Variance of Size-Age Curves: Bootstrapping with Autocorrelation Author(s): Stephen H. Bullock, Raymond M. Turner, J.

Rodney Hastings, Martin EscotoRodriguez, Zaira Ramirez Apud Lopez , Jose Luis Rodriguez-Navarro Source: Ecology, Vol. 85, No. 8 (Aug., 2004), pp. 2114-2117 Published by: Ecological Society of America Stable URL: http://www.jstor.org/stable/3450277 Accessed: 01/03/2010 10:26
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Ecology, 85(8), 2004, pp. 2114-2117

? 2004 by the Ecological Society of America

VARIANCE OF SIZE-AGE CURVES: BOOTSTRAPPING WITH AUTOCORRELATION

STEPHEN BULLOCK,1'5 H. RAYMOND TURNER,2 RODNEY M. MARTIN J. ESCOTO-RODRIGUEZ,3 HASTINGS,2 ZAIRARAMIREZ APUD L6PEZ,3AND JOSELUIS RODRiGUEZ-NAVARRO4
'Departamento de Biologia de la Conservacion, Centro de Investigacion Cientifica y de Educaci6n Superior de Ensenada, Apartado Postal 2732, 22800 Ensenada, Baja California, Mexico 2U.S. Geological Survey, 520 North Park Avenue, Tucson, Arizona 85719 USA 3Facultad de Ciencias, Universidad Aut6noma de Baja California, Apartado Postal 1880, 22800 Ensenada, Baja California, Mexico 4Direccion de Telematica, C.I.C.E.S.E., Ensenada, Baja California, Mexico

Abstract. We modify a method of estimating size-age relations from a minimal set of individual increment data, recognizing that growth depends not only on size but also varies greatly among individuals and is consistent within an individual for several to many time intervals. The method is exemplified with data from a long-lived desert plant and a range of autocorrelation factors encompassing field-measured values. The results suggest that age estimates based on size and growth rates with only moderate autocorrelation are subject to large variation, which raises major problems for prediction or hindcasting for ecological analysis or management.
Key words: age-size relations; Fouquieria; growth; population structure; serial autocorrelation; simulation models; uncertainty estimation.

of growth. Its accuracy clearly depends on adequacy of the field sample, particularly in stages where the Size-age curves are important tools for conservative growth rate changes rapidly (the "stratification"), but management of plant and animal populations but are our present concern is with "randomization" of growth difficult to obtain (Martinez-Ramos and Alvarez-Buylrates among similar-size individuals. la 1998). For a typical situation of scarce data, LieIn nature, an individual that has particularly high or berman and Lieberman (1985) developed a bootstrap low growth in one time interval is likely to have simmethod for estimating size-age curves from increment in the next interval. This data for a single interval for marked individuals. Of ilarly high or low growth autocorrelated growth may be due not only to sizecourse the interval between two measurements should related resource capture and allocation, but also to gecorrespond to "typical" environmental conditions so that the increments can be considered typical; thus, an netics, micro-site features that are slowly changing or interval of one "year" is often less preferable than a permanent, or prolonged periods of pest pressure, supor release. These factors vary in transience, single multi-year interval. The Liebermans' method has pression, and probably also in their importance in different guilds been applied to trees in tropical wet and dry forests and environments. Autocorrelation is widely recog(Lieberman et al. 1985a, b, 1988, Korning and Balslev nized as a feature of growth in trees (Cook 1987, Mon1994, Bullock 1995, van Groenendael et al. 1996, Martinez-Ramos and Alvarez-Buylla 1998) but could as serud 1987, Swaine 1989, Sheil 1995, Fox et al. 2001) well be applied to other organisms like sea urchins or and might be expected in any organism where individsnakes. The Liebermans' growth-simulation program uals of similar size and/or age consistently have dif"CRECE" simulates a large number of individuals ferent access to resources for growth. Our studies of over many time intervals based on a stratified-random woody plants in deserts suggest that the effects of geoand slowly changing aspects of the vegprocedure. The increment for an individual in any given morphology etation might result in strong correlation of individual interval is selected from the field data, but the selection is first limited to individuals closest in size to the cur- growth between multi-year intervals (Pierson and Turnrent state of the simulated individual, then an increment er 1998, Escoto-Rodriguez and Bullock 2002). Of is chosen at random from that group. This procedure course, this cannot be measured with data from a single seems quite appropriate for a bootstrap approach, for interval, but the lack of any provision for autocorrethe use of typically nonnormal data (e.g., Kohyama and lation is an important reason that the Liebermans' Hara 1989) and because of the general size dependence growth simulation has not been more widely used (e.g., Clark and Clark 1992). Nonetheless, considerable effort has been applied to received12 August2003;revised9 March 2004; Manuscript understanding long-term population dynamics through 16 March 2004. CorrespondingEditor: B. Shipley. accepted 5 E-mail: sbullock@cicese.mx estimation and hindcasting of age structure. Many studINTRODUCTION 2114

