Resource Choice in Cuscuta Europaea (Plant Dlstbn/Nduar Autonomy/Donal Plants/Parsl Plants/Bost Dhice) COLLEEN K
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Proc. Natd. Acad. Sci. USA Vol. 89, pp. 12194-12197, December 1992 Ecology Resource choice in Cuscuta europaea (plant dlstbn/nduar autonomy/donal plants/parsl plants/bost dhice) COLLEEN K. KELLY* Edward Grey Institute, University of Oxford, South Parks Road, Oxford OX1 3PS, United Kingdom Communicated by Robert M. May, September 4, 1992 (receivedfor review June 30, 1992) ABSTRACT Individual stems with growing tps of dodder METHODS AND MATERIALS (Cuscuta europaea) were rnsplanted onto host plants (haw- thorn) of varying nt l statu. The p ite was more Dodder (Convolvulaceae) has no roots, only vestigial leaves, likely to coil on ("accept") hosts ofhih nutritional status and and does not photosynthesize. A stem of dodder infests its grow away from ("reject") hosts of poor qual. Dodder hosts by forming one or more loops about the host stem or leaf (a coiling bout), after which it sends pegs of absorptive exhibits this acc rejection respome befm taking up tissue (haustoria) into the host vascular system. Dodder any food from the host, so it is possible to dsole active possesses responses that may be used to effect rejection (Fig. choice from the passive effects of growth and m it. 1) and acceptance of resources. These responses are com- Probability of acceptance is gauged to expected reward. plete prior to any resource uptake and thus cannot be confused with the passive results of uptake (16). Higher plants vary in size and shape through variation in Hawthorn (Crataegus monogyna) is a native host of this number or morphology ofthe repeating subunits (modules) of dodder in Great Britain (26). Six hundred 45-cm rooted which they are composed (1-3). Differences among modules cuttings of a single hawthorn genotype were grown for 8 have primarily been assumed by population biologists to be months in John Innes compost no. 2 at Wytham Research the result of changes in growth dictated by changes in local Station (Oxon, U.K.). In July 1989, the roots were cleaned of resource uptake (e.g., refs. 4-7), although physiological potting material and the plants were repotted in 20-cm plastic studies show that plants can make qualitative changes in pots with John Innes silver sand, a non-nutritive, non- gross morphology in response to local resource conditions retentive potting medium. Forty-eight similar-sized plants that could be adaptive (e.g., refs. 8-12). Such changes could were selected for the experiments and removed to a small execute plant "choice": the acceptance or rejection of a glasshouse. In late February 1990 the glasshouse plants were some value placed on a regime of deionized water to exhaust any resource type or patch based on criteria of patch internally stored resources, so that subsequent growth would to the choosing plant. depend only on regulated nutrient supplements. One month Rejection of a resource in the absence of an alternative later the plants were randomly divided into four groups of 12 would indicate that a plant may strategically take the risk of each, and each group was subjected to a different nutrient forfeiting resources for the chance of acquiring better re- treatment. The nutrient treatments constituted a serial dilu- sources later, thus altering resource acquisition patterns. tion of a balanced, complete nutrient solution (27) supplying Resource choice could also determine entry of a plant into a 15, 7.5, 3.75, and 1.87 mM nitrogen (N) per week. The resource patch and in this way contribute to the notoriously treatment levels were chosen to span the range of possible variable size and shape of plants (13-15), traits that have host values. the full-strength treatment was only slightly less direct and indirect consequences for plant fitness through than that which induced leaf-burn in the host, and the lowest their effects on competition, herbivory, and seed set (16-22). treatment level produced only minimal amounts of host Additionally, choice combined with differential mortality of growth. It was expected either that dodder would show a 0-1 plant parts may affect the distribution of a population among response, in which at some point in the range of host values, resources. dodder would switch from rejecting hosts to accepting hosts However, previous demonstrations ofthe qualitative mor- (23), or that dodder would exhibit what are termed partial phological changes that plant choice would entail have been preferences, where host acceptance would rise with increas- based on contrasts between high and low values ofa nutrient ing host value (28). or condition (e.g., refs. 8-12), thus allowing no more than the Hawthorn growth was recorded at 10-day intervals from conclusion that plants do different things in different envi- the beginning ofnutrient applications. Growth was calculated It to determine under a two-valued as change in volume on a