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Interaction of Diffuse Competition and Insect Herbivory in Limiting Brittle Prickly Pear Cactus, Opuntia Fragilis (Cactaceae)

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Interaction of Diffuse Competition and Insect Herbivory in Limiting Brittle Prickly Pear Cactus, Opuntia Fragilis (Cactaceae) University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Svata M. Louda Publications Papers in the Biological Sciences 1995 Interaction of Diffuse Competition and Insect Herbivory in Limiting Brittle Prickly Pear Cactus, Opuntia fragilis (Cactaceae) Jutta C. Burger University of Nebraska - Lincoln Svata M. Louda University of Nebraska - Lincoln, [email protected] Follow this and additional works at: https://digitalcommons.unl.edu/bioscilouda Part of the Ecology and Evolutionary Biology Commons Burger, Jutta C. and Louda, Svata M., "Interaction of Diffuse Competition and Insect Herbivory in Limiting Brittle Prickly Pear Cactus, Opuntia fragilis (Cactaceae)" (1995). Svata M. Louda Publications. 2. https://digitalcommons.unl.edu/bioscilouda/2 This Article is brought to you for free and open access by the Papers in the Biological Sciences at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Svata M. Louda Publications by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. American Journal of Botany 82(12): 1558-1566. 1995. INTERACTIONOF DIFFUSE COMPETITION AND INSECT HERBIVORY IN LIMITING BRITTLE PRICKLY PEAR CACTUS, OPUNTIAFRAGILIS (CACTACEAE)~ JUTTAC. BURGER^ AND SVATAM. LOUDA~ School of Biological Sciences and Cedar Point Biological Station, University of Nebraska-Lincoln, Lincoln, Nebraska 68588-0343 We tested the effects of above- and belowground competition and evaluated insect herbivory on the growth of a common cactus (Opuntia fragilis) in Sandhills prairie. Our purpose was to determine the independent and joint contribution of these factors to the variation observed in cactus size and local abundance. We manipulated ambient prairie vegetation and surface water availability in a full factorial design. When Opuntia fragilis was released from competition with surrounding vege- tation, it grew significantly larger in the second growing season, both in terms of number and size of new cladodes. Ramets grown within live prairie vegetation averaged no net growth. These ramets were also more frequently fed upon by the larvae of two internally feeding cactus insects. As a result, insect herbivory reinforced the competitive suppression of the cactus by grasses. Water supplementation had no significant effect, either on cactus growth or on insect herbivory. We conclude that the mechanism by which dense prairie vegetation influenced net growth of 0. fragilis was both direct, through com- petition for nonwater resources such as light, and indirect, through its mediation of feeding by specialized insect herbivores. Furthermore, since the direct growth response to treatment did not precede the indirect effect of habitat-mediated variation in feeding by insects, our results contradict the current expectation that indirect effects require more time to be expressed than do direct effects. Competition can be intense in water-limited grassland for vegetation influence on cactus growth and distribu- ecosystems, and water availability can strongly influence tion. In this study, we experimentally examined both di- plant community composition (Weaver and Albertson, rect and indirect effects of prairie grasses on prickly pear 1936; Lauenroth, Dodd, and Sims, 1978; Lauenroth, growth and propagation. 1979; Barnes and Harrison, 1982). The standing biomass The influence of water on the abundance of prickly of grasses often correlates strongly with mean annual pear cacti is not clearly understood. As succulents, cacti rainfall, especially where soils have limited water-holding can store relatively large amounts of water and are there- capacity (Sala et al., 1988), such as in Sandhills prairie. fore able to endure long periods of drought (Nobel, Prickly pear cacti (Opuntia spp.) occur throughout the 1988). Additionally, as plants with crassulacean acid me- Great Plains grasslands. Increases in their densities have tabolism (CAM), photosynthesis entails lower daytime been recorded during and after severe droughts (Cook, transpiration rates than those of most other grassland 1942; Bement, 1968; Hyder et al., 1975), suggesting that plants (Szarek and Ting, 1975; Nobel, 1977). Prickly pear competition with grasses may suppress cacti and directly cacti, such as the small brittle prickly pear (Opuntia fra- limit their densities. gilis) that is indigenous to the Sandhills of Nebraska, Several studies have shown that the dense grass can- have extremely shallow roots (Burger, 1994). These roots opies produced in response to heavy rainfall are also as- seldom penetrate below the top 10 cm of soil. The dis- sociated with decreased densities of Opuntia