August2004 =0 o AC = 0.3 AC = 0.5 v AC = 0.7 O AC =0.9

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AGE ESTIMATESAND GROWTHAUTOCORRELATION

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Bullock 2002, Ramirez 2002). Although almost the entire range of cirio is within federal conservation areas in Mexico, there is continuing demand to legalize the exploitation of its decorative wood (INE-SEMARNAP 1997), but its regional population declined substantially during the 1900s (Bullock et al., in press). Data for this example come from permanent census and measurement plots that were established in 1963 by J. R. Hastings and R. M. Turner, near Catavifiacito
("LCI"; -29.755? N, 114.749? W, 540 m elevation)

and near the Arroyo Leoncito ("LC2"; -29.092? N, 114.166? W; 430 m elevation), in Baja California, M6xico. We used height measurements made in 1971 and 0 100 200 300 400 500 600 700 800 900 1000 1998, including 95 plants at LC1 (with heights of 7 to 1188 cm in 1971) and 144 plants at LC2 (with heights Median height (cm) of 5 to 1287 cm). The 27-year increments were adjusted FIG. 1. Median age for any given height of cirio at the to an interval of 10 years to facilitate visualization. LC2 site (BajaCalifornia,Mexico), based on 5000 simulated Each data set was used for the simulation of 5000 plants factor(AC). individualsfor each value of the autocorrelation over 400 years. The windows for selection of increments were uniformly 10 individuals. An estimate of ies have used mean growth rates, calculated for size the autocorrelation of growth in cirio has been made groups and/or estimated for any size from nonlinear from field data (0.79; Escoto-Rodrfguez and Bullock regression or spline curve fitting (e.g., among Sonoran 2002), but for this report we have used several values Desert cacti, Shreve 1910, Parker 1988, Pierson and (0.0, 0.3, 0.5, 0.7, 0.9) in order to illustrate the effects Turner 1998). This assumes that variation is not con- of different levels of autocorrelation. sequential and that as time progresses the variation is RESULTS AND DISCUSSION randomly redistributed among similar-size individuals. Other methods are needed where transient changes The median height-age relation for cirio at LC2 (Fig. are prominent in long-term population dynamics (Mar- 1) shows that no autocorrelation consistently gives the tinez-Ramos 1994, Terborgh et al. 1997, Lusk and lowest age estimates for any height, except perhaps for Smith 1998). One alternative approach for estimating plants above 9-m height. The increase in age at any the size-age relation is "individual-based" models height does not appear to be a linear function of the (Botkin et al. 1972, Huston et al. 1988). These incor- autocorrelation (AC) factor: the difference between AC porate generalized growth functions as well as mech- = 0.3 and 0.5 is much less than the difference between anistic details, but require enormous investments to AC = 0.7 and 0.9. However, the maximum difference provide basic data. Such models are useful in studying in age, at any height, between AC = 0 and 0.7 is only directional changes in the environment (Delcourt and about 30 years and this maximum occurs at heights of Delcourt 1991). However, most populations cannot be studied with such intensity, so it would be useful to have extremely simple models that also incorporate -1800AC = : 0 D000 autocorrelation of growth.
1500MATERIALS AND METHODS

