organ Mountains
1993 1994
142 (16)
15.2 (1,8)
20* (8)
1.9* (0.7)
Jornada L TER
1994
147 (30)
12.5 (1.8)
227

age in ocotillo is probably 150-200 years (Darrow 1943), a wide range of time increments are possible for analysis.
The opportunities for using stem segment production to monitor environmental change appear to be considerable given the large differences in growth measured between individuals, populations, and years (table 2, figs. 3,4) in a period of time as short as two years. These differences in growth imply a sensitivity to environmental parameters that is essential if growth is to be used successfully as a phytometric measure of a changing environment. AB in any organism, growth of any kind is also a function of internal, biotic regulation and allocation. However, distinct patterns of growth that emerge simultaneously over time in separate populations of ocotillo would signify environmental change.
Changes including those spawned by such processes as desertification and global warming should all be susceptible to detection and measurement with ocotillo stem segment analysis.
Compared to other desert species and other methods of relating growth to environmental conditions, stem segment analysis in ocotillo has several distinct advantages.
First, analysis is nondestructive and therefore conducive to repeated application on known individuals. Growth ring measurement in the few desert shrubs that can support such analysis is, by necessity, destructive (for example, Flinn and others 1994; Keeley 1993).
Second, ocotillo stem segments are so clearly marked by obvious nodal seams that their lengths can be measured with high accuracy and precision. Nodes are particularly distinctive in the upper two-thirds of each stem, but even lower segments are usually visible and distinct.
Third, because the number of stems per ocotillo individual is small (usually 1-50; Humphrey 1935) and each stem is quite distinct, measurements can be made on every stem of a study plant thus integrating stem growth throughout the individual. While it is possible to measure all stem growth in a given year on common desert perennials such as creosotebush (Larrea tridentata) and mesquite (Prosopis spp.), the effort expended to do so compared to the analogous effort necessary in ocotillo would be considerable.
Fourth, measurements can continue year after year because ocotillo segments are produced terminally in sequence and are not subject to abscission during periods of drought.
Fifth, stem segment analysis in ocotillo can provide highly detailed data on short-term environmental events not accessible by techniques valuable in the analysis of long-term changes in climate and vegetation. For example, packrat middens have proved to be valuable repositories of plant materials from which long-term changes in vegetation and environment may be discerned (Betancourt and others 1990), yet highly detailed short-term changes can not be discerned from midden materials.
While the possibilities for using ocotillo to track future environmental changes are appealing, the apparent inability to use unmarked, extant stem segments to infer past changes is disappointing. The extreme variability in segment production among stems on the same plant (figs. 2, 3) would seem to completely obliterate any segment length patterns that might be useful in assigning dates of production to specific segments. Techniques analogous to crossdating in dendrochronology (matching variations in width of growth rings among trees to determine the year in which individual rings were produced; Fritts 1976) have not been rigorously applied yet to ocotillo stem segment length data, but the probability that such techniques will be successful in associating dates of production with segments appears to be low given the high degree of complexity inherent in ocotillo stem growth. Nevertheless, this approach should be tried.
One additional variation on the crossdating approach is to use the number of spines per unit length of segment rather than just segment length in correlation analysis. Because each spine on an ocotillo stem is formed from petiole tissue produced by each primary leaf (Hendrickson 1977; Scott
1932), there is a one-to-one relationship between ephemeral primary leaves and permanent stem spines. If the number of primary leaves produced per unit length of stem segment varies from year to year, it might be possible to at least identify all segments on a plant that were produced in a given year. These cohorts of associated segments might then form the basis for further cross-correlational analyses. For example, it might be possible to link mean lengths of segment cohorts to specific years in which precipitation was either abnormally high or low, thus allowing the assignment of dates to specific stem segments. The possibility of using stem spines as permanent markers of growth is tantalizing, but its potential is presently unknown.
Conclusions
In considering the efficacy of utilizing stem growth in ocotillo to track environmental change, there is a clear dichotomy between the utility of measuring the length of unmarked, extant stem segments, and the utility of mea suring the length of stem segments produced after the establishment of benchmark segments. Unmarked, extant stem segments can not be assigned ages, or even be grouped into cohorts that were produced in the same year, and therefore can not be used to infer past environmental change. Conversely, segments produced after age-specific benchmarks have been established can be assigned dates of production and therefore, can be used to track ongoing environmental change.
Factors including the ease and accuracy with which the length of ocotillo stem segments can be measured, the nondestructive nature of stem segment analysis, and the potential sensitivity of ocotillo to environmental changes as evidenced by large differences in stem segment production between populations and years, collectively suggest that monitoring stem segment growth in ocotillo can be an effective method for tracking environmental change.
I thank Rich Spellenberg and the New Mexico State University Department of Biology for graciously providing space and technical support, Walt Whitford for insightful comments and unfailing enthusiasm, John Anderson for invaluable logistics support and baseline site information, and
Susan Killingbeck for superb field assistance. Primary financial support was provided by a grant from the University of Rhode Island Alumni Association. Earlier support from the National Science Foundation (BSR-8604421) set the stage for the development of stem segment analyses in ocotillo.
228

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