spp. (Hyder tribution of roots of cacti in the soil in general reflects et al., 1975; Dougherty, 1986). However, the mechanism the distribution of soil moisture for most cacti and for for this shift in abundance is not clear. Competition, be- Agave (Nobel, Miller and Graham, 1992). Additionally, lowground for water or nutrients or aboveground for precipitation stimulates production of "rain roots" in light, could be directly limiting the cacti. Alternately, in- many cacti (Nobel, 1988). Temporary increases in clad- creases in grass canopy density could lead to increased ode thickness have been measured in 0. polyacantha herbivore load (Cook, 1942; Louda, Keeler, and Holt, 1990; Burger and Louda, 1994). No experimental data cladodes after simulated rainfall events of as little as 2.5 yet simultaneously assess these alternative mechanisms mm (Dougherty, 1986). Therefore, Opuntia are able to absorb water from light rains that are virtually inacces- sible to more deeply rooted grasses. I Manuscript received 8 December 1994; revision accepted 16 May No strong correlation between precipitation and growth 1995. or density of Opuntia has been found to date. Yet, studies Present address: Department of Entomology, University of Califor- nia-Riverside, Riverside, California 9252 1-0314. have shown that water augments physiological and de- Author for correspondence. velopmental processes. Irrigation increases nighttime up- The authors thank A. Joern and K. l? Pmess for advice on methods take of CO, (Hanscom and Ting, 1977; Koch and Ken- and comments on the manuscript; K. Laumans, D. Lynch, and R. W. nedy, 1980; Ehleringer and Cooper, 1988; Goldstein et Otley for help in the field or with equipment, and The Nature Conser- al., 1991). Also, soil moisture can be critical for at least vancy for use of Arapaho Prairie. This research was partially funded by the Jessie A. Lee award to J. B. from the University of Nebraska, Lin- one stage in the life history of succulents: germination coln, and equipment from National Science Foundation grant BSR85- and establishment from seed (Jordan and Nobel, 1982; 16515 to S.M.L. Nobel, 1988). Water availability may therefore contribute Copyright 1995 Botanical Society of America. Used by permission. December 19951 BURGERAND LOUDA-COMPETI Watered Unwatered TABLE1. Initial repeated-measures analysis of variance for the cu- I mulative effects of competition and water on net growth of Opuntia :: fragilis. Growth measurements were square-root transformed prior T .. Live vegetation, to analysis. Whole-plot treatments were: I) ambient live vegetation; 1 " unclipped 11) dead vegetation, clipped in 1993; or 111) dead vegetation, clipped in 1992. Split-plot treatments were: watered weekly; or unwatered. 1 Source of transplants, from either greenhouse or field, was initially treated as a split-split-plot factor (T = time, R = replicate, V = vegetation, W = water, and S = source of transplant). Vegetation killed, Source of variation df MS F <P clipped late Time X Replicate 52 0.975 2.24 0.01 Time X Vegetation 8 3.908 8.99 0.01 Error 1 [T X V X R] 104 0.435 Vegetation killed, X 4 0.064 111 clipped early Time Water 0.15 0.97 T TXVXW 8 0.320 0.77 0.64 1 m Error 2 [T X R X W(V)] 156 0.417 Time X Source TXSXV TXSXW Error 3 [TI Fig. I. Split-plot design for a replicate block (N = 14) in which both competing vegetation and water availability were manipulated. Two ramets were planted into each split-plot on 8-10 June 1992. A pressure as grass cover increased. He, and several others third ramet was added to the experiment on 22 May 1993, but results since (e.g., Bugbee and Riegel, 1945; Houston, 1963; regarding the added ramets are not presented here. In early 1993, veg- Myers, 1981) hypothesized that dense grass cover pro- etation treatment I1 was clipped to resemble treatment 111. The unve- vided more favorable microhabitat for the insect herbi- getated treatments (I1 and 111) were not significantly different, and, thus vores of Opuntia. One recent experiment provides sup- were pooled for statistical analysis of cumulative effects (see Methods and Table 1). port for this hypothesis (Burger and Louda, 1994). Al- though many studies have suggested this phenomenon as a possible controlling factor for Opuntia populations (Dodd, 1940; Dougherty, 1986), few have quantified in- to limiting the distribution of some species of cacti in sect herbivory on study plants in relation to competitive deserts (Tschirley and Wagle, 1964; Jordan and Nobel, context (but see Houston, 1963; Myers, 1981). None of 1982). these studies, however, recorded both insect herbivore The role of soil nitrogen in cactus population dynamics feeding and plant response to experimental manipulations is also not well understood. Nitrogen availability is gen- of resources~such as water and-light. erally low in arid and semiarid environments, and it is The aim of
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