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Considering a variety of technical and biological problems in the growth-simulation program CRECE (Lieberman and Lieberman 1985), we developed "CRECERIA," a simpler and more robust program that combines a stratified-random bootstrap with a user-defined autocorrelation of growth (see Supplement). In the present report, we exemplify the effect of autocorrelation on the estimated size-age relation of cirio (Fouquieria columnaris (Kell.) Kell. ex Curran, Fouquieriaceae), a prominent species of the Vizcaino Region of the Sonoran Desert (Shreve 1964). Cirio is known to reach heights in excess of 25 m and age estimates based on growth rates have suggested a longevity of -300 yr or perhaps in excess of 700 yr (Humphrey and Humphrey 1990, Escoto-Rodriguez and

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factor for cirio at the LC2 site. Amage and autocorrelation plitude is the difference between individualsat the 2.5 and 97.5 percentilesfor height.

Amplitude of variation in height for any given

2116
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STEPHENH. BULLOCKET AL.

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Ecology,Vol. 85, No. 8

7-m cirio, the age might range from 110 to 330 yr (LC 1) or 125 to 375 yr (LC2). The two sites differed subO A A A o A A o0 0o 0 o 00 o 0A A 0 A A AA stantially in the behavior of larger individuals, with A 0 A 0 0 A 0 A 0 A 3000 more slowing of growth at LC2, while the difference A 0 0 A 0 A A 0 A 0 0 between fast- and slow-growing plants at LC1 became A A 0 0 A 0 A 0 0 0 0A 0 0 A A 0 A 0 A 0 A 0 0 0 A greater. A OA 0 A0 0 A 0 A 200Considering extremes, we have noted that the tallest OL 0 A OA f A0 A 0 A o LA o 0A AD 0 A reported cirio (>26 m) was estimated to be 713 yr old, 0 A AD A> 0 0OA A A on the basis of population mean growth rates (Hum0 A A AD O0 ?A 0 A o 0 0 A?A > 0 A o LCl? A 0 phrey 1991), but only 208 yr old according to that 100- AD o A o A A LC2o individual's growth rate recorded over 13 years (Es00 Oh 0 0 A A A AO 0 A coto-Rodriguez and Bullock 2002). Growth rates sim4CIO A L . , ilarly far above the population mean have been re-II n . . . . . . . . . . . . . . . . . corded for periods of several decades (Escoto-Rodri900 1200 0 600 1500 300 guez and Bullock 2002), adding credence to the lower Height (cm) age estimate. However, such rates did not occur in our FIG. 3. Median and 95% amplitude limits of age for any samples at LC1 and LC2, so no simulated trajectory given height of cirio at the LC1 andLC2 sites, basedon 5000 approached >20 m in 200 yr. near simulatedindividualswith autocorrelation the field-meaThese results show that individually consistent desuredvalue (AC = 0.7). viations from the population mean growth rate introduce large uncertainties into growth-based estimates of 3 to 5 m while the ages for plants over 8 m tend to age. Even an autocorrelation of 0.3 will soon result in converge (Fig. 1). We should emphasize that these wide confidence limits, which challenges the utility of trends appear without any mortality among the simu- estimated age structures, hindcasted population history, lated individuals. Also, we have shown elsewhere that management plans, or ecological interpretations based the curve for AC = 0 derived from CRECERIA is on growth, age, or history. The effects