branch-by-branch basis for all ronments. is not possible main more than 0.5 cm branches are the branches (and stem) long; system whether the observed responses right (adap- and stem were assumed to be cylinders. Because primary tive) things to do with regard to those particular levels of meristems had been removed, there was no growth in main- treatment. In order to demonstrate that plants can make stem length during the course of the experiment. Main-stem adaptive choices among resources, this study uses four levels length did not differ among treatments (F3,47 = 0.143, P = of treatment and draws upon the same cost-benefit criteria 0.9336), and overall average length from soil surface to tip that have been applied to resource choice in animals (23-25). was 32.9 ± 1.83 cm (mean SE). I show here in experiments with the clonal parasitic plant Parasite stems collected from a single naturally occurring dodder (Cuscuta europaea) an unequivocal demonstration parasite were transplanted onto the nutrient-regulated hosts that plants are able to make qualitative morphological on two separate runs, 7 July and 11 July. Transplants were changes gauged to the level of expected gain from the performed after the host plants showed significant differ- resource. ences among nutrient treatments in individual growth for two measurement periods (ANOVA; F3,47 = 2.98, P = 0.04 for The publication costs ofthis article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" *Present address: Department of Biological Sciences, P.O. Box in accordance with 18 U.S.C. §1734 solely to indicate this fact. 5218, University of North Texas, Denton, TX 76203-5218. 12194 Downloaded by guest on September 26, 2021 Ecology: Kelly Proc. Natl. Acad. Sci. USA 89 (1992) 12195 FIG. 1. Parasite rejection response. A transplanted parasite stem tied parallel to a host branch may reject a host by turning at right angles to the host plant and elongating in a trajectory directly away from the host. This response is complete within -3 daylight hours afterinitial contact between host and parasite. There is a 30-min interval between the first 2 exposures, and 20-min intervals between subsequent exposures. measurement period 8; F3,47 = 3.93, P = 0.01 for measure- parasite response after host treatment category had been ment period 9). Transplantation consisted of trimming each entered into the model, but if percent N was added to the parasite stem to 15 cm in the morning, recording the diameter analysis prior to host treatment category, the latter had no of the parasite stem at its base, and placing the stem in a significant effect. Parasite stem diameter did not affect host water-filled plastic test tube taped to the target host. Test acceptance by dodder (Table 2). All conclusions held regard- tubes were positioned so that the growing tip of the parasite less oforder ofentry ofthe variables (x2 = 0.64 when parasite stem could be tied to the newest tissue on the host. Only one stem diameter was entered into the model first), other than parasite stem was transplanted to each host at a time, that noted above. There was no significant difference be- allowing 96 replicates overall for the 2 runs ofthe experiment. tween the two runs ofthe experiment in parasite response (2 The experiment was considered complete when 95% of the = 1.72, P > 0.1). parasite stems had either rejected or accepted their hosts. The two stems that did not respond (i.e., did not show active rejection) were coded into the analysis as having accepted the DISCUSSION host. After the second run, the host sections with which the Arguments for non-seed choice by plants have relied upon parasite stems had come in contact were collected and observations of directional growth along a resource gradient assayed for concentration of Kjeldahl-determined total or- (5) or the previously mentioned differences between re- ganic N (29), as an indicator of host metabolic status. sponses to two treatment levels (e.g., refs. 8-12). Gradient- Data were analyzed by fitting a logistic regression using a oriented growth can show only that a plant will utilize generalized linear model, assuming a binomial distribution of available resources; two-value tests can demonstrate no the dependent variable (30). The independent variables were more than that plants do different things under different experimental run, nutrient application level, percent host stem nitrogen, and parasite stem diameter. Table 1. Summary of raw data No. of stems No. of stems Average RESULTS Treatment accepting hosts rejecting hosts N content Dodder was more likely to accept a host that had received 1.87 mM N 9 15 0.727 higher nutrient supplements (Tables 1 and 2). The parasite 3.75 mM N 10 14 0.749 was able to distinguish differences within as well as among 7.5 mM N 14 10 0.7% host nutrient categories: individual measures of host nutrient 15 mM N 19 5 0.983 status (percent N) accounted for significant variation in Each host plant received 1 liter of treatment solution per week.