are simply demessentially the same as the curve derived from a non- onstrated by the application of CRECERIA. Clearly, linear regression model of the height-growth rate re- understanding the population ecology of many sessile or low-vagility organisms will require more attention lation (Ramirez 2002). CRECERIA simulates many individual trajectories, to autocorrelation of growth, as well as to the factors such that population features other than the median or that may account for autocorrelation. mean can be readily examined. We have preferred to ACKNOWLEDGMENTS examine the spectrum of variation that includes 95% We thankRobertH. Webb,J. Mario SalazarCesefia, and of individuals, rather than parametric measures of var- Nora E. Martijena assistancein the fieldwork,which was for iance, because growth rates may be typically nonnor- fundedby CICESEand USGS. mal in any size class, and also nonlinear in relation to LITERATURE CITED size. This amplitude of variation (or difference between D. B., J. E Janak, and J. R. Wallis. 1972. Some the percentiles 2.5 and 97.5) is shown for cirio at LC2 Botkin, ecological consequences of a computer model of forest in Fig. 2. Without or with autocorrelation, the ampligrowth.Journalof Ecology 60:849-872. for tude of variation in height in relation to age is ap- Bullock, S. H. 1995. Estimationof age-size relationships five species of very dry tropicalforest. IAWABulletin 16: proximately a sigmoid curve, with a tendency to take 25. a stable value slightly below the maximum. Both the R. Bullock, S. H., N. E. Martijena, H. Webb,andR. M. Turner. is reached maximum amplitude and the age at which it In press. Twentiethcenturydemographic changes in cirio increase with greater autocorrelation. As with changes and card6nin Baja California.Journalof Biogeography. in the median, the effect of greater autocorrelation is Clark, D. A., and D. B. Clark. 1992. Life-historydiversity of canopy and emergenttrees in a neotropicalrain forest. nonlinear. In the present case, with AC = 0, the max62:315-344. Ecological Monographs imum amplitude is about 3 m at age <90 yr, but with Cook, E. R. 1987. On the of dis-aggregation tree-ringseries AC = 0.7 the amplitude reaches 7 m at roughly 200 studies. Pages 522-542 in G. C. Jacoby, for environmental Jr., and J. W. Hornbeck,editors. Proceedingsof the interyr of age. Despite the rather small effect on the median, analnationalsymposiumon ecological aspectsof tree-ring autocorrelation clearly can have a substantial effect on Proof ysis. U.S. Department Energy,U.S. Environmental variability and thus on the utility of age estimates based tection Agency, and USDA Forest Service, Washington, on regression analysis of growth. D.C., USA. ecolFig. 3 shows the application of CRECERIA to the Delcourt,H. R., and P. A. Delcourt. 1991. Quaternary characterization of the height-age relation for cirio at ogy: a paleoecological perspective. Chapmanand Hall, London,UK. LC1 and LC2. Taking the 95% criterion as our "conM., Escoto-Rodrfquez, and S. H. Bullock. 2002. Long-term the
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age of a 1-m cirio could be between 20 and 140 yr at LC1, with only a slightly smaller range at LC2. For a

growth rates of cirio (Fouquieria columnaris), a giant suc-

of culent of the SonoranDesert in Baja California.Journal 50:593-611. Arid Environments

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Fox, J. C., P. K. Ades, and H. Bi. 2001. Stochastic structure and individual-tree growth models. Forest Ecology and Management 154:261-276. Humphrey, R. R. 1991. Montevideo Valley and its tallest recorded cirio. Cactus and Succulent Journal 63:239-240. Humphrey, R. R., and A. B. Humphrey. 1990. Idria columnaris: age as determined by growth rate. Desert Plants 10: 51-54. Huston, M. A., D. L. DeAngelis, and W. Post. 1988. New computer models unify ecological theory. BioScience 38: 682-691. INE-SEMARNAP [Instituto Nacional de Ecologia, Secretaria de Medio Ambiente, Recursos Naturales y Pesca]. 1997. Programa de conservaci6n de la vida silvestre y diversificaci6n productiva en el sector rural 1997-2000. Instituto Nacional de Ecologia, Secretaria del Medio Ambiente, Recursos Naturales y de Pesca, M6xico, D.F, M6xico. Kohyama, T., and T. Hara. 1989. Frequency-distribution of tree growth-rate in natural forest stands. Annals of Botany 64:47-57. Korning, J., and H. Balslev. 1994. Growth rates and mortality patterns of tropical lowland tree species and the relation to forest structure in Amazonian Ecuador. Journal of Tropical Ecology 10:151-166. Lieberman, D., M. Lieberman, G. S. Hartshorn, and R. Peralta. 1985a. Growth rates and age-size relationships of tropical wet forest trees in Costa Rica. Journal of Tropical Ecology 1:97-109. Lieberman, D., M. Lieberman, R. Peralta, and G. S. Hartshorn. 1985b. Mortality patterns and stand turnover rates in a wet tropical forest in Costa Rica. Journal of Ecology 73:915-924. Lieberman, M., and D. Lieberman. 1985. Simulation of growth curves from periodic increment data. Ecology 66: 632-635. Lieberman, M., D. Lieberman, and J. H. Vandermeer. 1988. Age-size relationships and growth behavior of the palm Welfia georgii. Biotropica 20:270-273. Lusk, C. H., and B. Smith. 1998. Life history differences and tree species coexistence in an old-growth New Zealand rain forest. Ecology 79:795-806. Martinez-Ramos, M. 1994. Regeneraci6n natural y diversidad de especies arb6reas en selvas hdmedas. Boletin de la Sociedad Botanica de M6xico 54:179-224.

Martfnez-Ramos, M., and E. Alvarez-Buylla. 1998. How old are tropical rain forest trees? Trends in Plant Science 3: 400-405. Monserud, R. A. 1987. Time-series analysis applied to treering series. Pages 554-565 in G. C. Jacoby, Jr., and J. W. Hornbeck, editors. Proceedings of the international symposium on ecological aspects of tree-ring analysis. U.S. Department of Energy, U.S. Environmental Protection Agency, and USDA Forest Service, Washington, D.C., USA. Parker, K. C. 1988. Growth rates of Stenocereus thurberi and Lophocereus schottii in southern Arizona. Botanical Gazette 149:335-346. Pierson, E. A., and R. M. Turner. 1998. An 85-year study of saguaro (Carnegiea gigantea) demography. Ecology 79: 2676-2693. Ramirez Apud L6pez, Z. 2002. Modelos del crecimiento para la estimaci6n de la edad con aplicaci6n en el cirio (Fouquieria columnaris). Thesis. Facultad de Ciencias, Universidad Aut6noma de Baja California, Ensenada, Baja California, M6xico. Sheil, D. 1995. A critique of permanent plot methods and analysis with examples from Budongo Forest, Uganda. Forest Ecology and Management 77:11-34. Shreve, F 1910. The rate of establishment of the giant cactus. Plant World 13:235-240. Shreve, F. 1964. Vegetation of the Sonoran Desert. Pages 9186 in F Shreve and I. L. Wiggins, editors. Vegetation and flora of the Sonoran Desert. Stanford University Press, Stanford, California, USA. Swaine, M. D. 1989. Population dynamics of tree species in tropical forests. Pages 101-112 in L. B. Holm-Nielsen, I. C. Nielsen, and H. Balslev, editors. Tropical forests: botanical dynamics, speciation and diversity. Academic Press, London, UK. Terborgh, J., C. Flores, P. Mueller, and L. Davenport. 1997. Estimating the ages of successional stands of tropical trees from growth increments. Journal of Tropical Ecology 13: 833-856. Van Groenendael, J., S. H. Bullock, and L. A. Perez-Jim6nez. 1996. Aspects of the population biology of the gregarious tree Cordia elaeagnoides in Mexican tropical deciduous forest. Journal of Tropical Ecology 12:11-24.

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SUPPLEMENT CRECERIA, a program for estimating size-age relations, is available in ESA's Electronic Data Archive, EcologicalArchives: E085-062-S 1.